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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.2024.1517917</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>Straw return was more beneficial to improving saline soil quality and crop productivity than biochar in the short term</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Cong</surname>
<given-names>Ping</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1960370"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/formal-analysis/"/>
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<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Song</surname>
<given-names>Jiashen</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/formal-analysis/"/>
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<role content-type="https://credit.niso.org/contributor-roles/visualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dong</surname>
<given-names>Jianxin</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Su</surname>
<given-names>Wenyan</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Feng</surname>
<given-names>Wenhao</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2887397"/>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Zhang</surname>
<given-names>Hongyuan</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/2879724"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/methodology/"/>
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<role content-type="https://credit.niso.org/contributor-roles/supervision/"/>
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</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China (The Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences</institution>, <addr-line>Beijing</addr-line>, <country>China</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Tobacco Research Institute, Chinese Academy of Agricultural Sciences</institution>, <addr-line>Qingdao</addr-line>, <country>China</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Graduate School of Chinese Academy of Agricultural Sciences</institution>, <addr-line>Beijing</addr-line>, <country>China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Bin Song, University of Helsinki, Finland</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Guangqiang Long, Yunnan Agricultural University, China</p>
<p>Jiangwen Nie, Yangtze University, China</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Hongyuan Zhang, <email xlink:href="mailto:zhanghongyuan@caas.cn">zhanghongyuan@caas.cn</email>
</p>
</fn>
<fn fn-type="equal" id="fn003">
<p>&#x2020;These authors have contributed equally to this work</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>20</day>
<month>01</month>
<year>2025</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1517917</elocation-id>
<history>
<date date-type="received">
<day>27</day>
<month>10</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>12</day>
<month>12</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2025 Cong, Song, Dong, Su, Feng and Zhang</copyright-statement>
<copyright-year>2025</copyright-year>
<copyright-holder>Cong, Song, Dong, Su, Feng and Zhang</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>Salinized soil often exhibits high salt content and low nutrient availability, leading to the reduction of soil ecosystem function and crop productivity. Although straw return has profound effects on saline soil improvement, how soil quality index (SQI), soil ecosystem multifunctionality (EMF), and crop yield respond to different organic ameliorants remain unclear. Herein, a field experiment was established to explore the influence of various straw management strategies (no organic ameliorant, CK; corn straw return, CS; and corn straw biochar return; CB) on the saline soil functions and crop productivity. In relation to CK and CB, CS significantly improved SQI by 52% and 35%, respectively. This may be due to the decreased soil salt (especially soluble Na<sup>+</sup>) and increased available nutrients under corn straw return. Furthermore, CS increased soil EMF than CK by 71% and CB by 39%, which was caused by the increased activities of 1,4-&#x3b2;-glucosidase, &#x3b2;-1,4-<italic>N</italic>-acetyl-glucosaminidase, and leucine aminopeptidase. The linear model further supported that soil enzyme activities are positively related to available nutrient contents and negatively correlated with salt content. Moreover, the crop yield under CS significantly increased by 22% compared to CK. Also, soil quality positively influenced crop yield, with soil salt and available phosphorus being the primary influencing factors. However, crop yield was not sensitive to soil EMF. In summary, straw return was more beneficial to improving soil quality and crop productivity than biochar in the short term in saline soils.</p>
