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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title>Frontiers in Plant Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Plant Sci.</abbrev-journal-title>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fpls.2023.1219673</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Field phenotyping for African crops: overview and perspectives</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Cudjoe</surname>
<given-names>Daniel K.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1665912"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Virlet</surname>
<given-names>Nicolas</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/381183"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Castle</surname>
<given-names>March</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2507997"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Riche</surname>
<given-names>Andrew B.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1020284"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mhada</surname>
<given-names>Manal</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1117754"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Waine</surname>
<given-names>Toby W.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Mohareb</surname>
<given-names>Fady</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/59244"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Hawkesford</surname>
<given-names>Malcolm J.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/26032"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Sustainable Soils and Crops, Rothamsted Research</institution>, <addr-line>Harpenden</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>School of Water, Energy and Environment, Cranfield University</institution>, <addr-line>Cranfield, Bedfordshire</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>AgroBiosciences Department, Mohammed VI Polytechnic University (UM6P)</institution>, <addr-line>Bengu&#xe9;rir</addr-line>, <country>Morocco</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Bo Li, Syngenta, United Kingdom</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Chenglong Huang, Huazhong Agricultural University, China; Jun Liu, Shandong Provincial University Laboratory for Protected Horticulture, China</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Malcolm J. Hawkesford, <email xlink:href="mailto:malcolm.hawkesford@rothamsted.ac.uk">malcolm.hawkesford@rothamsted.ac.uk</email>; Toby W. Waine, <email xlink:href="mailto:t.w.waine@cranfield.ac.uk">t.w.waine@cranfield.ac.uk</email>; Fady Mohareb, <email xlink:href="mailto:f.mohareb@cranfield.ac.uk">f.mohareb@cranfield.ac.uk</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>04</day>
<month>10</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>14</volume>
<elocation-id>1219673</elocation-id>
<history>
<date date-type="received">
<day>09</day>
<month>05</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>07</day>
<month>09</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2023 Cudjoe, Virlet, Castle, Riche, Mhada, Waine, Mohareb and Hawkesford</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Cudjoe, Virlet, Castle, Riche, Mhada, Waine, Mohareb and Hawkesford</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>Improvements in crop productivity are required to meet the dietary demands of the rapidly-increasing African population. The development of key staple crop cultivars that are high-yielding and resilient to biotic and abiotic stresses is essential. To contribute to this objective, high-throughput plant phenotyping approaches are important enablers for the African plant science community to measure complex quantitative phenotypes and to establish the genetic basis of agriculturally relevant traits. These advances will facilitate the screening of germplasm for optimum performance and adaptation to low-input agriculture and resource-constrained environments. Increasing the capacity to investigate plant function and structure through non-invasive technologies is an effective strategy to aid plant breeding and additionally may contribute to precision agriculture. However, despite the significant global advances in basic knowledge and sensor technology for plant phenotyping, Africa still lags behind in the development and implementation of these systems due to several practical, financial, geographical and political barriers. Currently, field phenotyping is mostly carried out by manual methods that are prone to error, costly, labor-intensive and may come with adverse economic implications. Therefore, improvements in advanced field phenotyping capabilities and appropriate implementation are key factors for success in modern breeding and agricultural monitoring. In this review, we provide an overview of the current state of field phenotyping and the challenges limiting its implementation in some African countries. We suggest that the lack of appropriate field phenotyping infrastructures is impeding the development of improved crop cultivars and will have a detrimental impact on the agricultural sector and on food security. We highlight the prospects for integrating emerging and advanced low-cost phenotyping technologies into breeding protocols and characterizing crop responses to environmental challenges in field experimentation. Finally, we explore strategies for overcoming the barriers and maximizing the full potential of emerging field phenotyping technologies in African agriculture. This review paper will open new windows and provide new perspectives for breeders and the entire plant science community in Africa.</p>
</abstract>
<kwd-group>
<kwd>African crops</kwd>
<kwd>phenotypes</kwd>
<kwd>field phenotyping</kwd>
<kwd>high-throughput phenotyping</kwd>
<kwd>phenotyping infrastructures</kwd>
<kwd>low-cost phenotyping</kwd>
<kwd>African agriculture</kwd>
<kwd>precision agriculture</kwd>
</kwd-group>
<contract-sponsor id="cn001">OCP Group<named-content content-type="fundref-id">10.13039/501100022668</named-content>
</contract-sponsor>
<contract-sponsor id="cn002">Biotechnology and Biological Sciences Research Council<named-content content-type="fundref-id">10.13039/501100000268</named-content>
</contract-sponsor>
<counts>
<fig-count count="3"/>
<table-count count="3"/>
<equation-count count="0"/>
<ref-count count="256"/>
<page-count count="23"/>
<word-count count="13260"/>
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<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Technical Advances in Plant Science]</meta-value>
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</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<p>The global demand for food is projected to increase in the coming decades, driven by population growth, climate change, pandemics, shifts in food consumption and biofuel use (<xref ref-type="bibr" rid="B237">Tilman et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B109">Godfray and Robinson, 2015</xref>; <xref ref-type="bibr" rid="B1000">van Dijk et&#xa0;al., 2021</xref>). Ensuring that crop production is sufficient to meet future goals is a challenge for plant and agricultural sciences.</p>
<p>In Africa, agricultural crops provide food and income for smallholder farmers and consumers. Despite the huge agricultural potential, agricultural productivity in African countries continues to remain the lowest in the world (<xref ref-type="bibr" rid="B34">Bjornlund et&#xa0;al., 2020</xref>). Many studies have indicated that yields of several important staple crops may be stagnating or even declining across the continent (<xref ref-type="bibr" rid="B207">Roudier et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B143">Knox et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B200">Ray et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B183">Parkes et&#xa0;al., 2018</xref>). This is the case for key staple crops such as maize, rice, wheat, millet, sorghum, cowpea, cassava and yam, which together account for a large portion of the population&#x2019;s diet. Therefore, food supply&#xa0;systems would be negatively affected if yield gains in these crops continue to slow due to environmental stresses and production constraints.</p>
<p>Addressing food security in Africa is a vast challenge that needs to be tackled in many complementary directions. Infrastructure development adapted to local needs, good farming practices, management, and political will are some of the major axes of development for food security. Improving crop performance and tolerance/resistance to biotic and abiotic conditions is the challenge facing the scientific community and innovative methods are needed.</p>
<p>Advanced field phenotyping, e.g. using digital approaches, has developed substantially over the past decade and provides means for real-time monitoring of response to environmental stresses and nutrition, and aids unravelling the relationships between yield and complex genotypic traits. The identification of genotypes with superior traits of agricultural interest remains one of the major targets for the genetic improvement of crops (<xref ref-type="bibr" rid="B241">Varshney et&#xa0;al., 2021</xref>).</p>
<p>The genomes of many agricultural crops such as rice (<xref ref-type="bibr" rid="B160">Matsumoto et&#xa0;al., 2005</xref>), sorghum (<xref ref-type="bibr" rid="B186">Paterson et&#xa0;al., 2009</xref>), maize (<xref ref-type="bibr" rid="B218">Schnable et&#xa0;al., 2009</xref>), soybean (<xref ref-type="bibr" rid="B217">Schmutz et&#xa0;al., 2010</xref>) and recently wheat (<xref ref-type="bibr" rid="B14">Appels et&#xa0;al., 2018</xref>) have been sequenced. However, the advances made in genomic approaches such as maker-assisted selection and high-throughput sequencing (<xref ref-type="bibr" rid="B66">Crossa et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B215">Scheben et&#xa0;al., 2018</xref>) are yet to be complemented with accurate field phenotyping methods (<xref ref-type="bibr" rid="B164">Minervini et&#xa0;al., 2015</xref>). Most of the traits of agronomic relevance (e.g., yield) are complex, and quantitative, requiring tools for their phenotypic assessment in the field (<xref ref-type="bibr" rid="B203">Reynolds et&#xa0;al., 2020</xref>). Furthermore, open field rather than controlled environment measurements are more likely to be useful in identifying genotypes that will perform better in farming practice, especially when large plots that mimic real farm conditions (i.e., environmental and management conditions) are employed (<xref ref-type="bibr" rid="B201">Rebetzke et&#xa0;al., 2014</xref>).</p>
<p>In addition, precision agriculture (PA) is becoming increasingly important in today&#x2019;s technologically advanced world (<xref ref-type="bibr" rid="B149">Langemeier and Boehlje, 2021</xref>; <xref ref-type="bibr" rid="B108">Gobezie and Biswas, 2023</xref>) and PA remains one of the cardinal principles of field phenotyping. The PA farming management concept relies on modern digital techniques to monitor and optimize agricultural production processes to improve crop performance (<xref ref-type="bibr" rid="B121">Hedley, 2015</xref>; <xref ref-type="bibr" rid="B110">Gokool et&#xa0;al., 2023</xref>). Despite PA&#x2019;s contributions to sustainable agriculture, its use in resource-constrained smallholder farming environments, particularly in Sub-Saharan Africa (SSA), has been very limited (<xref ref-type="bibr" rid="B108">Gobezie and Biswas, 2023</xref>). Recent developments in sensor technologies, machine vision, and higher-resolution digital cameras, in tandem with advanced data processing power and other portable tools have paved the way for high-throughput plant phenotyping in the field to benefit crop breeding programs (<xref ref-type="bibr" rid="B73">Deery et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B267">Zhang et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B17">Araus et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B9">Ahmed et&#xa0;al., 2023</xref>). From the field phenotyping perspective, these emerging technologies are enabling automated intensive data collection and increasing the ability to investigate plant function and structure through non-invasive methods with high accuracy. Such field phenotyping methods will aid crop improvement efforts to meet the expected demand for food and agricultural products in the future.</p>
<p>The development and application of these high-throughput tools for field phenotyping are currently focused on the main staple crops grown in the most developed agricultural regions. Over the decades, breeders and agronomists in Africa have used traditional phenotyping based on manual methods either for selecting traits or for improving yields through changes in agronomic practices (<xref ref-type="bibr" rid="B128">Iizumi and Sakai, 2020</xref>). However, traditional phenotyping in breeding is time-consuming, laborious and data collection is insufficient to fulfil the needs of plant breeders which impedes breeding progress. Therefore, further advances in phenotyping methods and appropriate implementation are required to increase the effectiveness of selection in breeding programs, speed up genetic gains, reduce costs and enable monitoring of plant status more efficiently than is currently feasible. The sophistication and cost of current plant phenotyping equipment (<xref ref-type="bibr" rid="B202">Reynolds et&#xa0;al., 2019</xref>) have restricted them from being widely applied in the developing world and especially in Africa. Additionally, insufficient technical, operational, regulatory restrictions and conceptual capacity in the plant science community have further limited implementation. Therefore, it is timely to begin to apply these technologies more widely, both geographically and with respect to target crops in Africa. Affordable high-throughput phenotyping aims to achieve reasonably priced solutions for all the components comprising the phenotyping pipeline which will promote their adoption for the breeding of African crops (<xref ref-type="bibr" rid="B250">Whalen and Yuhas, 2019</xref>; <xref ref-type="bibr" rid="B37">Bongomin et&#xa0;al., 2022</xref>).</p>
<p>Few studies have covered the use of modern field phenotyping approaches employing remote sensing in Africa (e.g., <xref ref-type="bibr" rid="B170">Mutanga et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B57">Chivasa et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B45">Buchaillot et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B37">Bongomin et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B136">Kassim et&#xa0;al., 2022</xref>). For instance, <xref ref-type="bibr" rid="B37">Bongomin et&#xa0;al. (2022)</xref> recently reviewed the status of field phenotyping in Uganda with focus on the application of drones and image analytics.</p>
<p>In this review, we provide a background on African agriculture and cover the concept of digital field phenotyping, focused on traits that may be measured by emerging technologies and which could be applicable to African crops. The current developments of field phenotyping in Africa, including initiatives, implementation challenges and prospects are comprehensively reviewed. We observed that the lack of suitable field phenotyping infrastructures and approaches using digital technologies is limiting the development of improved crop cultivars and will negatively affect the agricultural industry and food security in Africa. We emphasize the potential for incorporating cutting-edge, low-cost phenotyping tools (i.e., portable field sensors, UAVs) into breeding schemes and for identifying agricultural crop responses to environmental constraints through field experimentation. Finally, we consider policy directions for tackling the implementation challenges (i.e., practical, financial, geographical and political) of digital field phenotyping and realizing the full potential of available field phenotyping resources (i.e., technologies, tools and know-how) appropriate for African crops.</p>
