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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.2025.1512294</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Impact of climate change on the potential global prevalence of <italic>Macrophomina phaseolina</italic> (Tassi) Goid. under several climatological scenarios</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Farag</surname>
<given-names>Peter F.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2384075/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Alkhalifah</surname>
<given-names>Dalal Hussien M.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Ali</surname>
<given-names>Shimaa K.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/methodology/"/>
<role content-type="https://credit.niso.org/contributor-roles/validation/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Tagyan</surname>
<given-names>Aya I.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2849380/overview"/>
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</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Hozzein</surname>
<given-names>Wael N.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
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<aff id="aff1">
<sup>1</sup>
<institution>Department of Microbiology, Faculty of Science, Ain Shams University</institution>, <addr-line>Abbasia</addr-line>, <country>Egypt</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Biology, College of Science, Princess Nourah bint Abdulrahman University</institution>, <addr-line>Riyadh</addr-line>, <country>Saudi Arabia</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Department of Agricultural Microbiology, Faculty of Agriculture, Beni-Suef University</institution>, <addr-line>Beni-Suef</addr-line>, <country>Egypt</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Department of Botany and Microbiology, Faculty of Science, Beni-Suef University</institution>, <addr-line>Beni-Suef</addr-line>, <country>Egypt</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Rachid Lahlali, Ecole Nationale d&#x2019;Agriculture de Mekn&#xe8;s, Morocco</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Chaofeng Wang, University of Nebraska-Lincoln, United States</p>
<p>Chris Little, Kansas State University, United States</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Aya I. Tagyan, <email xlink:href="mailto:i_aya50@yahoo.com">i_aya50@yahoo.com</email>; Wael N. Hozzein, <email xlink:href="mailto:hozzein29@yahoo.com">hozzein29@yahoo.com</email>
</p>
</fn>
<fn fn-type="other" id="fn003">
<p>&#x2020;ORCID: Peter F. Farag, <uri xlink:href="https://orcid.org/0000-0003-3329-7915">orcid.org/0000-0003-3329-7915</uri>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>16</day>
<month>04</month>
<year>2025</year>
</pub-date>
<pub-date pub-type="collection">
<year>2025</year>
</pub-date>
<volume>16</volume>
<elocation-id>1512294</elocation-id>
<history>
<date date-type="received">
<day>20</day>
<month>11</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>21</day>
<month>03</month>
<year>2025</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2025 Farag, Alkhalifah, Ali, Tagyan and Hozzein</copyright-statement>
<copyright-year>2025</copyright-year>
<copyright-holder>Farag, Alkhalifah, Ali, Tagyan and Hozzein</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>
<sec>
<title>Introduction</title>
<p>Climate change forms one of the most dangerous problems that disturb the earth today. It not only devastates the environment but also affects the biodiversity of living organisms, including fungi. <italic>Macrophomina phaseolina</italic> (Tassi) Goid. is one of the most pervasive and destructive soil-borne fungus that threatens food security, so predicting its current and future distribution will aid in following its emergence in new regions and taking precautionary measures to control it.</p>
</sec>
<sec>
<title>Methods</title>
<p>Throughout this work, there are about 324 records of <italic>M. phaseolina</italic> were used to model its global prevalence using 19 environmental covariates under several climate change scenarios for analysis. Maximum Entropy (MaxEnt) model was used to predict the spatial distribution of this fungus throughout the world while algorithms of DIVA-GIS were chosen to confirm the predicted model.</p>
</sec>
<sec>
<title>Results</title>
<p>Based on the Jackknife test, minimum temperature of coldest month (bio_6) represented the most effective bioclimatological parameter to fungus distribution with a 52.5% contribution. Two representative concentration pathways (RCPs) 2.6 and 8.5 of global climate model (GCM) code MG, were used to forecast the global spreading of the fungus in 2050 and 2070. The area under curve (AUC) and true skill statistics (TSS) were assigned to evaluate the resulted models with values equal to 0.902 &#xb1; 0.009 and 0.8, respectively. These values indicated a satisfactory significant correlation between the models and the ecology of the fungus. Two-dimensional niche analysis illustrated that the fungus could adapt to a wide range of temperatures (9 &#xb0;C to 28 &#xb0;C), and its annual rainfall ranges from 0&#xa0;mm to 2000&#xa0;mm. In the future, Africa will become the low habitat suitability for the fungus while Europe will become a good place for its distribution.</p>
</sec>
<sec>
<title>Discussion</title>
<p>The MaxEnt model is potentially useful for predicting the future distribution of <italic>M. phaseolina</italic> under changing climate, but the results need further intensive evaluation including more ecological parameters other than bioclimatological data.</p>
</sec>
</abstract>
<kwd-group>
<kwd>biogeography</kwd>
<kwd>DIVA-GIS</kwd>
<kwd>global warming</kwd>
<kwd>maxent</kwd>
<kwd>species distribution modeling</kwd>
</kwd-group>
<counts>
<fig-count count="10"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="81"/>
<page-count count="13"/>
<word-count count="5052"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Plant Pathogen Interactions</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<p>