</abstract>
<kwd-group>
<kwd>saline soil</kwd>
<kwd>soil quality index</kwd>
<kwd>crop yield</kwd>
<kwd>ecosystem multi-functionality</kwd>
<kwd>straw return</kwd>
<kwd>biochar</kwd>
</kwd-group>
<counts>
<fig-count count="5"/>
<table-count count="0"/>
<equation-count count="5"/>
<ref-count count="57"/>
<page-count count="9"/>
<word-count count="3985"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Plant Nutrition</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<p>It is anticipated that the worldwide population will reach approximately 9.8 billion by 2050; the currently arable land, however, cannot meet the food requirements of the increasing population (<xref ref-type="bibr" rid="B12">FAO, 2018</xref>). It is therefore crucial to enhance crop sustainability and productivity by rehabilitating degraded land resources. Salinization-induced soil degradation is a major environmental problem that critically influences global agricultural productivity and sustainable development (<xref ref-type="bibr" rid="B30">Qadir et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B31">Sahab et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B38">Song et&#xa0;al., 2023</xref>). Currently, it is estimated approximately 1 billion ha of land worldwide is experiencing varying degrees of salinization, which constitutes approximately 10% of the total arable land (<xref ref-type="bibr" rid="B43">Wang et&#xa0;al., 2017</xref>). Furthermore, due to global climate change and poor irrigation as well as tillage management strategies, the area of land impacted by salt content is increasing annually by 1.5&#x2013;2.5 &#xd7; 10<sup>5</sup> ha (<xref ref-type="bibr" rid="B28">Mustafa et&#xa0;al., 2019</xref>). Therefore, a valid, low-cost, and environmentally friendly strategy is required for the improvement of saline soils to fulfill the development of sustainable agriculture (<xref ref-type="bibr" rid="B17">Kheir et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B27">Meena et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B37">Song et&#xa0;al., 2024</xref>).</p>
<p>Currently, straw return to the field is widely supported as an eco-friendly method for soil improvement (<xref ref-type="bibr" rid="B41">Turmel et&#xa0;al., 2015</xref>). Numerous studies suggested that straw return could enhance saline soil health via a series of pathways such as improvement of soil aeration conditions and structure, promotion of salt leaching and nutrient recycling, and provision of energy for microorganisms (<xref ref-type="bibr" rid="B42">Urraa et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B49">Xie et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B14">Ibrahim et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B53">Zhang et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B38">Song et&#xa0;al., 2023</xref>). Nevertheless, straw return generally induces a positive priming effect on native soil organic carbon (SOC) mineralization by enhancing unstable organic C and particular soil microorganisms (<xref ref-type="bibr" rid="B51">Xu et&#xa0;al., 2019</xref>). Furthermore, there has been a rising focus on the effects of biochar application on saline soil improvement in recent years. Biochar is produced through the pyrolytic carbonization of organic substances (i.e., straw) under high temperatures and anaerobic environments (<xref ref-type="bibr" rid="B20">Lehmann and Joseph, 2015</xref>; <xref ref-type="bibr" rid="B47">Wu et&#xa0;al., 2024</xref>). Because of its preferable stability, porosity, and extensive specific surface area, straw biochar has proven significant effectiveness in decreasing soil salt content, improving soil microstructure, reducing nutrient leaching and enhancing soil fertility, and boosting microbial and enzyme activities in saline soil (<xref ref-type="bibr" rid="B25">Mahmoud et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B3">Akhtar et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B2">Aborisade et&#xa0;al., 2023</xref>). However, straw biochar may also promote the oxidation of volatile substances and surface functional groups (<xref ref-type="bibr" rid="B33">Singh et&#xa0;al., 2010</xref>). Once passivated, corn straw biochar interacts with soil, creating a protective matrix (<xref ref-type="bibr" rid="B33">Singh et&#xa0;al., 2010</xref>). Although many studies have found the benefits of the application of straw and biochar on individual soil index and function, there is a limited number of comprehensive frameworks designed to assess soil quality that integrate various indexes into a synthetic index (<xref ref-type="bibr" rid="B13">Gunasekaran et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B29">Paz-Ferreiro et&#xa0;al., 2017</xref>).</p>