</sec>
<sec id="s2">
<label>2</label>
<title>African crops and the challenges to production</title>
<p>African countries are important producers of major crops with diverse agro-climatic and ecological conditions, and cultural diversity (<xref ref-type="bibr" rid="B150">Leakey et&#xa0;al., 2022</xref>). Sub-Saharan West Africa is composed of a wide variety of ecosystems and an equally high number of production systems (<ext-link ext-link-type="uri" xlink:href="https://www.fao.org/3/AC349E/ac349e04.htm">https://www.fao.org/3/AC349E/ac349e04.htm</ext-link>). Generally, crop production is concentrated in areas with a favourable combination of agro-bioclimatic conditions. In the Sahelian zone, cereals such as millet and sorghum are the predominant crops with annual rainfall (200-600&#xa0;mm), transitioning to maize, groundnuts and cowpeas farther south in the Sudanian savannah zone (the so-called &#x201c;Middle Belt&#x201d;). These food crops are among the top five harvested crops in the Sahelian countries &#x2013; Burkina Faso, Senegal, Mauritania, Mali, Chad and Niger. According to <xref ref-type="bibr" rid="B91">FAOSTAT (2018a)</xref> data, maize is the major essential staple food in sub-Saharan Africa, accounting for nearly 20% of total calorie intake. The same source indicates that in Sub-Saharan West Africa, millet and sorghum account for roughly 64% of total cereal production. Across the rainy forests of the Guinean zone (1200-2200&#xa0;mm of rainfall per year) crops are predominantly root and tuber crops such as cassava and yams which are mostly cultivated in Ghana, Nigeria, C&#xf4;te d&#x2019;Ivoire and Sierra Leone. Yam is the second most important crop in Africa in terms of production after cassava (<xref ref-type="bibr" rid="B91">FAOSTAT, 2018a</xref>). Rice, on the other hand, is one of the most widely harvested crops in this humid zone, ranking first in Guinea, Liberia and Sierra Leone in terms of area harvested (<xref ref-type="bibr" rid="B228">Soullier et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B77">Duvallet et&#xa0;al., 2021</xref>).</p>
<p>Crop production in West Africa is mostly rainfed and crop production is vulnerable to climate change, which manifests itself in unpredictably high temperatures and erratic rainfall patterns (<xref ref-type="bibr" rid="B229">Sultan and Gaetani, 2016</xref>; <xref ref-type="bibr" rid="B7">Affoh et&#xa0;al., 2022</xref>). The five principal crops in West Africa in terms of harvested area (in millions of hectares per year on average in the last decade) are cassava (81), maize (19), millet (10), sorghum (12), yam (57) (<xref ref-type="bibr" rid="B1001">FAOSTAT, 2022</xref>). Major cash crops are cocoa, coffee and cotton. Declining soil fertility and unpredictable climate change impacts (among other factors) have made it difficult to maintain the yields of these major crops (<xref ref-type="bibr" rid="B222">Shimeles et&#xa0;al., 2018</xref>). Over the last three decades, the agricultural sector in West Africa has been characterized by strong production growth in some major staple crops culminating in increased production volumes for both domestic and export markets (<xref ref-type="bibr" rid="B36">Blein et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B89">FAO, 2015</xref>). Similarly to West Africa, Central Africa&#x2019;s principal food crops include cassava, peanuts, sorghum, millet, maize, sesame and plantains. Additionally major cash crops for export include cotton, coffee and tobacco (<xref ref-type="bibr" rid="B175">Ochieng et&#xa0;al., 2020</xref>).</p>
<p>In Northern Africa, particularly Morocco, crop production is regionally diverse owing to different climatic conditions, agro-ecological zones, land-crop tenure and farming systems (<xref ref-type="bibr" rid="B179">Ouraich and Tyner, 2018</xref>). This geographical diversity results in varied agriculture, with crops ranging from cereals and vegetables to fruits and nuts, grains, legumes, etc., that contribute significantly towards the country&#x2019;s agricultural sustainability and food security. Cereal production accounts for 65% of cultivable agricultural areas (<xref ref-type="bibr" rid="B179">Ouraich and Tyner, 2018</xref>). Most cereal production occurs under rainfed conditions. As a result, productivity performance is influenced by precipitation levels. For instance, 7.3 million tonnes of wheat were produced in 2018 making it the 20th largest producer in the world and 2.8 million tonnes of barley being the 15th largest producer in the world (<xref ref-type="bibr" rid="B92">FAOSTAT, 2018b</xref>). However, drought is a persistent threat to crop production especially the lowlands where cereals are grown are particularly at risk because of the wide variations in annual precipitation (<xref ref-type="bibr" rid="B243">Verner et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B162">Meliho et&#xa0;al., 2020</xref>). In recent years, quinoa has sparked particular attention in Morocco (<xref ref-type="bibr" rid="B59">Choukr-Allah et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B123">Hirich et&#xa0;al., 2021</xref>). It remains one of the most nutrient-dense crops and is recognized as a &#x2018;Superf Food&#x2019; due to its nutritional benefits. Thus, Morocco is one of the few North African countries capable of achieving self-sufficiency in food production (<xref ref-type="bibr" rid="B210">Saidi and Diouri, 2017</xref>).</p>
<p>Grains and cereals (e.g., maize, wheat, barley, oats and sorghum) are South Africa&#x2019;s most important crops occupying more than 60% of the acreage under cultivation (<xref ref-type="bibr" rid="B87">FAO, 2022</xref>). Together, these crops account for one of the largest agricultural industries contributing more than 30% to the total gross value of agricultural production (<xref ref-type="bibr" rid="B87">FAO, 2022</xref>). Maize, the country&#x2019;s most important crop and largest locally produced field crop, is a dietary staple supplying most of the carbohydrate needs, a source of livestock feed and is an export crop (<xref ref-type="bibr" rid="B84">Epule et&#xa0;al., 2022</xref>).</p>
<p>The country has emerged as the largest maize producer and exporter in the Southern African Development Community (SADC) region and Africa as a whole (<xref ref-type="bibr" rid="B97">Fisher et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B87">FAO, 2022</xref>). According to the <xref ref-type="bibr" rid="B87">FAO, 2022</xref>, in 2021 South Africa produced 17 million metric tonnes of maize, making it the 9th largest producer in the world. Moreover, it produced 2.6 million metric tonnes of potato and 2.3 million metric tonnes of wheat. Largely, South Africa has a semi-arid climate characterized by summer and winter rainfall seasons. Unpredictable weather conditions due to climate change have a severe impact on maize and wheat production which accounts for more than 36% of the total value of field crops (<xref ref-type="bibr" rid="B41">Bradshaw et&#xa0;al., 2022</xref>).</p>
<p>Smallholder farmers dominate agriculture in East African countries, contributing up to 90% of total agricultural production (<xref ref-type="bibr" rid="B211">Salami et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B154">Livingston et&#xa0;al., 2011</xref>). A cereal&#x2010;legume mixed cropping pattern is the dominant system that includes maize, millet, sorghum and wheat (<xref ref-type="bibr" rid="B239">Van Duivenbooden et&#xa0;al., 2000</xref>). Over 40% of the region is covered by the maize mixed cropping system, which is followed by the pastoral (14%), root crop (12%) and cereal-root crop mixed system (11%) (<xref ref-type="bibr" rid="B6">Adhikari et&#xa0;al., 2015</xref>). Teff is a significant crop in the Ethiopian highlands, while other significant crops in the area include cassava, bananas and rice. The mixed cropping system in East Africa is based on millet in the drier regions and on maize and cassava in the humid regions (<xref ref-type="bibr" rid="B6">Adhikari et&#xa0;al., 2015</xref>). The main cash crops in most of the East African countries in SSA are coffee, tea, cotton, tobacco and sugarcane. Rainfall variability negatively impact on crop production in East African countries (<xref ref-type="bibr" rid="B181">Palmer et&#xa0;al., 2023</xref>). Generally, the major challenges to crop production in Africa are unproductive soils, pests and diseases, drought, and poor crop management (<xref ref-type="bibr" rid="B231">Tadele, 2017</xref>). The distribution of major crops in each sub-region except Northern Africa is summarized in <xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Major crop distribution in Sub-Saharan African region based on average production values between 2011-13. Adapted from <xref ref-type="bibr" rid="B1002">FAOSTAT (2016)</xref>. FAO, <ext-link ext-link-type="uri" xlink:href="http://faostat3.fao.org/">http://faostat3.fao.org/</ext-link>.
</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-14-1219673-g001.tif"/>
</fig>
</sec>
<sec id="s3">
<label>3</label>
<title>Digital and image-based field phenotyping</title>
<p>Experiments with repeated trials in diverse environments are often necessary to screen plants for desirable traits. This becomes problematic when there is the need to screen a large panel of genotypes for valuable traits (i.e., yield potential or abiotic and biotic stress tolerance) to assess genotype, environment, and management (G &#xd7; E&#xd7; M) interactions (<xref ref-type="bibr" rid="B15">Araus and Cairns, 2014</xref>). Over the years, the measurement of individual plants in controlled conditions has dominated most of the phenotyping research. However, controlled environments often do not accurately mimic plant growth and development in field conditions (<xref ref-type="bibr" rid="B252">White et&#xa0;al., 2012</xref>). Field phenotyping is becoming more widely recognized as the approach that gives the most accurate representation of traits in real-world cropping systems (<xref ref-type="bibr" rid="B233">Tariq et&#xa0;al., 2020</xref>). Thus, field phenotyping is an important component of crop improvement to assess how the genotype, the environment, and their interaction (G &#xd7; E) influence quantitative traits in a complex and dynamic manner (<xref ref-type="bibr" rid="B96">Fiorani and Schurr, 2013</xref>; <xref ref-type="bibr" rid="B15">Araus and Cairns, 2014</xref>; <xref ref-type="bibr" rid="B172">Neilson et&#xa0;al., 2015</xref>). Furthermore, field phenotyping is employed to discover novel traits, identify new germplasm carrying relevant but complex traits for breeding, and for testing proof of concept to validate traits (<xref ref-type="bibr" rid="B248">Watt et&#xa0;al., 2020</xref>). Traditionally, destructive sampling has been used to quantify certain observable plant traits, including laboratory analysis to characterize phenotypes based on their genetic and physiological functions. Digital phenotyping approaches seek to reduce this need (<xref ref-type="bibr" rid="B238">Tripodi et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B244">Virlet et&#xa0;al., 2022</xref>).</p>
<p>Different measurement approaches including novel technologies such as non-invasive imaging, robotics and sensor positioning systems have been incorporated in well-designed field phenotyping installations for high-throughput phenotyping (e.g., <xref ref-type="bibr" rid="B15">Araus and Cairns, 2014</xref>; <xref ref-type="bibr" rid="B142">Kirchgessner et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B220">Shakoor et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B245">Virlet et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B190">Pieruschka and Schurr, 2022</xref>). These significant strides in field phenotyping have fostered a major international collaborative effort directed toward data and protocol standardization (<xref ref-type="bibr" rid="B191">Pieruschka and Schurr, 2019</xref>; <xref ref-type="bibr" rid="B156">Lorence and Jimenez, 2022</xref>). The appeal of these platforms is the increased throughput and objectivity in data collection compared to traditional field approaches.</p>
<p>Non-invasive portable devices, ground-wheeled, motorized gantry scanalyzer systems, agricultural robots and aerial vehicles that deploy a wide range of cameras and sensors, together with high-performance computing are currently required to conduct field phenotyping in a timely and economical manner (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). Together, these platforms are able to phenotype plant characteristics throughout the season in field environments (<xref ref-type="bibr" rid="B252">White et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B99">Fritsche-Neto and Bor&#xe9;m, 2015</xref>; <xref ref-type="bibr" rid="B135">Jimenez-Berni et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B102">Furbank et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B151">Li et&#xa0;al., 2021</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Overview of the most common field phenotyping systems and approaches at proximal and remote sensing scales. The proximal sensing approach is based on ground-based platforms such as handheld spectrometers, hand-pushed carts equipped with sensors, tractor-based platforms fitted with multiple cameras and gantry scanalyzer systems that collect spectral information of crops in close range or contact. On the other hand, the remote sensing technique is based on aerial platforms including unmanned aerial vehicles (i.e., drones), manned aircraft and satellites that acquire spectral imagery of crops without making physical contact but at a distance. <xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref> was modified from (<xref ref-type="bibr" rid="B192">Pineda et&#xa0;al., 2021</xref>).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-14-1219673-g002.tif"/>
</fig>
<p>In recent years, manned and unmanned aerial vehicle (UAV) remote sensing platforms have emerged as convenient high-throughput tools for field phenotyping (<xref ref-type="bibr" rid="B180">Pajares, 2015</xref>; <xref ref-type="bibr" rid="B221">Shi et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B93">Feng et&#xa0;al., 2021</xref>). These remote sensing approaches, particularly UAVs enable quick and non-destructive high throughput phenotyping, with the benefit of adaptable and convenient operation (<xref ref-type="bibr" rid="B258">Yang et&#xa0;al., 2017a</xref>). These phenotyping platforms can combine multiple sensors such as digital cameras, infrared thermal imagers, light detection and ranging (LiDAR), multispectral cameras and hyperspectral sensors for various assessments of morphological and physiological plant traits (<xref ref-type="bibr" rid="B111">Gonzalez-Dugo et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B258">Yang et&#xa0;al., 2017a</xref>; <xref ref-type="bibr" rid="B50">Camino et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B205">Roitsch et&#xa0;al., 2019</xref>).</p>