<italic>Macrophomina phaseolina</italic> (Tassi) Goid. is one of the most devastating necrotrophic, seed- and soil-borne pathogenic fungus that belongs to the Botryosphaeriaceae family (<xref ref-type="bibr" rid="B16">Dell&#x2019;Olmo et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B52">Ortiz et&#xa0;al., 2023</xref>). It infects more than 800 plant species over the world, including economically important crops such as <italic>Glycine max</italic> (L.) Merr. (soybean), <italic>Helianthus giganteus</italic> E. Watson (sunflower), <italic>Vicia faba</italic> L. (bean), <italic>Gossypium hirsutum</italic> L. (cotton), <italic>Sesamum indicum</italic> L. (sesame), and cereal plants causing charcoal rot, dry root rot, wilt, blight, and damping-off diseases (<xref ref-type="bibr" rid="B21">Farr and Rossman, (2022)</xref>; <xref ref-type="bibr" rid="B70">Tan&#x10d;i&#x107; &#x17d;ivanov et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B34">Kaur et&#xa0;al., 2023</xref>). This fungus is characterized by forming a spherical aggregating mass of hyphae called microsclerotia, which can survive up to 15 years in soil and crop debris as a resistant structure to overcome several inadequate environmental conditions, making disease control a challenge (<xref ref-type="bibr" rid="B40">Marquez et&#xa0;al., 2021</xref>).</p>
<p>Climate has a major role in the prevalence of <italic>M. phaseolina</italic> which is thermophilic in nature and reflects a critical correlation with soil and environmental factors (<xref ref-type="bibr" rid="B8">Bashir, 2017</xref>). For disease occurrence, high temperature and low moisture played a pivotal role in the development and distribution of this fungus, where maximum disease was observed at 25-32&#xb0;C air and 23-35&#xb0;C soil temperature (<xref ref-type="bibr" rid="B8">Bashir, 2017</xref>; <xref ref-type="bibr" rid="B40">Marquez et&#xa0;al., 2021</xref>). Some other factors are also responsible for the occurrence of disease such as different pathogen strains, inconsistency in disease resistance and susceptibility, and soil physical and chemical characteristics that alter the interaction between pathogen and host (<xref ref-type="bibr" rid="B8">Bashir, 2017</xref>).</p>
<p>Generally, <italic>M. phaseolina</italic> is geographically distributed in tropical and sub-tropical areas with semi-arid weather (<xref ref-type="bibr" rid="B76">Wrather et&#xa0;al., 2001</xref>; <xref ref-type="bibr" rid="B63">Sarr et&#xa0;al., 2014</xref>). Despite the fact that <italic>M. phaseolina</italic> is a disease that thrives in warm climates, it has been observed in recent years to spread in a number of different locations and is now ubiquitous all over the world (<xref ref-type="bibr" rid="B73">Veverka et&#xa0;al., 2008</xref>). According to the Intergovernmental Panel on Climate Change (IPCC), one of the primary reasons for its appearance is climate change. According to the IPCC, global warming is likely to continue, and the average temperature of the earth&#x2019;s surface is expected to rise by 0.3&#x2013;4.5 degrees Celsius (<xref ref-type="bibr" rid="B14">Chen et&#xa0;al., 2022</xref>). Thus, this phenomenon has disparate effects on biodiversity and has altered fungal attributes, resulting in yield losses and economic damage (<xref ref-type="bibr" rid="B26">Ghini et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B16">Dell&#x2019;Olmo et&#xa0;al., 2022</xref>). Nowadays, the fungus can adapt to various agroecological conditions, and its aggressivity fluctuates depending on different environmental factors (biotic and abiotic) and geographic areas (<xref ref-type="bibr" rid="B42">Mihail and Taylor, 1995</xref>; <xref ref-type="bibr" rid="B20">Fang et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B9">Borer et&#xa0;al., 2016</xref>).</p>
<p>Climate change has introduced additional hurdles in safeguarding crops from fungal infections, jeopardizing food security. Understanding fungal dispersal and predicting appropriate future environments are essential for implementing preventative measures for its prevention and control (<xref ref-type="bibr" rid="B18">Dietzel et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B65">Savary et&#xa0;al., 2019</xref>). Examining the spatial distribution of infections yields critical insights into their prevalence and the influence of environmental conditions on phytopathogens and epidemics. A variety of spatial statistical approaches have been employed to characterize the spread of fungal diseases and affected plants (<xref ref-type="bibr" rid="B77">Wu et&#xa0;al., 2001</xref>; <xref ref-type="bibr" rid="B69">Taliei et&#xa0;al., 2013</xref>). The clarification of the present distribution status of <italic>M. phaseolina</italic> in relation to climate change and the constraints of current mitigation efforts is crucial since there are numerous opportunities for future research on this fungus (<xref ref-type="bibr" rid="B53">Pandey and Basandrai, 2020</xref>).</p>
<p>Geographic Information Systems (GIS) facilitate the mapping of pathogen distribution and the spatial modeling of environmental factors influencing disease occurrence by describing, analyzing, and visualizing data associated with geographic coordinates (<xref ref-type="bibr" rid="B22">Fischer and Nijkamp, 1992</xref>; <xref ref-type="bibr" rid="B47">Murad and Khashoggi, 2020</xref>). It is regarded as an advantageous instrument for forecasting species proliferation and assessing infestation impacts (<xref ref-type="bibr" rid="B3">Alkhalifah et&#xa0;al., 2022</xref>). Conserving species in their native habitats needed comprehension of their spatial distribution patterns and ecological interconnectedness. Distribution Models (SDMs) integrate geographical data from various sources utilizing GIS tools (<xref ref-type="bibr" rid="B7">Balakrishnan et&#xa0;al., 2018</xref>).</p>