<p>Recently, there has been an incremental emphasis on soil ecosystem multifunctionality (EMF) for assessing the intricate interactions among biological, geochemical, and physical processes (<xref ref-type="bibr" rid="B46">Wittwer et&#xa0;al., 2021</xref>). Soil extracellular enzymes are proteins exhibiting notable catalytic activity that are released by crop roots and microorganisms (<xref ref-type="bibr" rid="B56">Zhou et&#xa0;al., 2023</xref>). These enzymes are associated with shifts in soil microbial characteristics and are able to indicate the status of soil nutrients. Consequently, they are frequently employed as key indicators for assessing soil ecosystem functions (<xref ref-type="bibr" rid="B52">Xue et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B37">Song et&#xa0;al., 2024</xref>). With the addition of different organic ameliorants, the changes in soil salt content and fertility can greatly influence microbial metabolism, thus affecting the utilization and assimilation of nutrients by microorganisms via the production of extracellular enzymes, and ultimately can exert various effects on soil EMF (<xref ref-type="bibr" rid="B39">Stark et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B53">Zhang et&#xa0;al., 2020</xref>). However, how different organic ameliorants affect soil enzyme activities and EMF by regulating soil physicochemical properties reflected in soil quality is not clear. Notably, straw and biochar additions can supply the soil with a substantial amount of exogenous nutrients, alleviate the constraints on microbial nutrient utilization, and enable crops to efficiently absorb and utilize nutrients for high yields (<xref ref-type="bibr" rid="B34">Singh et&#xa0;al., 2016</xref>). Nevertheless, due to the high C/N ratio of these organic materials, their applications also reduce crop yield by encouraging soil microorganisms to secrete extracellular enzymes, which compete with crops for available nutrients (<xref ref-type="bibr" rid="B48">Xiao et&#xa0;al., 2022</xref>). Therefore, a thorough understanding of the changes in soil quality and EMF, along with their relationship with crop yield, is essential for establishing compatible management strategies to rehabilitate saline soils.</p>
<p>In order to fulfill these knowledge gaps, a field experiment was performed in 2023 to assess the variations of soil quality, EMF, as well as crop yield under different organic ameliorants (no organic ameliorant, corn straw return, and corn straw biochar return) in saline soil. We aimed to i) identify which straw return strategy is better to improve soil quality, soil EMF, and crop productivity in saline soils in the short term and ii) determine the relationship among soil quality, soil EMF, and crop yield under different organic ameliorants in saline soils. We hypothesized that i) organic ameliorants could enhance soil quality by decreasing soil salt, increasing soil nutrient contents, and further enhancing soil EMF; ii) however, crop yield may be more sensitive to saline soil quality than soil EMF; and iii) compared to straw biochar, straw return may be better at improving saline soil quality and crop productivity in the short term.</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>Study site</title>
<p>The field experiment was carried out in Nonggao District (37&#xb0;02&#x2032;N, 118&#xb0;25&#x2032;E), Guangrao County, Shandong, China. This region exhibits a warm temperate continental monsoon climate. The average annual precipitation and temperature are 532 mm and 12.3&#xb0;C, respectively. Meteorological data in 2023 are presented in <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S1</bold>
</xref>. The soil at the experimental site is a typical coastal saline soil, and the soil properties at 0&#x2013;20 cm, before the experiment started, were as follows: pH value of 8.46, a salt content of 1.88 g kg<sup>&#x2212;1</sup>; soluble K<sup>+</sup>, Ca<sup>2+</sup>, Na<sup>+</sup>, Mg<sup>2+</sup>, Cl<sup>&#x2212;</sup>, SO<sub>4</sub>