<p>Alternatively, field phenotyping can be accomplished on the ground utilizing a fully automated fixed-site phenotyping platform (e.g., <xref ref-type="bibr" rid="B142">Kirchgessner et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B245">Virlet et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B26">Bai et&#xa0;al., 2019</xref>), hand-held sensors, portable spectroradiometers, hand-pushed carts or high-clearance tractors carrying multiple high-resolution sensors to measure phenotypic features non-destructively (<xref ref-type="bibr" rid="B60">Comar et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B12">Andrade-Sanchez et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B65">Crain et&#xa0;al., 2016</xref>). The use of rapid non-invasive portable devices that carry sensors for crop status monitoring has advanced field data collection due to their applicability and ease of operation (<xref ref-type="bibr" rid="B184">Parks et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B259">Yang et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B61">Condorelli et&#xa0;al., 2018</xref>). Recently, field phenotyping has become more flexible by integrating ground-based and aerial platforms (<xref ref-type="bibr" rid="B194">Potgieter et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B102">Furbank et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B173">Ninomiya, 2022</xref>). <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref> summarizes the diverse ground-based and aerial field phenotyping platforms, their applications, advantages, and limitations.</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Applications and limitations of field phenotyping platforms.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Phenotyping platform</th>
<th valign="top" align="left">Examples</th>
<th valign="top" align="left">Applications</th>
<th valign="top" align="left">Advantages</th>
<th valign="top" align="left">Limitations</th>
<th valign="top" align="left">References</th>
</tr>
</thead>
<tbody>
<tr>
<th valign="top" colspan="6" align="left">Ground-based platforms</th>
</tr>
<tr>
<td valign="top" align="left">Fixed-site systems</td>
<td valign="top" align="left">Field scanalyzers (i.e Rothamsted field scanalyzer, Maricopa field scanalyzer)</td>
<td valign="top" align="left">Ground cover, canopy height, plant<break/>geometry, growth, growth stages,<break/>vegetation indices, chlorophyll<break/>fluorescence parameters</td>
<td valign="top" align="left">Unmanned continuous operation with good repeatability, deploy a wide range of sensors, fully automated. Not limited by soil conditions</td>
<td valign="top" align="left">Expensive, monitor a limited number of plots, limited by weather conditions</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B245">Virlet et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B1003">Burnette et&#xa0;al., 2018</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Permanent platforms based on a cable-suspended multi-sensor system</td>
<td valign="top" align="left">The ETH field phenotyping platform, the University of Nebraska phenotyping system</td>
<td valign="top" align="left">Monitor canopy cover, canopy height, and traits related to thermal and multi-spectral imaging with selected examples from winter wheat, maize, and soybean</td>
<td valign="top" align="left">Produce precise, high-resolution images, deploy a wide range of sensors, fully automated</td>
<td valign="top" align="left">Monitor a limited area of crop, difficult to move, expensive, and limited by weather conditions</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B142">Kirchgessner et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B26">Bai et&#xa0;al., 2019</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Handheld sensors</td>
<td valign="top" align="left">Point spectroradiometers, thermal sensors, chlorophyll meters, imagers</td>
<td valign="top" align="left">Estimate chlorophyll fluorescence, canopy temperature, nitrogen status, leaf area, plant height, yield</td>
<td valign="top" align="left">Ground truth reference to validate aerial measurements (UAVs) and airplanes, low-cost and easy to use</td>
<td valign="top" align="left">Labour intensive and time-consuming, limited plot coverage, measurement bias</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B259">Yang et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B13">Andrianto et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B105">Garriga et&#xa0;al., 2017</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">In-field mobile platforms</td>
<td valign="top" align="left">Phenocart, proximal sensing cart, phenomobiles, manned buggies</td>
<td valign="top" align="left">Estimate biomass, leaf area index, counting plants, plant height, early vigour, and plant maturity</td>
<td valign="top" align="left">Manually operated, low-cost, easier to construct, multiple traits evaluations, deploy<break/>more sensors, flexibility with payload and view angle geometry; very adaptable</td>
<td valign="top" align="left">The motorized platforms are costly to construct and run, need technical expertise, hard operation for large-scale experiments. Limited by weather and soil conditions</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B251">White and Conley, 2013</xref>; <xref ref-type="bibr" rid="B12">Andrade-Sanchez et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B73">Deery et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B65">Crain et&#xa0;al., 2016</xref>
</td>
</tr>
<tr>
<th valign="top" colspan="6" align="left">Aerial platforms</th>
</tr>
<tr>
<td valign="top" align="left">Unmanned aerial vehicles (UAVs)</td>
<td valign="top" align="left">Broadly classified into Rotocopters, fixed<break/>wing systems, parachutes, and blimps</td>
<td valign="top" align="left">Traits such as canopy cover, canopy height, crop lodging, growth indices, and canopy temperature can be estimated from the imagery</td>
<td valign="top" align="left">Rotocopters (i.e drones) can deploy a wide range of sensors, including thermal, multispectral, and hyperspectral cameras, high hovering capabilities, better flight time</td>
<td valign="top" align="left">Lower speeds for image stitching, lens distortion, and overlap of the acquired images can affect orthomosaic, battery use and flying time may be limited by the payload, and operability is limited in windy, wet, dull, variable light, or cold conditions</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B212">Sankaran et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B55">Chawade et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B124">Holman, 2020</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Satellite imaging</td>
<td valign="top" align="left">Digital Globe WorldView-2 satellite, WorldView-3 satellite, RADARSAT-2</td>
<td valign="top" align="left">In precision agriculture for germplasm evaluation, multi-location yield trials, field observation of crop biophysical parameters, weather predictions</td>
<td valign="top" align="left">Evaluation of moderate to large-sized trial, multi-location evaluation; provides automated coverage of isolated field trials across a larger geographical area</td>
<td valign="top" align="left">Affected by weather conditions, resolution, frequency of imaging, takes a long time from image acquisition to access, costly, higher frequency of satellite revisits, cloud cover can<break/>interfere with imaging</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B234">Tattaris et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B263">Yang et&#xa0;al., 2017b</xref>; <xref ref-type="bibr" rid="B258">Yang, 2018</xref>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Modified from <xref ref-type="bibr" rid="B152">Li et&#xa0;al., 2014</xref> and <xref ref-type="bibr" rid="B73">Deery et&#xa0;al., 2014</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s4">
<label>4</label>
<title>Traits assessed by sensor platforms and their relevance for field phenotyping</title>
<p>For field phenotyping, traits that have been evaluated by sensors in the field have been reviewed recently by <xref ref-type="bibr" rid="B248">Watt et&#xa0;al. (2020)</xref> and include for example; (a) plant morphological development (i.e., including seed establishment and growth of the crop, the timing, and dynamics of flower and fruit development); (b) functional traits that are related to the photosynthetic capacity and carbon uptake during the phenological growth phase; (c) traits related to biotic and abiotic stress resistance/tolerance; (d) traits that determine crop water status (e.g., water uptake and transpiration and water-use efficiency) of plants; (e) yield-related traits and harvest quality of crops (i.e., biomass yield) and (f) the structural and functional root traits (i.e., root architecture). These traits have been previously classified into morphometric and physiological parameters (<xref ref-type="bibr" rid="B196">Qiu et&#xa0;al., 2018</xref>). Traits such as plant height, stem diameter, leaf area or leaf area index, leaf angle, stalk length and in-plant space are morphometric parameters. Physiological parameters include traits such as photosynthetic rate, chlorophyll content, water stress, leaf water content, biomass, and salt resistance, which together can impact plant growth. It should be emphasized that different phenotypic traits have specific time frames within the phenological cycle of the plant when they are relevant for the breeder and farmer. Currently, the most researched crops in field phenotyping are economic crops, such as wheat, maize, barley, sorghum, tomato, bean and grape because they have significant economic value for agricultural development. A challenge is to extend phenotyping into the vast range of African crops, some of which may be of only local importance.</p>
<p>Field phenotyping makes use of a variety of sensors due to the large number of phenotypic traits that must be measured. Several conventional and novel sensors such as digital cameras, range cameras, depth cameras, spectral sensors, lidar or laser sensors, thermal sensors, fluorescence sensors, multispectral cameras, hyperspectral cameras and others are employed and integrated for plant trait measurement in field phenotyping (<xref ref-type="bibr" rid="B196">Qiu et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B205">Roitsch et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B256">Xie and Yang, 2020</xref>).</p>
<p>Since plants develop rapidly during their early growth stages, frequent measurements during their establishment are a prerequisite for the quantitative selection of vigour phenotypes. Drones fitted with conventional RGB (red-green-blue) cameras, in combination with advanced image processing pipelines, can automatically detect crop stands (single plants) and determine seed emergence, germination rates and timing under extreme climatic events in the field (<xref ref-type="bibr" rid="B153">Liu et&#xa0;al., 2017</xref>).</p>
<p>Most plants display strong morphological changes during their phenological development, which is greatly influenced by the availability of resources and changes in abiotic and biotic factors. Therefore, the development of robust, automated, and precise methods to measure morphological plant traits in field conditions is still required (<xref ref-type="bibr" rid="B107">Gibbs et&#xa0;al., 2017</xref>).</p>
<p>The leaf is one of the important components of a plant. It plays a major role in plant growth given that its growing status influences the efficiency of the direct solar energy utilization by plants. Hence, it is a significant parameter in plant phenotyping. Measurements of morphometric parameters of the leaf and other canopy features (i.e., leaf area, stem height, number of tillers, and inflorescence architecture) have been evaluated using non-destructive multi-sensor approaches (<xref ref-type="bibr" rid="B48">Busemeyer et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B96">Fiorani and Schurr, 2013</xref>; <xref ref-type="bibr" rid="B199">Rahaman et&#xa0;al., 2015</xref>). However, the most frequently used geometric measure of plant canopy is the green leaf area index (GLAI), which relates the one-sided green leaf area per unit projected ground area (<xref ref-type="bibr" rid="B56">Chen and Black, 1992</xref>). For instance, UAV multispectral imagery has been used to characterize GLAI dynamics of a large maize panel under contrasted environmental conditions and thus holds great potential for yield predictions in breeding programs (<xref ref-type="bibr" rid="B35">Blancon et&#xa0;al., 2019</xref>). LAI can also be evaluated, indicating plant coverage, from spectral images (<xref ref-type="bibr" rid="B67">Dammer et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B216">Schirrmann et&#xa0;al., 2016</xref>).</p>
<p>Plant canopy architecture and other morphological traits of plant organs have been measured concurrently with 3D proximal sensing techniques. A body of recent reviews has compared the performances of the most common 3D sensors for high-throughput plant phenotyping (<xref ref-type="bibr" rid="B152">Li et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B195">Qiu et&#xa0;al., 2019</xref>). The 3D acquisition devices and approaches commonly used are LiDAR time-of-flight cameras, mono, and multi-view stereo vision and structure-from-motion. The LiDAR sensors can scan and extract morphological traits of plant organs from 3D point clouds. For example, LiDAR was used to estimate plant height, ground cover and above-ground biomass in wheat (<xref ref-type="bibr" rid="B135">Jimenez-Berni et&#xa0;al., 2018</xref>). However, LiDAR sensors are expensive (<xref ref-type="bibr" rid="B152">Li et&#xa0;al., 2014</xref>), take significant time and there is a need to increase scanning time to increase the spatial resolution. Deploying a UAV-based system may reduce this challenge.</p>
<p>Plant height is a key indicator for canopy structure, yield, carbohydrate storage capacity and lodging occurrence (<xref ref-type="bibr" rid="B125">Holman et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B120">Hassan et&#xa0;al., 2019</xref>). Additionally, it has significant applications in predicting biomass, identifying plant cultivars, plant stress and phenological stages (<xref ref-type="bibr" rid="B1">Aasen et&#xa0;al., 2015</xref>). The traditional method of measuring height using a metre rule is labor-intensive, cumbersome and low throughput. In recent years, the development of drones and imaging sensors that capture high-resolution images has enabled high-throughput plant height estimation. For instance, <xref ref-type="bibr" rid="B125">Holman et&#xa0;al. (2016)</xref> estimated wheat height using UAV-based RGB images and terrestrial LiDAR.</p>
<p>Chlorophyll is a vital plant trait because it is strongly related to crop physiological status and may be indicative of photosynthetic rate, crop stress, nutrition status, yield, and plant productivity (<xref ref-type="bibr" rid="B189">Peng et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B158">Maimaitijiang et&#xa0;al., 2017</xref>). The most popular tools for evaluating vegetation health using visible and near-infrared light are spectral sensors. Chlorophyll meters such as the SPAD-502 are frequently used instruments to measure the relative chlorophyll content. Handheld chlorophyll meters and fluorescence meters have been used to assess plant nitrogen status, photosynthesis, yield and its components in crops (<xref ref-type="bibr" rid="B259">Yang et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B13">Andrianto et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B95">Fern&#xe1;ndez-Calleja et&#xa0;al., 2020</xref>). Additionally, chlorophyll can be measured using NDVI sensors and portable spectrometers in the field (<xref ref-type="bibr" rid="B1004">Bai et&#xa0;al., 2016</xref>).</p>