<p>Species distribution modeling (SDM) is a crucial technique that delineates the specific habitat of each species (<xref ref-type="bibr" rid="B60">Runquist et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B17">Deneu et&#xa0;al., 2022</xref>). In recent years, numerous modeling software applications utilizing various mathematical methods have been created to achieve this objective; however, MaxEnt (Maximum Entropy Model) and DIVA-GIS are the most effective and precise tools employed to assess the impact of climate change on diverse fungal species. CLIMEX, GARP, and HABITAT are widely utilized methods for assessing the future distribution of certain species in response to climate change; nonetheless, their efficacy has been noted to be inferior to that of MaxEnt (<xref ref-type="bibr" rid="B67">Shabani et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B31">Hosni et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B81">Zurell et&#xa0;al., 2020</xref>).</p>
<p>This study aims to examine the effects of climate change on the worldwide occurrence of <italic>Macrophomina phaseolina</italic> (Tassi) Goid., a critical soil-borne fungal disease that jeopardizes food security in many crops. This research aims to estimate the current and future distribution of <italic>M. phaseolina</italic> under various climatological scenarios by leveraging a comprehensive dataset of occurrence records of this pathogen and employing species distribution modeling techniques, notably the Maximum Entropy (MaxEnt) model. The research aims to discover critical environmental factors affecting the habitat appropriateness of the fungus and to evaluate how shifting climate conditions may impact its regional distribution. This study seeks to address the crucial question: How will climate change influence the distribution and prevalence of <italic>Macrophomina phaseolina</italic> in the forthcoming decades?</p>
</sec>
<sec id="s2" sec-type="materials|methods">
<label>2</label>
<title>Materials and methods</title>
<sec id="s2_1">
<label>2.1</label>
<title>Global occurrence data collection for <italic>M. phaseolina</italic>
</title>
<p>In this study, most of the current distribution records of <italic>M. phaseolina</italic> were gathered from published scientific literature, and the rest of the occurrence data were obtained from the Global Biodiversity Information Facility (GBIF) digital databases (<xref ref-type="bibr" rid="B25">GBIF.org, 2022</xref>). After choosing the precise location data and removing the duplicated and high spatial uncertain records (data points characterized by a considerable degree of uncertainty concerning their geographic coordinates. This uncertainty may stem from multiple reasons, including: Inaccurate Location Data: The supplied coordinates may not accurately represent the true location of the event; and Low Precision: The information may rely on general geographic descriptors instead of precise coordinates, resulting in uncertainty), a total of 324 geo-referenced coordinates (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>) were saved as comma delimited (CSV) Excel format and used for species distribution modeling (SDM) analysis (<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>Global prevalence of <italic>M. phaseolina</italic> according to the collected occurrence data.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g001.tif"/>
</fig>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Bioclimatological covariates</title>
<p>Nineteen bioclimate covariates were downloaded from the global WorldClim database (<ext-link ext-link-type="uri" xlink:href="http://www.worldclim.org">www.worldclim.org</ext-link>, accessed on 6 Feb 2023) to start the species distribution modeling at a spatial resolution of around 5 Km<sup>2</sup> (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S2</bold>
</xref>). These variables were generated using the average interpolated climate data from 1950 to 2000 (<xref ref-type="bibr" rid="B30">Hosni et&#xa0;al., 2022</xref>). Layers of bioclimatic variables 8-9 and 18-19 were dislodged to establish the current climatic data due to their spatial distortions in those variable layers (<xref ref-type="bibr" rid="B62">Samy et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B31">Hosni et&#xa0;al., 2020</xref>). So, only 15 bioclimatic covariates were transformed into ASCII files using ArcGIS version 10.7. Pearson correlation coefficient has been applied to exclude extremely correlated covariates (r2 &#x2265; |0.8|) and minimize multicollinearity from distribution models (<xref ref-type="bibr" rid="B74">Wang et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B30">Hosni et&#xa0;al., 2022</xref>). According to this, only five climatic variables were selected to establish final models: Bio_6, Bio_1, Bio_4, Bio_12, and Bio_10.</p>
<p>We modeled the future distribution patterns for <italic>M. phaseolina</italic> to investigate the variability of their potential habitat across several climate scenarios (<xref ref-type="bibr" rid="B61">Saha et&#xa0;al., 2021</xref>). The potential values for climatic covariates under future climate conditions in the 2050s (average estimation between 2041 and 2060) and 2070s (average estimation between 2061 and 2080) were derived from the global climate model (GCM) [MRI-CGCM3, Code MG] developed by the Meteorological Research Institute under two IPCC-CMIP5 [Coupled Model Intercomparing Project Phase 5] representative concentration pathways (RCPs), 2.6 and 8.5 (<ext-link ext-link-type="uri" xlink:href="https://www.worldclim.org/data/cmip6/cmip6climate.html">https://www.worldclim.org/data/cmip6/cmip6climate.html</ext-link> (accessed on 5 Feb 2023). RCP 2.6 is the minimum greenhouse gas emission scenario, while RCP 8.5 is the maximum greenhouse gas emission scenario (<xref ref-type="bibr" rid="B29">Heringer et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B43">Mohammadi et&#xa0;al., 2019</xref>).</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>Distribution modeling procedures</title>