<sup>2&#x2212;</sup>, and HCO<sub>3</sub>
<sup>&#x2212;</sup> of 0.03, 0.13, 1.52, 0.10, 0.05, 0.45, and 0.03 g kg<sup>&#x2212;1</sup>, respectively; SOC of 7.6 g kg<sup>&#x2212;1</sup>; total nitrogen (N) of 1.01 g kg<sup>&#x2212;1</sup>; and available N, phosphorus (P), and potassium (K) of 50.41, 34.98, and 393.71 mg kg<sup>&#x2212;1</sup>, respectively.</p>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Experimental design</title>
<p>The study area is an abandoned land without tillage and fertilization before 2023. The study was established in 2023 and included three treatments with random design: i) CK, no organic ameliorant; ii) CS, corn straw return; and iii) CB, corn straw biochar return. Each treatment was conducted in triplicate, with individual plots measuring 30 m<sup>2</sup> (3 m &#xd7; 10 m). Before starting the experiment, corn straw (15 t ha<sup>&#x2212;1</sup>) and corn straw biochar (8 t ha<sup>&#x2212;1</sup>) were thoroughly mixed into the 0&#x2013;10-cm soil through plowing. The corn straw returning amount was based on the high straw yield (15 t ha<sup>&#x2212;1</sup>) in the local region. Following the principle of equal C input and referring to the C content in straw and biochar (shown in <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>), the application rate of biochar was determined to be 8 t ha<sup>&#x2212;1</sup> (<xref ref-type="bibr" rid="B44">Wang et&#xa0;al., 2024</xref>). Among them, corn straw was obtained from local corn fields, dried, and crushed before application. Corn straw biochar was prepared from the abovementioned corn stover in an anaerobic environment at 700&#xb0;C (<xref ref-type="bibr" rid="B7">Cong et&#xa0;al., 2022</xref>). The nutrient content of corn straw and straw biochar is presented in <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>. The spring corn variety was Ludan 506, sown on May 10, 2023, with a row spacing of 0.7 m for wide rows, 0.5 cm for narrow rows, plant spacing, and planting density of 0.2 m, and 90,000 plants ha<sup>&#x2212;1</sup>. Additionally, 750 kg ha<sup>&#x2212;1</sup> of controlled-release fertilizer was applied with an NPK ratio of 28:6:6, and 300 kg ha<sup>&#x2212;1</sup> of urea was added during the large mouth period. After sowing and during the big mouth period, water was irrigated twice with a volume of 750 m<sup>3</sup> ha<sup>&#x2212;1</sup> each time. Other management strategies followed the standard local conventional planting methods.</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>Soil and crop sampling and analysis</title>
<p>After harvesting in 2023, 0&#x2013;20-cm soil samples were obtained using a soil drill with a three-point sampling method. After removing roots, soil samples were divided into two portions. One subsample was kept at room temperature for analysis of soil salt; soluble ions; total N; available N, P, and K; and SOC; all of them were used to calculate the soil quality index (SQI) (<xref ref-type="bibr" rid="B24">Lu, 2000</xref>; <xref ref-type="bibr" rid="B4">Bao, 2010</xref>). The second subsample was stored at 4&#xb0;C in a refrigerator for up to 2 weeks to measure soil enzyme activities, including &#x3b2;-glucosidase (BG), cellobiosidase (CE), &#x3b2;-<italic>N</italic>-acetyl-glucosaminidase (NAG), and leucine aminopeptidase (LAP), which were used to calculate the soil EMF (<xref ref-type="bibr" rid="B26">Marx et&#xa0;al., 2001</xref>). Detailed methods for measuring soil properties are provided in <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S2</bold>
</xref>. The corn grain samples (two rows, 5 m long) were collected in each plot. After air-drying, the samples were threshed to precisely assess the corn yield.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>Calculations</title>
<sec id="s2_4_1">
<label>2.4.1</label>
<title>SQI</title>
<p>To assess SQI, each soil property was initially transformed into a value (0&#x2013;1) through the appropriate equation listed below. The soil properties were then grouped into two categories. If a given soil property improved with soil quality (total N; available N, P, and K; and SOC), the &#x201c;more is better&#x201d; approach was used, applying <xref ref-type="disp-formula" rid="eq1">Equation 1</xref>. For a soil property where lower values signify better quality (salt content), the &#x201c;less is better&#x201d; method was used with <xref ref-type="disp-formula" rid="eq2">Equation 2</xref> (<xref ref-type="bibr" rid="B18">Kuzyakov et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B57">Zhou et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B37">Song et&#xa0;al., 2024</xref>):</p>