<p>Crop nitrogen content can serve as a proxy for soil fertilizer availability, assisting farmers in precision nitrogen application to the soil. UAV-based hyperspectral imaging and ground-level optical sensors (SPAD-502, Duplex, and Multiplex) have been employed to estimate nitrogen fertilization status in maize (<xref ref-type="bibr" rid="B198">Quemada et&#xa0;al., 2014</xref>). In another study, <xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al. (2015)</xref> used a UAV equipped with a multispectral sensor (Green, Red, and NIR) to assess low nitrogen stress tolerance in corn. Additionally, vegetation indices (VIs) derived from spectral reflectance data captured by sensors devices such as the CropScan multispectral radiometer (<xref ref-type="bibr" rid="B272">Zhu et&#xa0;al., 2008</xref>), handheld spectroradiometers and the FieldSpec (<xref ref-type="bibr" rid="B98">Fitzgerald et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B236">Tilling et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B94">Feng et&#xa0;al., 2008</xref>), Tec5 (<xref ref-type="bibr" rid="B85">Erdle et&#xa0;al., 2013</xref>) can accurately measure nitrogen status in wheat and rice.</p>
<p>The above-ground biomass reflects light use efficiency and growth and is vital for carbon stock accumulation and monitoring (<xref ref-type="bibr" rid="B230">Swinfield et&#xa0;al., 2019</xref>). <xref ref-type="bibr" rid="B44">Brocks and Bareth (2018)</xref> estimated the biomass in barley using RGB images collected by UAV. Thermal infrared sensors are mostly used to detect crop water stress since they can provide temperature information for the crop (<xref ref-type="bibr" rid="B182">Park et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B193">Poblete et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B32">Bian et&#xa0;al., 2019</xref>). Thermal infrared sensors enable the estimation of canopy temperature which is a reflection of plant transpiration and plant water status. <xref ref-type="bibr" rid="B147">Kumar et&#xa0;al. (2020)</xref> used a proximal phenotyping cart (phenocart) mounted with low-cost consumer-grade digital cameras to characterize wheat germplasm for drought tolerance under field conditions. Plant yield has been considered an important agronomic trait for field phenotyping. <xref ref-type="bibr" rid="B27">Bascon et&#xa0;al. (2022)</xref> estimated rice yield using multispectral images.</p>
<p>The features of the sensors (e.g., spectral resolution, spatial resolution, specificity, and cost) should be considered according to the specific applications, phenotyping needs and context. In the African context, low-cost sensors and analysis pipelines which are not complex would benefit a broader user base for plant phenotypic trait assessments. The most successful trait assessment approach incorporates in time (throughout the crop cycle) and space (at the canopy level) the performance of the crop with respect to capturing resources (e.g., radiation, water and nutrients) and the efficiency of resource utilization (<xref ref-type="bibr" rid="B18">Araus et&#xa0;al., 2008</xref>). The aforementioned traits are discussed here with specific examples of sensors and automated measurement approaches used for their evaluation in the field (see <xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The advantages and limitations of each type of sensor are indicated.</p>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Emerging high-throughput phenotyping techniques and integrated sensor platforms applicable for plant trait assessment for field phenotyping.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Sensor</th>
<th valign="top" align="left">Examples</th>
<th valign="top" align="left">Crop species</th>
<th valign="top" align="left">Trait/phenotypic parameter</th>
<th valign="top" align="left">Applications</th>
<th valign="top" align="left">Advantages</th>
<th valign="top" align="left">Limitation</th>
<th valign="top" align="left">References</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Hyperspectral sensor</td>
<td valign="top" align="left">VNIR, SWIR</td>
<td valign="top" align="left">Rice,<break/>Wheat</td>
<td valign="top" align="left">Nitrogen status, nitrogen use efficiency, water content, yield estimation, canopy components</td>
<td valign="top" align="left">Evaluate spectral properties, explore hyperspectral bands, estimate indices for fertilizer accumulated in plant organs, early detection of plant stress</td>
<td valign="top" align="left">Accurate estimation of nitrogen content and other biochemical or physiological status</td>
<td valign="top" align="left">Update model for new crop species, image processing is challenging, sensors are costly, large data size</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B219">Seiffert et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B73">Deery et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B208">Sadeghi-Tehran et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B247">Wang et&#xa0;al., 2021</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Thermal sensor</td>
<td valign="top" align="left">Thermal infrared sensor, near-infrared camera, FLIR sensor</td>
<td valign="top" align="left">Wheat</td>
<td valign="top" align="left">Canopy temperature, drought tolerance, water use efficiency</td>
<td valign="top" align="left">Monitor crop temperature for abiotic stresses e.g., drought tolerance</td>
<td valign="top" align="left">Low-cost, precise and reliable in repeated experiments</td>
<td valign="top" align="left">Environmental factors have an impact on performance, very small temperature variations are undetectable, and cameras with higher resolution are heavier</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B62">Costa et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B72">Deery et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B209">Sagan et&#xa0;al., 2019</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Visible light sensor</td>
<td valign="top" align="left">RGB sensor, visible light camera</td>
<td valign="top" align="left">Rice</td>
<td valign="top" align="left">Shoot growth, phenology, greenness, plant vigour, leaf area</td>
<td valign="top" align="left">Visible phenotype parameters, classification of crop organs, greenness, growth and health, time series of vegetation indices</td>
<td valign="top" align="left">Affordable sensors are available</td>
<td valign="top" align="left">Visual spectral bands and properties are limited, Changes in illumination conditions cause image blur and noise errors</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B141">Kipp et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B117">Guo et&#xa0;al., 2015</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">3D sensor</td>
<td valign="top" align="left">LIDAR (Light Detection and Ranging) sensor, 3D laser scanner</td>
<td valign="top" align="left">Maize, Wheat</td>
<td valign="top" align="left">Plant height, canopy cover, above-ground biomass, crop architecture</td>
<td valign="top" align="left">Extract morphological traits of plants organs from 3D point clouds; measuring crop height and volume</td>
<td valign="top" align="left">3D plant information can be quickly captured through close-range observation</td>
<td valign="top" align="left">LIDAR can be sensitive to small variations in path length, field applications can be challenging</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B167">M&#xfc;ller-Linow et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B116">Guo et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B135">Jimenez-Berni et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B195">Qiu et&#xa0;al., 2019</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Fluorescence sensor</td>
<td valign="top" align="left">Fluorescence camera, LIFT fluorometer</td>
<td valign="top" align="left">Wheat</td>
<td valign="top" align="left">Photosynthetic capacity, chlorophyll content, quantum yield</td>
<td valign="top" align="left">Measure photosynthesis, chlorophyll, water stress</td>
<td valign="top" align="left">Automatic and rapid<break/>measurement of<break/>photosynthetic parameters</td>
<td valign="top" align="left">Limited for UAV imagery, can be affected by background noise, difficult to use in the field</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B52">Chaerle and Van Der Straeten, 2000</xref>; <xref ref-type="bibr" rid="B266">Zendonadi dos Santos et&#xa0;al., 2021</xref>
</td>
</tr>
<tr>
<td valign="top" align="center">Multispectral sensor</td>
<td valign="bottom" align="left"/>
<td valign="top" align="left">Sorghum,<break/>Maize</td>
<td valign="top" align="left">Disease resistance, nutrient use efficiency, N content, biomass, grain yield</td>
<td valign="top" align="left">Multiple plant responses to nutrient deficiency, water stress, diseases, etc.,</td>
<td valign="top" align="left">High-resolution, fast</td>
<td valign="top" align="left">Sensors can be expensive, limited to a few spectral bands</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B271">Zhao et&#xa0;al., 2021</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Spectrometer&#x2003;&#x2003;&#x2003;&#x2003;&#x2003;</td>
<td valign="bottom" align="left"/>
<td valign="top" align="left">Maize</td>
<td valign="top" align="left">Water content, seed composition, yield</td>
<td valign="top" align="left">Leaf and canopy growth, disease evaluation, leaf area, chlorophyll content, canopy temperature, and crop responses</td>
<td valign="top" align="left">Handy and easy to use, inexpensive</td>
<td valign="top" align="left">The quality of the data may be affected by soil background, spectral mixing could occur, and sensor calibration required</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B64">Cozzolino, 2014</xref>; <xref ref-type="bibr" rid="B13">Andrianto et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B58">Chivasa et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B51">Cavaco et&#xa0;al., 2022</xref>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Modified from <xref ref-type="bibr" rid="B270">Zhao et&#xa0;al., 2019</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s5">
<label>5</label>
<title>Overview of the status of field phenotyping in Africa</title>
<p>Despite the recent advances in high-throughput field phenotyping based on the non-destructive analysis of plant traits, Africa has yet to consolidate the gains of these cutting-edge technologies for research into agricultural productivity. In terms of the deployment of high-end field phenotyping tools and approaches, Africa cannot keep pace with many regions, even in the era of artificial intelligence (AI), &#x2018;internet-of-things&#x2019; (IoT) and technological advancements, although more affordable and lean phenotyping systems are now becoming available. Community-wide surveys and exchanges conducted by the International Plant Phenotyping Network (IPPN) and European Infrastructure for Multi-Scale Plant Phenomics and Simulation (EMPHASIS) within the growing phenotyping community in recent years have identified focus areas to assess the status of global plant phenotyping and crucial bottlenecks in the emerging field.</p>
<p>The major bottlenecks for developing field phenotyping in Africa were non-invasive phenotyping approaches, data management and cost among others (<xref ref-type="bibr" rid="B131">IPPN, 2016</xref>; <xref ref-type="bibr" rid="B206">Rosenqvist et&#xa0;al., 2019</xref>). This survey further reveals that in terms of using high-intensity field approaches (e.g., automation, robotics, image analysis and data storage management) for field phenotyping, Africa ranks lowest around the world. A recent survey conducted in the framework of the IPPN and EMPHASIS projects in 2020 (<xref ref-type="bibr" rid="B130">IPPN, 2020</xref>) which is reported by <xref ref-type="bibr" rid="B261">Yang et&#xa0;al. (2020)</xref> and <xref ref-type="bibr" rid="B86">Fahrner et&#xa0;al. (2021)</xref>, indicated that Africa is still behind in the implementation of high-throughput field phenotyping. This highlights the need for a broader deployment of high-throughput field phenotyping techniques, which are essential enablers or resources for agricultural sciences and breeding to address upcoming crop production challenges.</p>
<p>The IPPN over the years has been promoting the idea of strengthening modern plant phenotyping in African countries by giving travel grants to Africa and inviting students and researchers for International Plant Phenotyping symposia and internships. However, only a few institutional members are identified for collaboration in the region. In recent times, there have been some high-throughput field phenotyping research and initiatives in African countries such as South Africa, Ghana, Senegal, Morocco, Nigeria, Ethiopia, Kenya, Egypt, and Zimbabwe which is encouraging for the emerging field and will be highlighted in this review (see section 5.2 and <xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref>).</p>
<table-wrap id="T3" position="float">
<label>Table&#xa0;3</label>
<caption>
<p>Summary of some major characteristics of field phenotyping activities implemented in some African countries.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Region</th>
<th valign="top" align="left">Country</th>
<th valign="top" align="left">Area of high-throughput field phenotyping research</th>
<th valign="top" align="left">Prospects</th>
<th valign="top" align="left">Reference/web link</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">
<bold>West Africa</bold>
</td>
<td valign="top" align="left">Ghana</td>
<td valign="top" align="left">Exploration of digital agriculture, deployment of low-cost sensors and technologies for breeding, exploration of remote sensing for precision agriculture, GIS</td>
<td valign="top" align="left">Digital agriculture, low-cost precision agriculture, and breeding, use of high-throughput tools</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B118">Hall et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B146">Kpienbaareh et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B136">Kassim et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B225">Sie et&#xa0;al., 2022</xref>; <ext-link ext-link-type="uri" xlink:href="https://ftfpeanutlab.caes.uga.edu/Research/variety-development/high-throughput-phenotyping-in-senegal&#x2013;ghana-and-uganda.html">https://ftfpeanutlab.caes.uga.edu/Research/variety-development/high-throughput-phenotyping-in-senegal&#x2013;ghana-and-uganda.html</ext-link>
</td>
</tr>
<tr>
<td valign="bottom" align="left"/>
<td valign="top" align="left">Senegal</td>
<td valign="top" align="left">Exploration of digital agriculture, exploration of UAV imagery, multi-spectral imaging, GIS</td>
<td valign="top" align="left">Development of high-throughput approaches, digital agriculture, low-cost precision breeding</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B75">Dingkuhn et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B104">Gano et&#xa0;al., 2021</xref>; <ext-link ext-link-type="uri" xlink:href="https://www.devdiscourse.com/article/other/523595-senegals-embrace-of-the-digital-revolution-in-agriculture-marks-the-way-forward-for-africa">https://www.devdiscourse.com/article/other/523595-senegals-embrace-of-the-digital-revolution-in-agriculture-marks-the-way-forward-for-africa</ext-link>
</td>
</tr>
<tr>
<td valign="bottom" align="left"/>
<td valign="top" align="left">Nigeria</td>
<td valign="top" align="left">Use of field mobile agricultural robots, digital imaging, remote sensing, machine learning, GIS, site-specific analytics, drone imagery</td>