<p>Two modeling software: the maximum entropy (MaxEnt, version 3.4.1) and Clim. Model on DIVA-GIS software V7.5 were utilized to predict the suitable habitat of <italic>M. phaseolina</italic> (<xref ref-type="bibr" rid="B57">Phillips et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B56">Phillips and Dud&#xed;k, 2008</xref>). Both used presence-only and small sample-size data to forecast species distribution and model habitat suitability as a function of environmental variables with pseudoabsence points (Since the models are using presence-only data, pseudoabsence points are artificially created locations where the species is assumed to be absent. These points help balance the dataset and provide a reference against which to compare the present data, allowing the model to better understand the conditions under which the species thrives) (<xref ref-type="bibr" rid="B10">Bradie. and Leung, 2017</xref>). To evaluate the predictive performance of our models, species occurrence information for model calibration was divided into a training set (75% of occurrence records) and a test set (25% of occurrence records), where this process was repeated five times as a choose in Maxent option (<xref ref-type="bibr" rid="B30">Hosni et&#xa0;al., 2022</xref>). We followed (<xref ref-type="bibr" rid="B71">Tavanpour et&#xa0;al., 2019</xref>). for settings and used 10000 maximum random background points as pseudoabsence, regularization multiplier 1, 10000 maximum iterations with 10<sup>-5</sup> convergence threshold, and selecting the logistic output format. The habitat suitability areas of the resultant models were classified into 5 classes (not suitable, low, medium, high, and very high). Also, the Diva-GIS modeling tool was used to generate the limitation factor map. This map is a crucial component that helps identify and understand the factors that limit the distribution of the species. It provides valuable information about the environmental variables or conditions that influence the presence or absence of a species in a given area.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>Model interpretation and evaluation</title>
<p>The developed model was evaluated by calculating the area under the curve (AUC) of the receiver operating characteristic (ROC) plot, which varied from 0 (which corresponded to a random distribution) to 1 (which represented a perfect prediction) (<xref ref-type="bibr" rid="B55">Phillips et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B46">Mulieri and Patitucci, 2019</xref>). Models that have analysis of variance (AUC) values that are greater than 0.9 suggest outstanding prediction accuracy, while values that fall between 0.7 and 0.9 indicate good prediction accuracy, and values that are less than 0.7 indicate low prediction accuracy (<xref ref-type="bibr" rid="B54">Pearson, 2010</xref>). True Skill Statistics (TSS) was utilized in order to evaluate the predictability of the models that were projected, and the values that were utilized varied from -1 to 1 (<xref ref-type="bibr" rid="B5">Allouche et&#xa0;al., 2006</xref>). Negative numbers that are near to 0 suggest a weak association between the prediction model and the distribution, whereas positive values that are close to 1 show a significant relationship between the two. Furthermore, the jackknife test was utilized in structural equation modeling (SDM) to examine the impact of dominant environmental variables on model outcomes in order to choose dominant elements (<xref ref-type="bibr" rid="B5">Allouche et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B79">Yang et&#xa0;al., 2013</xref>).</p>
</sec>
</sec>
<sec id="s3" sec-type="results">
<label>3</label>
<title>Results</title>
<sec id="s3_1">
<label>3.1</label>
<title>Model performance</title>
<p>AUC values were used to evaluate the performance of the MaxEnt model. In our study, calibration of the model for <italic>M. phaseolina</italic> was satisfactory (AUC<sub>mean</sub> = 0.902 &#xb1; 0.009, <xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). This finding means that <italic>M. phaseolina</italic> current distribution characterized by the selected variables is excellent. The functional assessment of this model was supported by TSS where its value equals 0.8. This value represents a good quality modeling process, knowing that the acceptable TSS value is &#x2265; 0.5.</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>ROC curve and AUC value for the current period over the replicate runs.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g002.tif"/>
</fig>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>Contribution and effects of bioclimatic covariates</title>
<p>Following the removal of the other factors that were linked with <italic>M. phaseolina</italic>, the jackknife test was used to determine the percentages of contribution that each of the five most important climatological variables (bio_1, bio_10, bio_12, bio_4, and bio_6) had for the predictions of <italic>M. phaseolina</italic> distribution (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>, <xref ref-type="fig" rid="f4">
<bold>4B</bold>
</xref>). According to the results of this test, the climatic parameter that had the greatest impact on the distribution of fungi was the Minimum Temperature of the Coldest Month (bio_6), which had a value of 52.5%, followed by the annual mean temperature (Bio_1) with 18% contribution. The other bioclimatic factors, according to the jackknife test, were bio_4, bio_12, and bio_10 showed the lowest contribution percentage, respectively (<xref ref-type="fig" rid="f3">
<bold>Figures&#xa0;3</bold>
</xref>, <xref ref-type="fig" rid="f4">
<bold>4A</bold>
</xref>). According to the response curves and the frequency of the bioclimatic variables that contributed the most to the fungus&#x2019;s favorable bio_6 (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figures S1</bold>
</xref>, <xref ref-type="supplementary-material" rid="SM1">
<bold>S2</bold>
</xref>), the temperature range that the fungus thrived in was between 3.3 and 10 degrees Celsius (<xref ref-type="fig" rid="f4">
<bold>Figures&#xa0;4A&#x2013;C</bold>
</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Estimates of contribution percentage to species distribution for the most relevant climatological variables. Bio_6 is the minimum temperature of coldest period; Bio_1 is Annual mean air temperature; Bio_4 is the Temperature seasonality; Bio_12 is Annual precipitation; Bio_10 is the Mean temperature of the warmest quarter.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g003.tif"/>
</fig>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Selected climatic covariates: <bold>(A)</bold> The jackknife test of the five most important variables, <bold>(B)</bold> Response curve of the most effective climatic parameter (bio_6) on fungus distribution, <bold>(C)</bold> Frequency analysis of the distribution range of records against Bio_6.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g004.tif"/>