<disp-formula id="eq1">
<label>(1)</label>
<mml:math display="block" id="M1">
<mml:mrow>
<mml:mi>L</mml:mi>
<mml:mi>i</mml:mi>
<mml:mo>=</mml:mo>
<mml:mfrac>
<mml:mi>v</mml:mi>
<mml:mrow>
<mml:msub>
<mml:mi>v</mml:mi>
<mml:mrow>
<mml:mi>m</mml:mi>
<mml:mi>a</mml:mi>
<mml:mi>x</mml:mi>
</mml:mrow>
</mml:msub>
</mml:mrow>
</mml:mfrac>
</mml:mrow>
</mml:math>
</disp-formula>
<disp-formula id="eq2">
<label>(2)</label>
<mml:math display="block" id="M2">
<mml:mrow>
<mml:mi>L</mml:mi>
<mml:mi>i</mml:mi>
<mml:mo>=</mml:mo>
<mml:mfrac>
<mml:mrow>
<mml:msub>
<mml:mi>v</mml:mi>
<mml:mrow>
<mml:mi>m</mml:mi>
<mml:mi>i</mml:mi>
<mml:mi>n</mml:mi>
</mml:mrow>
</mml:msub>
</mml:mrow>
<mml:mi>v</mml:mi>
</mml:mfrac>
</mml:mrow>
</mml:math>
</disp-formula>
<p>where <italic>Li</italic> refers to the linear score of soil property <italic>i</italic>, and <italic>v</italic>, <italic>v<sub>max</sub>
</italic>, and <italic>v<sub>min</sub>
</italic> refer to the measured, maximum, and minimum values of the soil property <italic>i</italic>, respectively.</p>
<p>SQI was then determined using the SQI-area method. It involves evaluating the area encompassed through the radar diagram created from all soil properties (Kuzyakov et&#xa0;al., 2020):</p>
<disp-formula id="eq3">
<label>(3)</label>
<mml:math display="block" id="M3">
<mml:mrow>
<mml:mi>S</mml:mi>
<mml:mi>Q</mml:mi>
<mml:mi>I</mml:mi>
<mml:mo>=</mml:mo>
<mml:mn>0.5</mml:mn>
<mml:mo>&#xd7;</mml:mo>
<mml:mstyle displaystyle="true">
<mml:msubsup>
<mml:mo>&#x2211;</mml:mo>
<mml:mi>i</mml:mi>
<mml:mi>n</mml:mi>
</mml:msubsup>
<mml:mrow>
<mml:mi>L</mml:mi>
<mml:msup>
<mml:mi>i</mml:mi>
<mml:mn>2</mml:mn>
</mml:msup>
</mml:mrow>
</mml:mstyle>
<mml:mo>&#xd7;</mml:mo>
<mml:mtext>sin</mml:mtext>
<mml:mrow>
<mml:mo stretchy="false">(</mml:mo>
<mml:mrow>
<mml:mfrac>
<mml:mrow>
<mml:mn>2</mml:mn>
<mml:mo>&#xd7;</mml:mo>
<mml:mi>&#x3c0;</mml:mi>
</mml:mrow>
<mml:mi>n</mml:mi>
</mml:mfrac>
</mml:mrow>
<mml:mo stretchy="false">)</mml:mo>
</mml:mrow>
</mml:mrow>
</mml:math>
</disp-formula>
<p>where <italic>n</italic> represents the total number of soil properties.</p>
</sec>
<sec id="s2_4_2">
<label>2.4.2</label>
<title>Soil EMF</title>
<p>Enzyme activities were utilized to evaluate soil ecosystem multifunctionality (<xref ref-type="bibr" rid="B9">Delgado-Baquerizo et&#xa0;al., 2020</xref>). The Z-score approach was applied to normalize each soil enzyme activity, after which the average values were calculated (<xref ref-type="bibr" rid="B8">Delgado-Baquerizo et&#xa0;al., 2016</xref>):</p>
<disp-formula id="eq4">
<label>(4)</label>
<mml:math display="block" id="M4">
<mml:mrow>
<mml:msub>
<mml:mi>Z</mml:mi>
<mml:mi>i</mml:mi>
</mml:msub>
<mml:mo>=</mml:mo>
<mml:mfrac>
<mml:mrow>
<mml:mi>x</mml:mi>
<mml:mo>&#x2212;</mml:mo>
<mml:msub>
<mml:mi>m</mml:mi>
<mml:mi>i</mml:mi>
</mml:msub>
</mml:mrow>
<mml:mrow>
<mml:mi>s</mml:mi>
<mml:mi>d</mml:mi>
</mml:mrow>
</mml:mfrac>
</mml:mrow>
</mml:math>
</disp-formula>
<disp-formula id="eq5">
<label>(5)</label>
<mml:math display="block" id="M5">
<mml:mrow>
<mml:msub>
<mml:mi>Z</mml:mi>
<mml:mrow>
<mml:mi>S</mml:mi>
<mml:mi>c</mml:mi>
<mml:mi>o</mml:mi>
<mml:mi>r</mml:mi>
<mml:mi>e</mml:mi>
</mml:mrow>
</mml:msub>
<mml:mo>=</mml:mo>
<mml:mi>a</mml:mi>
<mml:mi>v</mml:mi>
<mml:mi>e</mml:mi>
<mml:mi>r</mml:mi>
<mml:mi>a</mml:mi>
<mml:mi>g</mml:mi>
<mml:mi>e</mml:mi>
<mml:mrow>
<mml:mo stretchy="false">(</mml:mo>
<mml:mrow>
<mml:msub>
<mml:mi>Z</mml:mi>
<mml:mi>i</mml:mi>
</mml:msub>
</mml:mrow>
<mml:mo stretchy="false">)</mml:mo>
</mml:mrow>
</mml:mrow>
</mml:math>
</disp-formula>
<p>where <italic>Z<sub>i</sub>
</italic> refers to enzyme activity, and <italic>x</italic>, <italic>m<sub>i</sub>
</italic>, and <italic>s<sub>d</sub>
</italic> correspond to the measured enzyme activity, mean enzyme activity, and its standard deviation, respectively.</p>
</sec>
</sec>
<sec id="s2_5">
<label>2.5</label>
<title>Statistical analysis</title>