<td valign="top" align="left">Development of high-throughput approaches, digital agriculture, low-cost precision breeding, deployment of digital technologies and innovations</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B127">Ifeanyieze et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B68">Daniel et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B79">Ejikeme et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B132">Iseki and Matsumoto, 2019</xref>; <xref ref-type="bibr" rid="B10">Alabi et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B133">Izuogu et&#xa0;al., 2023</xref>; <ext-link ext-link-type="uri" xlink:href="https://nitda.gov.ng/wp-content/uploads/2020/11/Digital-Agriculture-Strategy-NDAS-In-Review_Clean.pdf">https://nitda.gov.ng/wp-content/uploads/2020/11/Digital-Agriculture-Strategy-NDAS-In-Review_Clean.pdf</ext-link>
</td>
</tr>
<tr>
<td valign="top" align="left">
<bold>North Africa</bold>
</td>
<td valign="top" align="left">Morocco</td>
<td valign="top" align="left">High-throughput phenotyping, precision field-based phenotyping platform for drought/heat tolerance, development of quinoa phenotyping methodologies, expanding the precision and prediction value of phenotyping/genotypic data for new germplasm emerging from the wheat, adding an HTPP system for wheat abiotic stresses</td>
<td valign="top" align="left">Expanding phenotyping capabilities, low-cost precision breeding, deployment of digital technologies and innovations, expansion in remote sensing capabilities</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B33">Bijaber et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B69">Danzi et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B40">Bouras et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B134">Jabir and Falih, 2020</xref>; <xref ref-type="bibr" rid="B148">Laachrate et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B197">Quahir et&#xa0;al., 2022</xref>;<break/>
<ext-link ext-link-type="uri" xlink:href="https://www.fao.org/in-action/plant-breeding/nuestrosasociados/africa/morocco/es/">https://www.fao.org/in-action/plant-breeding/nuestrosasociados/africa/morocco/es/</ext-link>; <ext-link ext-link-type="uri" xlink:href="https://www.icarda.org/research/projects/precision-field-based-phenotyping-platform-droughtheat-tolerance-morocco-pwpp">https://www.icarda.org/research/projects/precision-field-based-phenotyping-platform-droughtheat-tolerance-morocco-pwpp</ext-link>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Egypt</td>
<td valign="top" align="left">High-throughput precision phenotyping for improvement of drought and salt tolerance in wheat genotypes, implementation of digital technology (mobile applications) for field phenotyping, AI-enabled system to enhance agriculture process, satellite imagery for crop monitoring</td>
<td valign="top" align="left">Expanding phenotyping capacities, low-cost precision agriculture, and breeding</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B83">El-Shirbeny et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B82">Elsayed et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B223">Shokr, 2020</xref>; <xref ref-type="bibr" rid="B25">Bahn et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B80">Elmetwalli et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B81">Elsafty and Atallah, 2022</xref>; <xref ref-type="bibr" rid="B3">Abdelnabby and Khalil, 2023</xref>; <xref ref-type="bibr" rid="B157">Mahdy and Ahmad, 2023</xref>; <xref ref-type="bibr" rid="B214">Sayed et&#xa0;al., 2023</xref>; <ext-link ext-link-type="uri" xlink:href="https://globalrust.org/geographic/egypt">https://globalrust.org/geographic/egypt</ext-link>; <ext-link ext-link-type="uri" xlink:href="https://www.fao.org/e-agriculture/news/egypt-turns-fao-digital-transformation-agriculture">https://www.fao.org/e-agriculture/news/egypt-turns-fao-digital-transformation-agriculture</ext-link>; <ext-link ext-link-type="uri" xlink:href="https://dailynewsegypt.com/2021/12/07/government-launches-ai-enabled-system-to-enhance-agriculture-process/">https://dailynewsegypt.com/2021/12/07/government-launches-ai-enabled-system-to-enhance-agriculture-process/</ext-link>
</td>
</tr>
<tr>
<td valign="top" align="left">
<bold>Southern Africa</bold>
</td>
<td valign="top" align="left">South Africa</td>
<td valign="top" align="left">Deployment of field scanalyzer (FieldScan) for spectral crop measurement, remote sensing for precision agriculture</td>
<td valign="top" align="left">Expanding phenotyping capacities, low-cost precision agriculture, and breeding, advancing remote sensing capabilities</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B170">Mutanga et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B43">Brewer et&#xa0;al., 2022a</xref>, <xref ref-type="bibr" rid="B42">b</xref>; <xref ref-type="bibr" rid="B49">Buthelezi et&#xa0;al., 2023</xref>
</td>
</tr>
<tr>
<td valign="bottom" align="left"/>
<td valign="top" align="left">Zimbabwe</td>
<td valign="top" align="left">UAV-based high-throughput phenotyping, multispectral remote sensing in maize varietal response to maize streak virus (MSV) disease, high-throughput phenotyping of maize performance under phosphorus fertilization, remote sensing methodologies for crop monitoring under conservation agriculture</td>
<td valign="top" align="left">Expanding phenotyping capacities, low-cost precision agriculture, and breeding</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B138">Kefauver et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B114">Gracia-Romero et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B169">Musungwini, 2018</xref>; <xref ref-type="bibr" rid="B45">Buchaillot et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B58">Chivasa et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B113">Gracia-Romero et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B224">Shonhe and Scoones, 2022</xref>; <xref ref-type="bibr" rid="B185">Parwada and Marufu, 2023</xref>;</td>
</tr>
<tr>
<td valign="top" align="left">
<bold>East Africa</bold>
</td>
<td valign="top" align="left">Kenya</td>
<td valign="top" align="left">Satellite-based assessment of maize yield variations in smallholder farms, GIS and remote sensing capabilities</td>
<td valign="top" align="left">Expanding phenotyping capacities, low-cost precision agriculture, and breeding</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B138">Kefauver et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B145">Kotikot and Onywere, 2015</xref>; <xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B47">Burke and Lobell, 2017</xref>; <xref ref-type="bibr" rid="B159">Manzi and Gweyi-Onyango, 2021</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Ethiopia</td>
<td valign="top" align="left">GIS for precision agriculture, imaging technologies for crop trait analysis</td>
<td valign="top" align="left">Expanding phenotyping capacities, low-cost precision agriculture, and breeding</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B11">Alemaw and Agegnehu, 2019</xref>; <xref ref-type="bibr" rid="B1006">Bontpart et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B71">Debesa et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B31">Beyene et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B70">Debalke and Abebe, 2022</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>Like in many developing countries, field phenotyping in African countries is mostly based on conventional and traditional methodologies which rely heavily on manually recorded measurements of phenotypic data or visual assessment of plant parameters. It entails manually inspecting crops and measuring several crop characteristics that affect yield traits, including plant height, number of tillers, leaf color, leaf shape, leaf area index (LAI), chlorophyll content, growth stages, above-ground biomass and stress tolerance (<xref ref-type="bibr" rid="B106">Gedil and Menkir, 2019</xref>; <xref ref-type="bibr" rid="B37">Bongomin et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B24">Badu-Apraku et&#xa0;al., 2023</xref>). In practice, in traditional field phenotyping, breeders or research evaluators inspect the trial fields and rate the plots according to how they feel, taste, smell, and appear (<xref ref-type="bibr" rid="B140">Kim, 2020</xref>). Such phenotyping methods have several disadvantages such as being low-throughput, time-consuming, laborious, expensive and error-prone (<xref ref-type="bibr" rid="B54">Chapu et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B255">Xiao et&#xa0;al., 2022</xref>). Although these methods have been beneficial in developing new crop cultivars and improved yields, it is crucial that more effective phenotyping methods be used to increase the accuracy of data collection.</p>
<p>In parallel, field phenotyping is undertaken to evaluate the agronomic performance of crops in breeding programs, germplasm collections and in biotechnology programs to deliver improved cultivars that can cope with environmental stresses (e.g., <xref ref-type="bibr" rid="B19">Asare-Bediako et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B106">Gedil and Menkir, 2019</xref>; <xref ref-type="bibr" rid="B204">Rezende et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B137">Kavhiza et&#xa0;al., 2022</xref>). These phenotyping research targets are focused on key crops for food security but are predominantly low-throughput phenotyping based on field trials. In sub-Saharan Africa, breeding programs championed by the Alliance for a Green Revolution in Africa (AGRA) have been dedicated to priority crops such as rice, maize, cassava, yam, beans, cowpea and vegetables under various regional breeding networks for improved varieties and seed systems (<xref ref-type="bibr" rid="B88">FAO, 2011</xref>; <xref ref-type="bibr" rid="B8">AGRA, 2019</xref>).</p>
<p>Previous studies have used a variety of calibration data, including ground-based survey methods and crop model simulations, to predict yield in smallholder systems (<xref ref-type="bibr" rid="B47">Burke and Lobell, 2017</xref>; <xref ref-type="bibr" rid="B176">Ogutu et&#xa0;al., 2018</xref>). However, there has been emerging evidence in SSA suggesting inaccurate farmer-reported crop production estimates in smallholder production systems (<xref ref-type="bibr" rid="B254">World Bank, 2010</xref>; <xref ref-type="bibr" rid="B112">Gourlay et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B2">Abay et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B246">Wahab, 2020</xref>). These anomalies in crop yield estimation at smallholder, country and regional levels can cause price fluctuations (i.e., inflation), wrong national policy decisions and food insecurity among others. High-throughput and/or digital phenotyping might offer a better estimation of regional and national crop production.</p>
<p>Recent advances in sensor technology and the availability of free high-resolution (spatial and temporal) multispectral satellite images have also presented an opportunity to predict the yield of maize (<xref ref-type="bibr" rid="B57">Chivasa et&#xa0;al., 2017</xref>) and detect leaf spot diseases in groundnut (<xref ref-type="bibr" rid="B225">Sie et&#xa0;al., 2022</xref>), adaptation responses to early drought stress in sorghum (<xref ref-type="bibr" rid="B104">Gano et&#xa0;al., 2021</xref>) as well as mapping spatial distribution on a near real-time basis for a region, which hitherto was not feasible.</p>
<sec id="s5_1">
<label>5.1</label>
<title>Field phenotyping initiatives and programs in Africa</title>
<p>Despite the low implementation of high-throughput field phenotyping in Africa, there are some efforts by research organizations to adopt the technology in some countries. Prominent among these initiatives is a global network for precision field-based wheat phenotyping. (<ext-link ext-link-type="uri" xlink:href="https://globalrust.org/content/global-network-precision-field-based-wheat-phenotyping">https://globalrust.org/content/global-network-precision-field-based-wheat-phenotyping</ext-link>). Based on a global network of wheat partners, field phenotyping platforms are being developed with the support of the CGIAR research program on wheat and co-investing national agricultural research centers around the world, including some African countries such as Kenya, Ghana, Nigeria, Ethiopia, and Morocco.</p>
<p>The main goal of this network is to generate high-quality phenotypic data to assist plant breeders in developing disease and drought-resistant, high-yielding wheat varieties with a broad genetic base and maximizing the potential of new genotyping technologies. Additional but vital goals are to share knowledge and germplasm to accelerate new germplasm development and dissemination as well as develop capacities of breeders and plant scientists in precision field phenotyping. Some examples of these field phenotyping interventions being implemented include the development and application of precise phenotyping approaches, standardized protocols and novel tools for heat stress assessment in Sudan, <italic>Septoria tritici</italic> blotch in durum wheat in Tunisia (<xref ref-type="bibr" rid="B30">Ben M&#x2019;Barek et&#xa0;al., 2022</xref>), <italic>Septoria tritici</italic> blotch in durum wheat and wheat rusts in Ethiopia (<xref ref-type="bibr" rid="B139">Kidane et&#xa0;al., 2017</xref>; <ext-link ext-link-type="uri" xlink:href="https://globalrust.org/content/sources-resistance-septoria-tritici-blotch-identified-ethiopian-durum-wheat">https://globalrust.org/content/sources-resistance-septoria-tritici-blotch-identified-ethiopian-durum-wheat</ext-link>), heat and drought tolerance in spring wheat in Morocco, yield potential in Egypt and Zimbabwe and drought and yield potential in Kenya (<ext-link ext-link-type="uri" xlink:href="https://globalrust.org/content/global-network-precision-field-based-wheat-phenotyping">https://globalrust.org/content/global-network-precision-field-based-wheat-phenotyping</ext-link>).</p>
<p>Additionally, low-cost high-throughput phenotyping tools for field selection for disease, drought and crop variety performance are currently being developed. These tools will be used in breeding programs in Senegal, Ghana and Uganda and will serve as &#x201c;centers of excellence for peanut breeding&#x201d; in West and Eastern Africa (<ext-link ext-link-type="uri" xlink:href="https://ftfpeanutlab.caes.uga.edu/Research/variety-development/high-throughput-phenotyping-in-senegal&#x2013;ghana-and-uganda.html">https://ftfpeanutlab.caes.uga.edu/Research/variety-development/high-throughput-phenotyping-in-senegal&#x2013;ghana-and-uganda.html</ext-link>).</p>
<p>In West Africa, the field phenotyping network, since its inception in 2016 in the sub-region, has implemented high-throughput UAV (drone-based) phenotyping methodologies which are functional for sorghum, cowpea, pea nut and pearl millet (<xref ref-type="bibr" rid="B104">Gano et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B22">Audebert et&#xa0;al., 2022</xref>). The network is advancing breeding activities through &#x2018;fine phenotyping&#x2019;, varietal evaluations in diverse environments to identify hot spots for specific stresses, including farmers&#x2019; fields to test promising breeding lines in participating countries such as Senegal, Ghana, Mali and Burkina Faso.</p>
<p>The establishment of the network has facilitated infrastructure development, equipment acquisition, data management paired with long-term training of dedicated students, technicians and breeders capable of doing both breeding and carrying out high-throughput phenotyping measurements. In the subregion, three sites have been chosen as prospective hubs for high throughput phenotyping. Each hub including Bambey (ISRA research station, Senegal), Sotouba (IER research station, Bamako, Mali) and Farako-ba (INERA research Station, Bobo Dioulasso, Burkina Faso) exemplifies the diversity of soil and climate conditions in the region. According to <xref ref-type="bibr" rid="B22">Audebert et&#xa0;al. (2022)</xref>, the network setup in Senegal is the most advanced while Mali and Burkina Faso lag behind mainly due to limited phenotyping equipment and funding challenges.</p>