</fig>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>Limitation factor map</title>
<p>
<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref> depicts the limiting effects of the fungus through its range. On the map, in the Middle East and Australia, the fungus distribution is affected by the bio_12 (Annual precipitation) as a limitation factor, especially drought through these deserts. Temperature seasonality (bio_4) limits the existence of <italic>M. phaseolina</italic> in Brazil, the tropical zone of Africa, and parts of Southeast Asia; very high temperatures there could form a limitation to this species. In Europe, the fungus is largely influenced by the low values of the average annual temperature (bio_1). These three factors form the main limitation factor through the wide range of <italic>M. phaseolina</italic>.</p>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Map showing key limiting factors for global distribution of <italic>M. phaseolina</italic>.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g005.tif"/>
</fig>
</sec>
<sec id="s3_4">
<label>3.4</label>
<title>Two-dimensional niche analysis</title>
<p>The present study utilized the enveloped test to create the 2D niche of <italic>M. phaseolina</italic> based on the most significant environmental variables used in examining this fungus. The test was conducted between the annual mean temperature (bio_1) and annual precipitation (bio_12) (<xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref>). The results demonstrated a broad spectrum of adaptability to varying environmental conditions, with 318 observations, of which 287 (90.3%) fell within this range. The yearly temperature fluctuates between 9&#xb0;C and 28&#xb0;C, while the annual precipitation varies from 0&#xa0;mm to 2000&#xa0;mm. The observed outcome from the frequency influence of the minimum temperature during the coldest month on the fungus confirms its remarkable adaptability to a broad spectrum of cold temperatures, ranging from 3.3&#xb0;C to 10&#xb0;C (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4C</bold>
</xref>). These observations shed light on the broad prevalence of this fungus as it can grow in dry, hot deserts and cold, rainy regions.</p>
<fig id="f6" position="float">
<label>Figure&#xa0;6</label>
<caption>
<p>The two-dimensional niche of <italic>M. phaseolina</italic> between environmental covariates bio_1 (red dots) and bio_12 (green dots). The blue box represent envelope of these to variables (the range that this species could live within)The green dotes indicated the homogeneity of this points and occurrent of it on the enveloped of this species even for all 19 bioclimatic variables while the red dotes indicate the occurrence of this points outside the enveloped either for the tested variables (Bio_1 &amp; Bio 12) or one or more other bioclimatic variables.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g006.tif"/>
</fig>
</sec>
<sec id="s3_5">
<label>3.5</label>
<title>Current prediction of the potential distribution of <italic>M. phaseolina</italic>
</title>
<p>According to the distribution points and environmental variables, the current models generated by MaxEnt and DIVA-GIS showed compatible habitat suitability and agreed with the actual collected distribution data of <italic>M. phaseolina</italic> (<xref ref-type="fig" rid="f7">
<bold>Figures&#xa0;7</bold>
</xref>, <xref ref-type="fig" rid="f8">
<bold>8</bold>
</xref>). This fungus is an ecumenical cosmopolitan species that inhabits all continents. On the basis of the map, we are able to draw the conclusion that the only regions that appear to be exempt from the invasion of this fungus are those that have extremely cold weather or very dry, hot desert places. This is the case in the Sahara Desert of Africa and the Middle East, as well as in colder countries such as the northern sections of Russia and Canada. There is a wide variety of habitats that are suitable for the different regions of the planet. In Europe, the models showed that the habitat appropriateness for the fungus was extremely high and good across the entire territory, which included Spain, Italy, Turkey, Greece, and Germany. On the other hand, the northern east territories of Europe exhibited habitat suitability that was low to medium. The eastern coast and small parts of the western coast of Australia also showed high and very high risk, while its central part showed medium climate suitability. Meanwhile, New Zealand followed the same pattern. Africa had low-to-moderate climate appropriateness across the majority of the continent, with elevated and extreme hazards in the central to northern regions and southern nations of the continent. Also, small areas of Horn Africa, such as Somalia appeared highly suitable. Moreover, in Asia, the risk is high to very high mainly through China and India. In North America, the resulting current models indicated low suitability of <italic>M. phaseolina</italic> distribution over its land, except for the eastern coast of the United States and the western coast of the Mexican Gulf, which showed very high (excellent) suitability. Finally, South America appeared to have very high suitability in Brazil and Chile.</p>
<fig id="f7" position="float">
<label>Figure&#xa0;7</label>
<caption>
<p>Predicted current potential global distribution of <italic>M. phaseolina</italic> using MaxEnt.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g007.tif"/>
</fig>
<fig id="f8" position="float">
<label>Figure&#xa0;8</label>
<caption>
<p>Predicted current potential global distribution of <italic>M. phaseolina</italic> using Bioclim DIVA-GIS.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g008.tif"/>
</fig>
</sec>
<sec id="s3_6">
<label>3.6</label>
<title>Future prediction of the potential distribution of <italic>M. phaseolina</italic>
</title>
<p>The predictive models for the potential spread of <italic>M. phaseolina</italic> under four future climate change scenarios RCP 2.6 and RCP 8.5, for the years 2050 and 2070, are illustrated in <xref ref-type="fig" rid="f9">