<p>Similarly, the Regional Study Centre for the Improvement of Drought Adaptation (CERAAS) in complementing the field phenotyping initiatives of the West African field phenotyping network, has developed robust UAV imagery-based data collection and spatial modelling methodologies to accurately measure key traits of cereal crops to advance plant breeding programs. UAVs equipped with a multispectral imaging system coupled with a fully automated image processing pipeline can indirectly measure agronomic and phenological characteristics of cereal crops in agricultural field trials (<xref ref-type="bibr" rid="B161">Mbaye et&#xa0;al., 2022</xref>).</p>
<p>Moreover, to advance the promotion and advancement of precision agriculture (PA) in Africa, the African Association for Precision Agriculture (AAPA), an initiative of the African Plant Nutrition Institute (APNI) is spearheading this goal (<ext-link ext-link-type="uri" xlink:href="https://paafrica.org/AAPA">https://paafrica.org/AAPA</ext-link>). Since its establishment in 2020, the AAPA has worked in partnership with academia, research institutions, agri-food industry, financial institutions, and public and private sector organizations to develop and scale up PA strategies and innovations through sustainable integration into African agriculture to address food security (i.e., reduce yield gaps) climate change, and land degradation challenges.</p>
</sec>
<sec id="s5_2">
<label>5.2</label>
<title>Field phenotyping research in African countries</title>
<sec id="s5_2_1">
<label>5.2.1</label>
<title>The case in Ghana</title>
<p>Digitalization of Agriculture is a new trend facilitated by digital platforms aimed at transforming small scale agriculture by providing agricultural services to smallholder farmers in Ghana (<xref ref-type="bibr" rid="B20">Atanga, 2020</xref>; <xref ref-type="bibr" rid="B5">Abdulai et&#xa0;al., 2023</xref>). These digital platforms include simple devices such as mobile phones or radio to a more sophisticated devices (e.g., field sensors, GIS, drones, field sensors, machinery sensors and diagnostics precision systems).</p>
<p>In Ghana some of the notable digital platforms transforming the small-scale farming sector include the TROTRO Tractor Limited (an agritech company) that combines mechanization with IoT and technology to make agricultural machinery (i.e., tractors and combined harvesters) available, accessible, and affordable to farmers thereby enhancing their efficiency and productivity (<ext-link ext-link-type="uri" xlink:href="https://www.trotrotractor.com">https://www.trotrotractor.com</ext-link>). The use of remote sensing as a decision support system (DSS) tool to optimize irrigation and farm management towards increasing yields has also been demonstrated (<xref ref-type="bibr" rid="B146">Kpienbaareh et&#xa0;al., 2019</xref>). These innovations primarily address the numerous issues smallholders and rural farmers confront in the present food systems, such as climate change, low access to inputs and restricted access to information (<xref ref-type="bibr" rid="B74">Degila et&#xa0;al., 2023</xref>).</p>
<p>As in many African countries breeding and field phenotyping is mostly based on conventional manual methods. However, to evaluate crop performance and improve breeding competitiveness, modern technologies using high-throughput techniques are being implemented but at a slow pace (e.g., <xref ref-type="bibr" rid="B118">Hall et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B136">Kassim et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B225">Sie et&#xa0;al., 2022</xref>). For instance, the responses of two populations of groundnut genotypes with various maturities to early and late leaf spot diseases were assessed under field conditions using UAV imagery (<xref ref-type="bibr" rid="B136">Kassim et&#xa0;al., 2022</xref>). In another breeding program, a smartphone-based RGB images detected leaf spot resistance and predicted yield in groundnut (<xref ref-type="bibr" rid="B225">Sie et&#xa0;al., 2022</xref>). In a resource constraint economy, Ghana is faced with numerous challenges such as lack of research funding, phenotyping infrastructures and technical personnel among others that can advance rapid characterization of agriculturally relevant traits (e.g., growth, yield, stress resistance). To increase its phenotyping capabilities will require a concerted effort from all stakeholders across the crop production value chain.</p>
</sec>
<sec id="s5_2_2">
<label>5.2.2</label>
<title>The case in Senegal</title>
<p>Senegal is making strides in precision agriculture by employing digital tools to address crop production challenges (<ext-link ext-link-type="uri" xlink:href="https://www.apni.net/wp-content/uploads/2020/02/WAFPA-Tine.pdf">https://www.apni.net/wp-content/uploads/2020/02/WAFPA-Tine.pdf</ext-link>). Even though advancement in modern breeding and field phenotyping methodologies has been slower and predominantly based on conventional methods (e.g., <xref ref-type="bibr" rid="B75">Dingkuhn et&#xa0;al., 2015</xref>), the use of drones for agricultural monitoring (i.e., stress detection, disease surveillance, crop performance) aided by high-throughput phenotyping has been exploited thanks to initiatives by the CERAAS and West African field phenotyping network. For instance, UAV multi-spectral imaging has been employed for the estimation of shoot biomass, leaf area index (LAI) and plant height of West African sorghum varieties under severe drought conditions (<xref ref-type="bibr" rid="B104">Gano et&#xa0;al., 2021</xref>). The drone-based field phenotyping approach developed could help identify essential traits and cultivars for drought tolerance in sorghum breeding. The main challenges confronting crop field phenotyping in Senegal are lack of equipment, technical personnel and funding (<xref ref-type="bibr" rid="B22">Audebert et&#xa0;al., 2022</xref>). However, Senegal being a hub for field phenotyping in West Africa, has the potential to increase its field phenotyping capabilities in the future.</p>
</sec>
<sec id="s5_2_3">
<label>5.2.3</label>
<title>The case in Nigeria</title>
<p>According to a recent review by <xref ref-type="bibr" rid="B133">Izuogu et&#xa0;al. (2023)</xref>, the digitalization of agriculture in Nigeria has reduced middlemen&#x2019;s participation in agriculture, offered small-holder farmers opportunities to improve their productivity and markets, and strengthened the connections between extension and research facilities. The authors demonstrated that for effective digitalization of agriculture, training was required in the areas of skills development, use of demand-driven digital services, digital privacy, and security issues. The challenges of digitalization of agriculture identified were lack of technical expertise, inadequate infrastructure, and high purchase and maintenance costs. The use of remote sensing techniques for precision crop production and monitoring has been implemented but to a lesser extent. <xref ref-type="bibr" rid="B127">Ifeanyieze et&#xa0;al. (2014)</xref> have previously reviewed the remote sensing techniques needed for the smooth implementation of precision crop management by farmers as a climate change adaptation strategy in Nigeria. Few research groups have utilized remote sensing techniques for field phenotyping. For instance, <xref ref-type="bibr" rid="B79">Ejikeme et&#xa0;al. (2017)</xref> used a satellite-based crop prediction model to estimate crop statistics of major crops including rice, cassava, yam, and maize. Recently, the Institute of Tropical Agriculture (IITA) through its collaborative soybean breeding programs has implemented machine learning (ML) models and multispectral high-resolution UAV imagery to aid rapid high-throughput phenotypic workflow for soybean yield estimation (<xref ref-type="bibr" rid="B10">Alabi et&#xa0;al., 2022</xref>). Other breeding programs used manual field evaluation coupled with digital imaging analysis for phenotyping tomato breeding population (<xref ref-type="bibr" rid="B68">Daniel et&#xa0;al., 2016</xref>).</p>
<p>The use of a handheld optical NDVI sensor for the evaluation of shoot biomass in field-grown staking yam has been implemented (<xref ref-type="bibr" rid="B132">Iseki and Matsumoto, 2019</xref>). Altogether, Nigeria has great potential for improving its field phenotyping capabilities.</p>
</sec>
<sec id="s5_2_4">
<label>5.2.4</label>
<title>The case in Morocco</title>
<p>Morocco is among the few African countries well-positioned for widespread agricultural digitalization for precision agriculture and field phenotyping to increase crop production and cope with adverse environmental conditions such as drought. <xref ref-type="bibr" rid="B134">Jabir and Falih (2020)</xref>, recently reviewed the state of digital agriculture in Morocco and highlighted the opportunities and challenges that need to be addressed. The design and implementation of a wireless sensor network (WSN) and decision support tools (i.e., drones) for monitoring the agricultural environment have been demonstrated (<xref ref-type="bibr" rid="B134">Jabir and Falih, 2020</xref>). Nevertheless, challenges such as sensor deployment and inadequate software analytics still exist (<xref ref-type="bibr" rid="B144">Kobo et&#xa0;al., 2017</xref>). Morocco is home to the International Centre for Agricultural Research in the Dry Areas (ICARDA&#x2019;s) phenotyping facilities (<xref ref-type="bibr" rid="B126">ICARDA phenotyping platforms in Morocco</xref>), including a precision phenotyping platform at Sidi el Aidi (Settat) (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>) and a phenomobile system (PhenoBuggy) situated at the main research station in Marchouch (Rabat) designed for drought and heat stress tolerance studies (<ext-link ext-link-type="uri" xlink:href="https://www.cgiar.org/news-events/news/icardas-phenotyping-facilities-a-game-changing-solution-for-abiotic-stress-tolerance-in-crops/">https://www.cgiar.org/news-events/news/icardas-phenotyping-facilities-a-game-changing-solution-for-abiotic-stress-tolerance-in-crops/</ext-link>). The PhenoMA is another high-throughput phenotyping platform currently installed in Benguerir (<xref ref-type="bibr" rid="B197">Quahir et&#xa0;al., 2022</xref>). Field phenotyping using various remote sensing techniques has been deployed for drought monitoring (<xref ref-type="bibr" rid="B33">Bijaber et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B40">Bouras et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B148">Laachrate et&#xa0;al., 2020</xref>), and grain yield prediction (<xref ref-type="bibr" rid="B29">Belmahi et&#xa0;al., 2023</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>The ICARDA's precision field phenotyping platforms installed at Sidi el Aidi (Settat) in Morocco. Images are in courtesy of Andrea Visioni of ICARDA-Morocco.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-14-1219673-g003.tif"/>
</fig>
</sec>
<sec id="s5_2_5">
<label>5.2.5</label>
<title>The case in Egypt</title>
<p>Digital agriculture appears promising in addressing the major challenges facing the agri-food sector in Egypt and across the Middle East and North Africa (MENA) countries (<xref ref-type="bibr" rid="B25">Bahn et&#xa0;al., 2021</xref>). Available evidence indicates that the adoption of digital and precision agriculture technologies is still in its infancy and is typically driven by high-value agricultural production (<xref ref-type="bibr" rid="B81">Elsafty and Atallah, 2022</xref>; <xref ref-type="bibr" rid="B214">Sayed et&#xa0;al., 2023</xref>). However, Egypt has made strides in the utilization of modern technologies for agricultural crop management employing big data in tandem with cloud support systems, IoT, UAVs, satellite imagery, AI, machine learning, and remote sensing (<xref ref-type="bibr" rid="B223">Shokr, 2020</xref>; <xref ref-type="bibr" rid="B3">Abdelnabby and Khalil, 2023</xref>; <xref ref-type="bibr" rid="B214">Sayed et&#xa0;al., 2023</xref>). Typical high-throughput field phenotyping methodologies has been implemented in various crops for quantifying wheat characteristics in the Nile Delta (<xref ref-type="bibr" rid="B80">Elmetwalli et&#xa0;al., 2022</xref>) and estimating the growth performance and yield of soybean exposed to different drip irrigation regimes under arid conditions (<xref ref-type="bibr" rid="B1005">Elmetwalli et&#xa0;al., 2020</xref>). Additionally, remote sensing techniques based on thermal imaging and passive reflectance have been used to estimate the crop water status and grain yield in wheat (<xref ref-type="bibr" rid="B83">El-Shirbeny et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B82">Elsayed et&#xa0;al., 2017</xref>).</p>
</sec>
<sec id="s5_2_6">
<label>5.2.6</label>
<title>The case in South Africa</title>
<p>The agricultural sector in South Africa has been developing and moving towards becoming a knowledge-intensive enterprise due to new innovations and technologies incorporated in the digital economy (<xref ref-type="bibr" rid="B28">Baum&#xfc;ller and Kah, 2019</xref>; <xref ref-type="bibr" rid="B38">Born et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B227">Smidt and Jokonya, 2022</xref>). Due to this transformation, conventional production methods have gradually been replaced with more advanced, efficient and innovative systems (e.g., remote sensing) for crop breeding and phenotyping (<xref ref-type="bibr" rid="B170">Mutanga et&#xa0;al., 2016</xref>).</p>
<p>Field phenotyping using modern high-throughput infrastructures and precision agriculture techniques is better developed in South Africa compared to other countries on the continent (<xref ref-type="bibr" rid="B174">Nyaga et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B165">Mukhawana et&#xa0;al., 2023</xref>). Some research groups are making efforts in championing field phenotyping and precision agriculture through workshops and implementation of UAV remote sensing applications and other approaches for agricultural monitoring (stress detection, nutrient and irrigation management) (<ext-link ext-link-type="uri" xlink:href="https://www.fabinet.up.ac.za/index.php/research-groups/remote-sensing">https://www.fabinet.up.ac.za/index.php/research-groups/remote-sensing</ext-link>). For example, the Forestry and Agricultural Biotechnology Institute (FABI) and the Agricultural Research Council (ARC) (<ext-link ext-link-type="uri" xlink:href="https://www.arc.agric.za/Pages/Home.aspx">https://www.arc.agric.za/Pages/Home.aspx</ext-link>) are committed to building phenotyping infrastructures and disseminating emerging technologies for agricultural development.</p>
<p>Various remote sensing applications have been employed targeted at different scales of crop monitoring (e.g., crop water use efficiency) in precision agriculture (e.g., <xref ref-type="bibr" rid="B168">Munghemezulu et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B249">Wellington, 2023</xref>). For instance, foliar temperature and stomatal conductance have been used as indicators of water stress in maize based on optical and thermal imagery acquired using a UAV platform (<xref ref-type="bibr" rid="B43">Brewer et&#xa0;al., 2022a</xref>). The utility of multispectral UAV imagery as proxy for predicting chlorophyll content of maize at various growth stages in smallholder farming systems has been reported (<xref ref-type="bibr" rid="B42">Brewer et&#xa0;al., 2022b</xref>). The physiological processes of the maize canopy are intimately tied to and influenced by LAI, which is closely related to its productivity (<xref ref-type="bibr" rid="B188">Peng et&#xa0;al., 2021</xref>). Another study has focused on estimating the LAI of maize in smallholder farms across the growing season using UAV-derived multi-spectral data (<xref ref-type="bibr" rid="B49">Buthelezi et&#xa0;al., 2023</xref>). Maize is a major crop in South Africa, therefore, significant research on the crop using high-throughput techniques will aid in developing improved cultivars for farmers. South Africa has a great potential for becoming the field phenotyping hub of Africa due to the massive investment in modern technologies.</p>