<bold>Figure&#xa0;9</bold>
</xref>. For RCPs 2.6 and 8.5 during the period 2050 (<xref ref-type="fig" rid="f9">
<bold>Figures&#xa0;9A&#x2013;C</bold>
</xref>), the most affected continents by the prevalence of the fungus are Europe and South America. The eastern region in Europe, including Russia, and northern areas in South America will become high and very high habitat suitability. Other continents showed no great differences in the pathogenicity of the fungus in the future. On the contrary, the virulence of this fungus will decrease and can&#x2019;t invade some territories of Africa. For RCPs 2.6 and 8.5 during period 2070 (<xref ref-type="fig" rid="f9">
<bold>Figures&#xa0;9B&#x2013;D</bold>
</xref>), the predictive models illustrated a dramatic change in the fungus distribution, where there is a noticeable decrease in the spreading of the fungus in most regions in Africa, India, and the United States compared to the current status and period 2050. On the other hand, the continued increase of its distribution in Eastern Europe.</p>
<fig id="f9" position="float">
<label>Figure&#xa0;9</label>
<caption>
<p>Models of predicted global future distribution of <italic>M. phaseolina</italic> under two representative concentration pathways (RCPs): <bold>(A)</bold> 2050 for RCP 2.6; <bold>(B)</bold> 2050 for RCP 8.5; <bold>(C)</bold> 2070 for RCP 2.6, and <bold>(D)</bold> 2070 for RCP 8.5.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g009.tif"/>
</fig>
<p>The calibration maps of current and future forecasts for two different RCPs in 2050 and 2070 are used to summarize the level of changes in <italic>M. phaseolina</italic> distribution owing to global warming (<xref ref-type="fig" rid="f10">
<bold>Figure&#xa0;10</bold>
</xref>). Under low presumptive emissions of greenhouse gases (GHG) (RCP 2.6 in 2050 and 2070), the changes are slightly notable and usually not significant on all continents. However, the fungus will lose some of its habitats, especially in areas of Africa, and lose its habitat in India and Australia for the period 2050 than 2070 (<xref ref-type="fig" rid="f10">
<bold>Figures&#xa0;10A&#x2013;C</bold>
</xref>). Moreover, for the highest presumptive emissions of GHG (RCP 8.5 in 2050 and 2070), the fungus will lose its habitat suitability, especially in the equatorial and tropical regions in Africa, India in Asia, and north parts of Australia, while there is a clear gain in suitability appears in Eastern Europe (<xref ref-type="fig" rid="f10">
<bold>Figures&#xa0;10B&#x2013;D</bold>
</xref>).</p>
<fig id="f10" position="float">
<label>Figure&#xa0;10</label>
<caption>
<p>Calibration maps illustrate gain and loss in habitat suitability of <italic>M. phaseolina</italic> through the studying future scenarios against the current status with a threshold (&gt;0.5): <bold>(A)</bold> 2050 for representative concentration pathway 2.6 (RCP 2.6); <bold>(B)</bold> 2050 for RCP 8.5; <bold>(C)</bold> 2070 for RCP 2.6, and <bold>(D)</bold> 2070 for RCP 8.5.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-16-1512294-g010.tif"/>
</fig>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<label>4</label>
<title>Discussion</title>
<p>Undoubtedly, climate change has become the center of world attention in recent years. This phenomenon affects the biodiversity of living organisms, including fungi, leading to the extinction of some species, and increasing the aggressivity of others (<xref ref-type="bibr" rid="B66">Sax et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B51">Nnadi and Carter, 2021</xref>; <xref ref-type="bibr" rid="B44">Mora et&#xa0;al., 2022</xref>). One Health (OH) is the concept that the health of humans, animals, plants, and their shared ecosystem is inextricably linked (<xref ref-type="bibr" rid="B11">Centers for Disease Control and Prevention (CDC), 2022</xref>). This approach tackles burgeoning problems such as food safety (<xref ref-type="bibr" rid="B24">Garcia et&#xa0;al., 2020</xref>). Plants supply over 80% of the food consumed by humans and are the main source of nutrition for livestock, however, plant diseases often threaten the availability of plants for humans and animals (<xref ref-type="bibr" rid="B64">Savary et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B23">Food and Agriculture Organization of the United Nations (FAO), 2020</xref>). In addition, agricultural crops may act as carriers of many human pathogens and harmful fungal-based toxins, making these plants the main origin of foodborne outbreaks (<xref ref-type="bibr" rid="B59">Rizzo et&#xa0;al., 2021</xref>). Increasing the studies in these fields will demonstrate the value of the OH approach for the perception and mitigation of the negative impacts of these issues.</p>
<p>
<italic>Macrophomina phaseolina</italic> can cause substantial yield losses in crops such as <italic>Glycine max</italic> (L.) Merr. (soybean), <italic>Sorghum bicolor</italic> (L.) Moench (sorghum), and several cereals crops under high temperatures and low soil moisture (below 60%), impacting the incomes of farmers and threatening global food security (<xref ref-type="bibr" rid="B33">Kaur et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B27">Ghosh et&#xa0;al., 2018</xref>). Also, this fungus produces several types of mycotoxins, such as phaseolinone, mullein, kojic acid, and moniliformin, which negatively impact food safety for humans and animals (<xref ref-type="bibr" rid="B35">Khambhati et&#xa0;al., 2020</xref>). So, studies on species range changes in the near and long future are crucial for implementing effective management measures and conserving valuable species.</p>
<p>The present study forms a step for better elucidation of the habitat requirements of <italic>M. phaseolina</italic> and how it will respond to climate change. The results showed that the choice of environmental variables has a certain effect on the prediction of niche models. Many researchers who use the MaxEnt model to predict the distribution of species non-selectively use all the environmental factors or most environmental factors. The environmental variables, sourced from the WorldClim database, are derived from temperature and precipitation data tailored to the specific requirements of occurrence calculations. Consequently, there are unavoidable correlations between the autocorrelation of these variables and other matters (<xref ref-type="bibr" rid="B41">Merow and Silander, 2014</xref>; <xref ref-type="bibr" rid="B58">Remya et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B80">Yi et&#xa0;al., 2016</xref>). The predominant method employed for assessing model accuracy is the ROC curve method (AUC method), which is now acknowledged as a specialized model evaluator. It delivers performance evaluation data across all threshold ranges, as it is unaffected by diagnostic thresholds (<xref ref-type="bibr" rid="B74">Wang et&#xa0;al., 2018</xref>). The generated habitat suitability of our models coincided closely with the actual occurrence of fungus records with a high AUC value equal to 0.902, implying a close association between the model and the species&#x2019; ecology. Furthermore, the TSS value of 0.8 indicated that the model predictions and the dispersion of the fungus were in perfect accord (<xref ref-type="bibr" rid="B50">Naeem et&#xa0;al., 2018</xref>).</p>
<p>The most important influencing parameter to <italic>M. phaseolina</italic> distribution is the temperature, agreed with previous studies in microbial and biological organisms (<xref ref-type="bibr" rid="B38">Makori et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B68">Sohail et&#xa0;al., 2020</xref>). Temperature is a key factor in fungal growth dynamics and understanding the effect of temperature on fungal growth is an essential part of fungal physiology (<xref ref-type="bibr" rid="B6">Ancin-Murguzur et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B48">Mustafa et&#xa0;al., 2023</xref>). The majority of fungi are mesophilic where they can grow at temperatures within the range from 15&#xb0;C to 37&#xb0;C with an optimal temperature of 25&#x2013;30&#xb0;C (<xref ref-type="bibr" rid="B1">Aguilar-Paredes et&#xa0;al., 2023</xref>). Understanding the impact of temperature on fungal communities will aid the design of effective management strategies against climate change and associated microbial risks (<xref ref-type="bibr" rid="B32">Ib&#xe1;&#xf1;ez et&#xa0;al., 2023</xref>).</p>
<p>Here are a few essential considerations emphasizing the significance of limitation factor maps in SDM (<xref ref-type="bibr" rid="B75">Warren et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B19">Elith et&#xa0;al., 2010</xref>): Limitation factor maps assist in identifying the principal environmental factors that affect species dispersal. Through the examination of the correlation between species occurrence data and environmental variables, researchers can identify the most significant elements influencing habitat suitability for species. Incorporating limiting constraints into species distribution models enhances their accuracy and predictive capability. III) They offer insights on the ecological necessities and tolerances of a species. By delineating the variables that constrain its spread, scientists can enhance their comprehension of the species&#x2019; niche and the spectrum of environmental conditions in which it can endure. This knowledge enhances our comprehensive understanding of species-environment interactions and aids in evaluating species&#x2019; responses to environmental alterations. IV) They serve as essential instruments for conservation planning and management. They can assist in identifying regions with high habitat appropriateness for a species, places presently unsuited but capable of becoming suitable with appropriate interventions, and regions expected to remain unsuitable in the future due to constraints imposed by specific causes. This information is essential for prioritizing conservation initiatives, identifying crucial habitats, and executing successful management techniques (<xref ref-type="bibr" rid="B45">Moritz et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B49">Nabil et&#xa0;al., 2020</xref>).</p>
<p>The latest prediction map (<xref ref-type="fig" rid="f7">
<bold>Figure&#xa0;7</bold>
</xref>) indicates the global dissemination of <italic>M. phaseolina</italic>, corroborating numerous prior studies on its ecology and distribution (<xref ref-type="bibr" rid="B40">Marquez et&#xa0;al., 2021</xref>). Western Europe exhibits high to extremely high habitat suitability, whilst the colder nations in Eastern Europe demonstrate low suitability. This may result from the snowy conditions that inhibit fungal growth. Numerous studies have examined the impact of temperature on fungal development (<xref ref-type="bibr" rid="B13">Cesondes et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B15">Das et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B12">Cesondes et&#xa0;al., 2012</xref>). In Africa, the fungus exhibits exceptional climate suitability in equatorial, subequatorial, and tropical regions, where it endures elevated temperatures due to microsclerotia (<xref ref-type="bibr" rid="B39">Manici et&#xa0;al., 1995</xref>; <xref ref-type="bibr" rid="B2">Akhtar et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B37">Lodha et&#xa0;al., 2022</xref>). Sahara deserts and regions with elevated precipitation levels have limited habitat appropriateness, with insufficient soil moisture identified as a significant predisposing factor for the fungus (<xref ref-type="bibr" rid="B28">Goudarzi et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B36">Lodha and Mawar, 2020</xref>). India, China, and Southeast Asia exhibit exceptional compatibility for <italic>M. phaseolina</italic>. The fungus is predominantly found in the Old World; nevertheless, the results suggest that its habitat is also suitable in temperate regions of North America, southeastern South America, and western Australia.</p>