</sec>
<sec id="s5_2_7">
<label>5.2.7</label>
<title>The case in Zimbabwe</title>
<p>In Zimbabwe, the implementation of digitalized agriculture is low and tilted toward commercial farmers than smallholder community farmers (<xref ref-type="bibr" rid="B185">Parwada and Marufu, 2023</xref>). Specifically, highly literate, and resource-rich farming communities tend to use digitalized agriculture more frequently than farmers with lesser resources. At the communal level, farmers use mobile phones to obtain farming information relating to crop management, climate, and weather information (<xref ref-type="bibr" rid="B169">Musungwini, 2018</xref>; <xref ref-type="bibr" rid="B273">Zimbabwe Centre For High Performance Computing, 2021</xref>). The application of modern digital agriculture tools and infrastructure (i.e., sensors, robotics, AI, UAVs, and other advanced machinery is common in a few well-resourced commercial farms notably, those managed by large multinational companies (<xref ref-type="bibr" rid="B224">Shonhe and Scoones, 2022</xref>). <xref ref-type="bibr" rid="B185">Parwada and Marufu (2023)</xref> recently reviewed the challenges and opportunities for digitalization of the Zimbabwean agriculture. Key challenges such as lack of high-throughput infrastructures, digital illiteracy, and strict regulations for drone deployment among others have been highlighted for limiting digital agriculture applications. However, according to the authors, Zimbabwe have the potential for improving its digital agriculture for crop management, yield prediction, disease detection, climate forecasting, and soil management through precision agriculture. In recent years, few high-throughput phenotyping has been implemented in Zimbabwe using RGB picture vegetation indexes (<xref ref-type="bibr" rid="B138">Kefauver et&#xa0;al., 2015</xref>), and multi-spectral imaging for field phenotyping of maize (<xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>). Other studies include remote sensing methodologies for crop monitoring under conservation agriculture (<xref ref-type="bibr" rid="B114">Gracia-Romero et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B113">Gracia-Romero et&#xa0;al., 2020</xref>), affordable UAV-based RGB phenotyping techniques for evaluating maize performance under low nitrogen conditions (<xref ref-type="bibr" rid="B45">Buchaillot et&#xa0;al., 2019</xref>), and accelerating crop improvement in response to changing climate conditions employing UAV-based multispectral phenotyping for disease resistance in maize (<xref ref-type="bibr" rid="B58">Chivasa et&#xa0;al., 2020</xref>). Zimbabwe is among the few African countries capable of advancing its field phenotyping capabilities in the future.</p>
</sec>
<sec id="s5_2_8">
<label>5.2.8</label>
<title>The case in Kenya</title>
<p>Although there are several technologies currently available to Kenya&#x2019;s agricultural sector they have not yet become widely used (<xref ref-type="bibr" rid="B178">Osiemo et&#xa0;al., 2021</xref>). Large-scale adoption of digital solutions is hampered by a lack of digital literacy and infrastructure. Only a few research groups are skilled in using and maintaining back-end service operations like data management, blockchain, machine learning, IoT, GIS, and drones (<xref ref-type="bibr" rid="B178">Osiemo et&#xa0;al., 2021</xref>). However, the application of GIS and remote sensing techniques have been used to map frost hotspots for mitigating agricultural losses (<xref ref-type="bibr" rid="B145">Kotikot and Onywere, 2015</xref>), climate-smart crop management (<xref ref-type="bibr" rid="B159">Manzi and Gweyi-Onyango, 2021</xref>), and assessment of yield variations and its determinants in smallholder systems (<xref ref-type="bibr" rid="B47">Burke and Lobell, 2017</xref>). Similarly, high-throughput phenotyping platforms based on multi-spectral imaging and RGB vegetation indices have been implemented for field phenotyping of maize (<xref ref-type="bibr" rid="B138">Kefauver et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B264">Zaman-Allah et&#xa0;al., 2015</xref>). Kenya has the potential of expanding its phenotyping capacities through low-cost precision agriculture and breeding.</p>
</sec>
<sec id="s5_2_9">
<label>5.2.9</label>
<title>The case in Ethiopia</title>
<p>Digital agricultural innovations in precision agriculture have the potential to increase productivity while minimizing harmful environmental impacts along the value chains of agriculture and the food systems in Ethiopia (<xref ref-type="bibr" rid="B11">Alemaw and Agegnehu, 2019</xref>; <xref ref-type="bibr" rid="B232">Tamene and Ashenafi, 2022</xref>). In recent years, there have been some improvement in digital infrastructure in Ethiopia (<xref ref-type="bibr" rid="B4">Abdulai, 2022</xref>). However, the majority of Ethiopia&#x2019;s smallholder farmers have limited access to digital farming technologies (<xref ref-type="bibr" rid="B232">Tamene and Ashenafi, 2022</xref>). According to <xref ref-type="bibr" rid="B232">Tamene and Ashenafi (2022)</xref>, several challenges such as inadequate technological capacity, limited funding to develop and disseminate digital tools and lack of data sharing channels hampers the development of digital agriculture in Ethiopia. These barriers restrict the deployment of modern technologies for crop breeding and field phenotyping. Field phenotyping has relied largely on conventional methods as in the studies of eco-geographic adaptation and phenotypic diversity of Ethiopian teff across its cultivation range (<xref ref-type="bibr" rid="B253">Woldeyohannes et&#xa0;al., 2020</xref>) and genetic diversity in Ethiopian Durum Wheat (<xref ref-type="bibr" rid="B163">Mengistu et&#xa0;al., 2018</xref>). Field phenotyping using high-throughput techniques has been introduced in recent times. Remote sensing and GIS based methods has been used as crop yield predictors in wheat and maize (<xref ref-type="bibr" rid="B31">Beyene et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B70">Debalke and Abebe, 2022</xref>) as well as physical land suitability analysis for major cereal crops (<xref ref-type="bibr" rid="B71">Debesa et&#xa0;al., 2020</xref>). In essence, Ethiopia has the potential to accelerate its phenotyping capabilities. <xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref> summarizes some key field phenotyping activities that exist in the African countries discussed in this review.</p>
</sec>
</sec>
<sec id="s5_3">
<label>5.3</label>
<title>Current developing field phenotyping platforms in Africa</title>
<p>UAVs have been selected as the technical solution that is most suited for deployment across sites and trials throughout the several initiatives that made it possible for the West African field phenotyping network to get started (<xref ref-type="bibr" rid="B22">Audebert et&#xa0;al., 2022</xref>). For instance, in Senegal, the UAV platform comprises a FeHexaCopterV2 hexaCopter UAV system (Flying Eye Ltd., Sophia Antipolis, France) fitted with three cameras mounted on a two-axis gimbal pointing vertically downward. The camera consists of an RGB ILCE-6000 digital camera (Sony Corporation, New York, NY, USA), AIRPHEN multispectral camera (Hiphen, Avignon, France), and infrared thermographic camera Tau 2 (Flir system, Oregon, USA) that collects spectral imagery of crops such as sorghum, pearl millet and peanut and cowpea (<xref ref-type="bibr" rid="B104">Gano et&#xa0;al., 2021</xref>).</p>
<p>The Agricultural Research Council (ARC) of South Africa has installed a Phenospex planteye multispectral 3D laser scanner (i.e., the first of its kind in Africa) in the field (<ext-link ext-link-type="uri" xlink:href="https://phenospex.com/products/plant-phenotyping/fieldscan-high-throughput-field-phenotyping/fieldscan-3d-spectral-plant-measurements-in-the-field-south-africa/">https://phenospex.com/products/plant-phenotyping/fieldscan-high-throughput-field-phenotyping/fieldscan-3d-spectral-plant-measurements-in-the-field-south-africa/</ext-link>). This state-of-the-art facility is fully automated, carrying a high-resolution sensor that combines the strength of 3D vision with the power of multispectral imaging. It captures plant data non-destructively and delivers precise and accurate plant parameters in real-time. Plant phenotypic features such as digital biomass, plant height, 3D leaf area, projected leaf area, leaf area index, leaf inclination, etc., can be measured. The spectral information allows for the quantification of plant health, disease, senescence, N-content, chlorophyll levels, etc. Therefore, this phenotyping facility could assist in the characterization and development of varieties with improved biotic and abiotic stress resistance for key crops such as grapefruit, sunflower, green maize and other cereals in Southern Africa.</p>
<p>Recently, a unique close-to-field high-throughput plant phenotyping platform &#x201c;PhenoMA&#x2019;&#x2019; has been installed in Benguerir, in the arid region of Morocco by the Mohammed VI Polytechnic University. PhenoMA consists of a 1440 fully automated lysimetric mini-plots system that can track the dynamics of water use and simulate drought scenarios. A critical component is a fully autonomous phenotyping robot (Hiphen PhenoMobile) that enables plant measurements at the canopy scale, using a range of sensors including RGB, multispectral, infrared (IR), and LiDAR cameras to monitor canopy development (<xref ref-type="bibr" rid="B197">Quahir et&#xa0;al., 2022</xref>).</p>
<p>Overall, due to the rich agricultural biodiversity of Africa, phenotyping in Africa has great potential to contribute to the development of improved crop varieties and enhanced food security. The utilization of high-throughput tools can boost the elucidation of new agriculturally proven traits and catalogue these phenotypes in their natural environment.</p>
</sec>
</sec>
<sec id="s6">
<label>6</label>
<title>Challenges limiting the application of high-throughput field phenotyping in Africa and the way forward</title>
<p>The application of emerging field phenotyping technologies has the potential to accelerate plant breeding efforts and crop production in Africa. On the other hand, most of these approaches reviewed here are at best relatively new or unknown to some of the plant science community in Africa. Field phenotyping is a critical component of crop improvement but remains a major bottleneck in African agriculture, as is the case globally. Some of the key challenges limiting the application of high-throughput field phenotyping in Africa are highlighted below.</p>
<sec id="s6_1">
<label>6.1</label>
<title>Lack of appropriate high-throughput field phenotyping approaches</title>
<p>Phenotypic analysis has become a major limiting factor in genetic and physiological analyses in plant sciences as well as in plant breeding in Africa. The inadequate phenotyping infrastructures and software analytical tools that can be used by agricultural practitioners to make sense of simple to complicated phenotypic datasets have contributed to the low implementation of high-throughput phenotyping. The operational complexity to support both data acquisition and analysis has limited the use of these platforms for research activities worldwide (<xref ref-type="bibr" rid="B53">Chapman et&#xa0;al., 2014</xref>), including developing continents like Africa. To this end, training in image analytics, software, and computer vision to provide a new generation of skilled personnel must be implemented by African governments, universities, and the private sector. Phenotyping advancement is critical for current breeding progress for crop improvement in Africa. While the development of efficient high-throughput field phenotyping remains a challenge for future breeding progress, the growing interest in low-cost solutions for remote-sensing approaches, machine vision, as well as data management, may facilitate technological adoption.</p>
</sec>
<sec id="s6_2">
<label>6.2</label>
<title>Cost of phenotyping infrastructures and maintenance</title>
<p>As a developing continent comprising highly indebted poor countries (HIPC) (<xref ref-type="bibr" rid="B122">Henri, 2019</xref>) and faced with multi-faceted economic hardships, the major limitation to the adoption and implementation of high-tech field phenotyping in Africa is the perceived high entry costs associated with the longer-term footprint of prototypical platforms (<xref ref-type="bibr" rid="B202">Reynolds et&#xa0;al., 2019</xref>). In several African countries, especially those discussed in this review, basic phenotyping tools and infrastructure even for the simplest field measurements and experimentation are scarce.</p>
<p>This prevents many research organizations in Africa such as IITA, CIAT, and Africa Rice, from implementing demand-driven approaches due to a lack of investment budget or avoiding the significant follow-up costs on maintenance of large phenotyping infrastructures. For instance, the use of ground vehicles, aerial vehicles and gantries may require huge investment costs (<xref ref-type="bibr" rid="B187">Pauli et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B242">Vergara-D&#xed;az et&#xa0;al., 2016</xref>).</p>
<p>Therefore, the requirements for such specialized equipment may be a bottleneck for widespread use in breeding programs in poor countries. To alleviate this challenge, low-cost concepts and methods of high-throughput phenotyping platforms (HTPPs) (e.g., sensors and platforms) that rely on easy-to-use technology must be disseminated in Africa by identifying demands, and relevance, and adopting the required approach given the current financial constraints. For instance, conventional digital cameras (i.e., digital photography) could provide a more convenient method since they are more affordable, portable, and easy to use (<xref ref-type="bibr" rid="B1007">Casades&#xfa;s and Villegas, 2014</xref>).</p>
</sec>
<sec id="s6_3">
<label>6.3</label>
<title>Limited investment and funding</title>
<p>Limited investments in science, technology, and innovation (STI) on the part of African governments, research institutions (e.g., academia) and the private sector have partly contributed to the poor implementation of high-throughput field phenotyping. The budgetary allocations dedicated to research, development, and innovation are small. For example, in Ghana, a minimum of 1% of gross domestic product (GDP) is applied towards research and development (<ext-link ext-link-type="uri" xlink:href="https://mesti.gov.gh/government-increase-research-funding/">https://mesti.gov.gh/government-increase-research-funding/</ext-link>). Similarly, in Morocco, the percentage of GDP to research as of 2010 was 0.63% (<xref ref-type="bibr" rid="B119">Hamidi and Benabdeljalil, 2013</xref>). This research funding gap is pervasive across the African continent.</p>