<p>The future predictive modeling and calibration maps indicate the spread of the fungus towards Eastern Europe, specifically Russia and Ukraine. The minimum temperature of the coldest month (bio_6) facilitated the fungus&#x2019;s adaptability to low temperatures (3.3&#xb0;C to 10&#xb0;C). This disruption may result from the adverse effects of global warming, which will certainly jeopardize the future production of numerous commodities, including <italic>Triticum aestivum</italic> L. (wheat) and <italic>Zea mays</italic> L. (maize) in Russia and Ukraine, representing over 30% of global wheat trade (<xref ref-type="bibr" rid="B72">US Department of Agriculture World Agricultural Supply and Demand Estimates (WASDE), 2023</xref>). Conversely, the fungus will forfeit the majority of its habitats in Africa due to the anticipated high temperature increase in equatorial regions and other areas that would be above the fungus&#x2019;s tolerance threshold. In the New World, the prevalence of fungus remains largely unchanged. These maps and data will assist specialists in plant pathology and management in assessing the future distribution risk of <italic>M. phaseolina</italic>.</p>
<p>The current study provides updated and detailed maps about the global prevalence of <italic>M. phaseolina</italic> under changing climate through the present and future periods, where this work is considered the first modeling to anticipate the global prevalence of this fungus using the robust predictive powers of MaxEnt and DIVA-GIS. In comparison to other works related to the distribution of fungi, (<xref ref-type="bibr" rid="B4">Alkhalifah et&#xa0;al., 2023</xref>). reported differences in habitat suitability between the current and future distributions of <italic>Fusarium oxysporum</italic>, especially in Europe, due to global warming. The most effective climatological parameter of <italic>F. oxysporum</italic> distribution was the annual mean temperature (Bio-1), which disagreed with our work. Also, the annual mean temperature (bio-1) formed the most contributed bioclimatological parameter to <italic>Aspergillus niger</italic> distribution (<xref ref-type="bibr" rid="B3">Alkhalifah et&#xa0;al., 2022</xref>). On the other hand, <italic>A. niger</italic> will gain new habitat in several parts of the world (the Eastern part of Europe and Central Asia) where it will form emergence medical and agricultural issues (<xref ref-type="bibr" rid="B3">Alkhalifah et&#xa0;al., 2022</xref>). From the limited works about the distribution of fungi responding to climate change, Europe will be a good habitat for emerging fungi. Also, the study of (<xref ref-type="bibr" rid="B78">Wu et&#xa0;al., 2024</xref>) utilized the MaxEnt model and ArcGIS to map suitable habitats for the invasive weeds <italic>Avena sterilis</italic> and <italic>Avena ludoviciana</italic> in Asia, highlighting the significant risk they pose to dryland crops under climate change.</p>
<p>Considering other environmental covariates involving human population, land cover, host animal distribution, and vegetation index could aid in ameliorating them (<xref ref-type="bibr" rid="B30">Hosni et&#xa0;al., 2022</xref>). However, the decreasing of future data on these variables may limit their utility in researching the effect of climate change on present distribution models. Despite it all, our research contributes to a greater understanding of the current and future distribution of <italic>M. phaseolina</italic> worldwide. The models generated in this study analyzed the impact of climate change on the existing and future prevalence of the fungus using bioclimatological factors.</p>
</sec>
<sec id="s5" sec-type="conclusions">
<label>5</label>
<title>Conclusions</title>
<p>When it comes to forecasting the future distribution of dangerous fungus, SDM is an important and powerful tool. Based on the findings of this research, it was determined that <italic>M. phaseolina</italic> will continue to spread towards Eastern Europe and some regions of South America, whereas it will be eradicated from certain locations in Africa and Asia. The current findings of this research serve as a cautionary tale about the ways in which climate change can potentially alter the geographic distribution of <italic>M. phaseolina</italic> across the globe. Therefore, in order to improve our ability to predict the spread of this fungus, we need to conduct additional research on it, with a particular focus on the habitat suitability that influences its invasion pattern. In order to combat the phenomenon of fungal adaptability to a variety of environmental conditions, it is of the utmost importance to create advanced monitoring and control measures.</p>
</sec>
</body>
<back>
<sec id="s6" sec-type="data-availability">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material</bold>
</xref>, further inquiries can be directed to the corresponding author/s.</p>
</sec>
<sec id="s7" sec-type="author-contributions">
<title>Author contributions</title>
<p>PF: Conceptualization, Writing &#x2013; original draft. DA: Funding acquisition, Writing &#x2013; review &amp; editing. SA: Methodology, Validation, Writing &#x2013; original draft. AT: Investigation, Methodology, Writing &#x2013; original draft. WH: Investigation, Supervision, Validation, Writing &#x2013; original draft.</p>
</sec>
<sec id="s8" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. We thank Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R15) Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia for funding the work.</p>
</sec>
<ack>
<title>Acknowledgments</title>
<p>We thank Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2025R15) Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia for funding of the work. The authors would thank the efforts of Marien Reduen from USAid for her help in linguistic revision of the manuscript.</p>
</ack>
<sec id="s9" 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="s10" sec-type="ai-statement">
<title>Generative AI statement</title>
<p>The author(s) declare that no Generative AI was used in the creation of this manuscript.</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>
</sec>
<sec id="s12" sec-type="supplementary-material">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fpls.2025.1512294/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fpls.2025.1512294/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="DataSheet1.zip" id="SM1" mimetype="application/zip"/>
<supplementary-material xlink:href="DataSheet2.csv" id="SM2" mimetype="text/csv"/>
</sec>
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