<p>Whereas research institutions and universities in developed economies, such as Europe (see <ext-link ext-link-type="uri" xlink:href="https://eppn2020.plant-phenotyping.eu/EPPN2020_installations#/">https://eppn2020.plant-phenotyping.eu/EPPN2020_installations#/</ext-link>), Australia, North America and Asia, have in recent years invested heavily in large-scale research infrastructure for automated and high-throughput field phenotyping, the same cannot be said for Africa. These large investments for plant phenotyping include funding, research hours and high-throughput installations (<xref ref-type="bibr" rid="B63">Costa et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B206">Rosenqvist et&#xa0;al., 2019</xref>; <ext-link ext-link-type="uri" xlink:href="https://eppn2020.plant-phenotyping.eu/">https://eppn2020.plant-phenotyping.eu/</ext-link>).</p>
<p>Furthermore, crops grown in Africa are frequently too local to attract international research funding for field phenotyping. Only a few essential African crop commodities, such as cassava and sweet potatoes, are funded solely by extrabudgetary sources. Most of the main staple crops are exclusively funded for phenotyping exploitation outside of Africa.</p>
<p>In addition to the above considerations, African governments and the Science Granting Councils Initiative (SGCI) in sub-Saharan African countries mandated to support the Science Granting Councils (SGCs), must dedicate enough funding for low-cost plant phenotyping research infrastructure in the sub-region in the short to medium term. This could be achieved by developing financing mechanisms and collaborating with private sector partners. Donor support to Africa for agriculture and food security research should also consider projects in modern plant phenotyping and digital agriculture.</p>
</sec>
<sec id="s6_4">
<label>6.4</label>
<title>Lack of Skilled technical personnel</title>
<p>A serious deficit of skilled technical personnel in the plant sciences and phenotyping ecosystem is evident in African countries. The building up of such competencies and the development of human resource capacity is necessary to operate simple-to-sophisticated equipment to accelerate breeding efforts through high-throughput phenotyping techniques. Another major barrier is the loss of talented and skilled personnel who were trained in developed nations and have contributed to the brain drain due to inadequate job prospects in Africa. Mostly, funds to pay salaries and absorb project operating costs are either limited or insufficient, resulting in a reduction of skilled personnel. Furthermore, due to the inadequacies in research and infrastructure in many African nations, training acquired overseas is sometimes unsuited to local demands. To address this constraint, digital agricultural competencies and sensor technologies should be integrated into undergraduate and postgraduate learning curricula to allow students to specialize in digital agriculture through their projects. This will create a plethora of career opportunities for competent skilled personnel who can adapt to the emerging technologies for field phenotyping.</p>
</sec>
<sec id="s6_5">
<label>6.5</label>
<title>Regulations controlling emerging technologies</title>
<p>Emerging technologies such as UAVs offer the advantages of being flexible, real-time and non-destructive for agricultural phenotyping, but they must adhere to strict operational standards to ensure their safe use. Strict airspace regulations in many jurisdictions around the world and particularly in African countries due to impact of political instability and military governments on UAV deployment may prohibit their use or make them unfeasible in practice (<xref ref-type="bibr" rid="B103">Gago et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B258">Yang et&#xa0;al., 2017a</xref>; <xref ref-type="bibr" rid="B23">Ayamga et&#xa0;al., 2021</xref>). For instance, authorization from regulatory authorities, such as the air force, civil aviation and police, are required to undertake UAV flight campaigns, which mostly take time to be approved causing issues in time-critical data collection applications. According to <xref ref-type="bibr" rid="B23">Ayamga et&#xa0;al. (2021)</xref>, in Africa, countries with regulations include Ghana, South Africa, Zimbabwe, Nigeria, Cameroon, Benin, Gabon, Senegal, Botswana, Namibia, Malawi, Tanzania, Zambia, Madagascar, Rwanda and Kenya. However, the lack of proper regulation and enforcement continues to limit the widespread adoption of drones. Unfortunately, these regulations combine to mean that most high-throughput techniques can only be implemented by multinational research institutions, even in those organizations, deployment of systems is limited to a few high-priority projects. Commitment of African governments and relevant stakeholders is crucial in the implementation and enforcement of regulations. The widespread deployment of drones stands to benefit farmers hence concerted effort need to be made to sustain its adoption by promoting public digital literacy on the technology, skill development for potential users and farmers on drone operation and developing the necessary policy framework with regulatory agencies to increase the safety and acceptability of using agricultural drones in Africa.</p>
</sec>
<sec id="s6_6">
<label>6.6</label>
<title>Weakness of phenotyping linkages</title>
<p>At the regional and continental levels, networking is a powerful tool for increasing scientific collaboration and fostering information sharing. There seems to be weak collaborations between the African plant science community and international phenotyping partners which hampers technological transfer and adoption. As high-throughput field phenotyping initiatives have started in Africa, there is a need to strengthen national and institutional efforts within the continent for the development and application of accurate and high-throughput field phenotyping capabilities. The West Africa field phenotyping network should be strengthened and better resourced to carry out their mandate. Similar initiatives such as the EMPHASIS (<ext-link ext-link-type="uri" xlink:href="https://emphasis.plant-phenotyping.eu">https://emphasis.plant-phenotyping.eu</ext-link>) should be experimented to provide a more practical use of the available phenotyping data.</p>
<p>The IPPN should spread its operations to Africa to develop programs and establish synergies geared towards face-lifting plant phenotyping projects in the continent. Again, African governments and their partners should invest in building a center of excellence or shared facilities for African plant scientists. Finally, a more urgent challenge is, however, that the international phenotyping community needs to bridge the gap between advanced economies and developing regions of the world such as Africa to benefit from the huge research efforts made internationally.</p>
</sec>
</sec>
<sec id="s7">
<label>7</label>
<title>Concluding remarks and future perspectives</title>
<p>This review provides an overview of high-throughput field phenotyping and its implications for African crops. It highlights the prospects of emerging high-throughput phenotyping techniques and integrated sensor platforms for plant trait assessment for field phenotyping that could apply to African crops. High-throughput field phenotyping has superior advantages that facilitate quick, non-destructive, and high-throughput detection, thus overcoming the shortcomings of conventional approaches. The readiness and the potential adoption of high-throughput field phenotyping for practical implementation in Africa are of paramount interest and should be demonstrated.</p>
<p>Field phenotyping solutions of immediate to long-term feasibility for African crops will likely rely on a combination of available techniques or prototypes of low-cost sensors and imaging approaches to study crop performance. Manual methods dominate the field phenotyping ecosystem with only a few countries beginning to explore high-throughput techniques through digital and precision agriculture. Notably, high-throughput phenotyping cannot yet completely replace manual measurements but should be promoted. The implementation of high-throughput phenotyping in general, and low-cost methods for field evaluation, is still fraught with challenges in Africa. Challenges identified by this present review include the high upfront cost of the prototypical platforms, huge funding gap, lack of conceptual and technical capacity, lack of technology transfer infrastructure and methodological approaches, lack of phenotyping network on the continent and the needed legislation in some cases, amongst others.</p>
<p>Lack of financial resources, a problem pervasive in African countries needs to be tackled holistically. Public-private partnerships could support resolving these financial and investment challenges to foster political will. Although in some countries, this public-private drive is already being implemented through close collaboration between universities and agricultural research organizations, these efforts need to be stepped up. In parallel, African governments should dedicate enough funding, incentives, and tools to breeders to advance research and innovations regarding high-end plant breeding. We suggest that donor support to Africa for agriculture and food security research should also consider projects in modern plant phenotyping to cope with current and projected climate change.</p>
<p>This will open the possibility of investing more in current sensor and imaging technologies for field data collection and the use of cost-effective phenotyping technologies that are already available to increase the throughput, quantity and quality of phenotypic data. The wide range of applications for these phenotyping technologies makes them good candidates and feasible choices for adoption in Africa which hitherto were prohibitive in terms of cost and deployment. The advantages of improved sensor-platform integration have facilitated the development of complete phenotyping systems that can gather, integrate and store data for many subsystems concurrently in a structured, efficient and cost-effective way. Such platforms have been widely adopted by research groups in developed countries and are gradually adopted by plant breeders in Africa as the technology develops and the benefits are proven.</p>
<p>In addition to the adoption of high throughput field phenotyping approaches in African countries, precision agriculture will also greatly benefit and revitalize the establishment of closer interaction between breeders and farmers to develop protocols mutually for the optimal use of improved crop varieties. The tools and knowledge exchange are expected to spur a second green revolution to meet the agricultural challenges to feed the ever-increasing African population. In terms of advancing field crop phenotyping in Africa for agricultural crop sustainability, we propose that breeding priority should be given to the most important staple crops such as maize, wheat, yam, cassava, cowpea, sorghum, etc. These crops form the backbone for food security and hence their improvement is crucial in the wake of prevailing climate change and production constraints. We suggest that each country selects traits that are of high demand and relevance by farmers and consumers when designing breeding strategies. In parallel, high-throughput phenotyping should be incorporated into national agricultural research policies and prioritize the practical implementation of field phenotyping. By and large, these could be achieved when governmental and private sector participation, as well as financial support, is readily available.</p>
<p>To overcome the challenges with the deployment of phenotyping tools and the integration of software to deliver accurate data acquisition, processing, analysis and management, a multidisciplinary team of expert-level skills and competencies may be required. This will necessitate deliberate training and capacity improvement of African plant scientists and students in software engineering and computer science domains, including AI, demanding true interdisciplinary partnerships to provide meaningful results and inform decision-making, while addressing the issue of training cost and related risks. In this instance, we recommend technological adoption rather than complete technological development considering the financial constraints and the low-level expertise in software and equipment development. However, as the plant phenotyping industry develops the development of new technologies from scratch may be feasible in Africa.</p>
<p>Furthermore, we propose encouraging collaborations between the African plant science community with their international counterparts to foster collaborative research, effective technological transfer and adoption. This review recommends close collaboration with the IPPN and similar phenotyping networks to benefit from the unprecedented investments made in field phenotyping infrastructures globally. Consequently, crop scientists may leverage ground-breaking advancements in high-throughput field data collection, image analysis and data management. Efforts should be made to foster synergies among different African countries by establishing transnational interdisciplinary networks that incorporate expertise in all aspects of plant breeding.</p>
<p>To address the limited investments in science, technology and innovation (STI), a commitment for expanded and long-term funding of agricultural research and development is essential. At the policy and operational levels, barriers must be overcome to allow the smooth establishment of public-private partnerships for transformational change in research and demand-driven technologies for breeders and farmers. There is renewed interest both from private and public institutions in developed countries to support African agriculture. Hence, African agricultural institutions need to develop strategies and synergies that include building partnerships that must be implemented to tackle the challenges, especially in the face of climate change and food insecurity.</p>
<p>The widespread adoption of high-throughput field phenotyping techniques in African countries could only be made possible in plant breeding programs if it can be proven as something worthwhile in terms of genetic gains attained with resources invested. Hence, costs must be reasoned in relation to the precision, repeatability, heritability, cost per unit plot or trait, prevailing climatic and economic condition, etc., required in a particular phenotyping activity. Given what has been said, to ensure that such implementation of field phenotyping can be translated into yield gains, low-cost phenotyping tools must be adopted. On this basis, affordable, easy-to-handle, reliable tools, and phenotyping infrastructures for small to large-scale field phenotyping may become a strategic choice and pave the way for practical implementation. Such technologies applicable to phenotyping methodologies should be available soon due to the high demands and efforts by the phenotyping community in Africa.</p>
</sec>
<sec id="s8" sec-type="author-contributions">
<title>Author contributions</title>
<p>DC, NV, TW, FM, and MH provided the conceptualization of the manuscript. DC drafted, wrote, and edited the manuscript. NV, MC, AR, MM, TW, FM, and MH substantially reviewed the manuscript. TW, FM, and MH provided supervision. All authors read and approved the final manuscript. All authors contributed to the article.</p>
</sec>
</body>
<back>
<sec id="s9" sec-type="funding-information">
<title>Funding</title>
<p>This research is funded by OCP S.A under the Mohammed VI Polytechnic University (UM6P), Rothamsted Research, and Cranfield University program. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) through the Designing Future Wheat program [BB/P016855/1].</p>
</sec>
<sec id="s10" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec id="s11" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
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