<p>One-way analysis of variance (ANOVA) was carried out to explore the effect of organic ameliorants (CK, CS, and CB) on soil physicochemical properties, enzyme activities, and corn yield. Multiple comparisons were conducted using Fisher&#x2019;s least significant difference (LSD) test, with a significance threshold of <italic>p</italic> &lt; 0.05. The relationships among SQI, soil EMF, and crop yield were investigated using a linear regression model. Random Forest analysis was carried out to confirm the important factors of crop yield among soil physicochemical properties using R (&#x201c;randomForest&#x201d; package). All figures were drawn using OriginPro 2021, and statistical analyses were carried out using DPS 9.01.</p>
</sec>
</sec>
<sec id="s3" sec-type="results">
<label>3</label>
<title>Results</title>
<sec id="s3_1">
<label>3.1</label>
<title>Soil physicochemical properties and SQI</title>
<p>CS and CB decreased soil salt content by 22% and 18%, respectively; CS increased soil available N, available P, and available K by 91%, 49%, and 25% as compared to CK, respectively (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). CS then improved SQI by 52% as compared to CK (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). Furthermore, the SQI was 35% higher in CS than in CB by 35%.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Soil physicochemical properties at 0&#x2013;20 cm as affected by organic ameliorants. Organic ameliorants were as follows: CK, no organic ameliorant; CS, corn straw return; and CB, corn straw biochar return. N, nitrogen; P, phosphorus; K, potassium; SOC, soil organic carbon. Bars were SE, and letters were least significant difference (LSD) at <italic>p</italic> &lt; 0.05 (n = 3).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1517917-g001.tif"/>
</fig>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Soil physicochemical property scores at the 0&#x2013;20 cm under organic ameliorants <bold>(A)</bold> and soil quality index (SQI) under organic ameliorants <bold>(B)</bold>. Organic ameliorants were as follows: CK, no organic ameliorant; CS, corn straw return; CB, corn straw biochar return. N, nitrogen; P, phosphorus; K, potassium; SOC, soil organic carbon. Bars are SE, and letters are least significant difference (LSD) at <italic>p</italic> &lt; 0.05 (n = 3).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1517917-g002.tif"/>
</fig>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>Soil enzyme activity</title>
<p>Soil enzyme activity responded differently to various organic ameliorants (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>). CS significantly increased the activities of BG, NAG, and LAP by 33%, 32%, and 13%, respectively; CB significantly increased the activities of CE and NAG by 22% and 11% as compared to CK, respectively (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2A</bold>
</xref>). Furthermore, compared to CB, CS increased BG, NAG, and LAP activities by 70%, 19%, and 15%, respectively (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Soil enzyme activity at 0&#x2013;20 cm under organic ameliorants <bold>(A)</bold>. Pairwise comparisons between soil properties at 0&#x2013;20 cm <bold>(B)</bold>. Organic ameliorants were as follows: CK, no organic ameliorant; CS, corn straw return; CB, corn straw biochar return. BG, 1,4-&#x3b2;-glucosidase; CE, cellobiosidase; NAG, &#x3b2;-1,4-<italic>N</italic>-acetyl-glucosaminidase; LAP, leucine aminopeptidase. Bars were SE, and letters were least significant difference (LSD) at <italic>p</italic> &lt; 0.05 (n = 3). *<italic>p</italic> &lt; 0.05, **<italic>p</italic> &lt; 0.01.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1517917-g003.tif"/>
</fig>
<p>Pairwise comparisons suggested that there are negative correlations between NAG activity and salt content (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3B</bold>
</xref>); positive correlations between the activities of BG, NAG, LAP, and available K; and positive correlations between the NAG activity and available N and P (<italic>p</italic> &lt; 0.05).</p>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>Soil ecosystem multifunctionality</title>
<p>CS increased soil EMF by 71% and 39% as compared to CK and CB, respectively (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4A</bold>
</xref>). The linear regression analysis indicated a positive correlation between soil EMF and SQI (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4B</bold>
</xref>).</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Soil ecosystem multifunctionality (EMF) <bold>(A)</bold> and its relationship with soil quality index (SQI) <bold>(B)</bold> at 0&#x2013;20 cm as affected by organic ameliorants. Organic ameliorants were as follows: CK, no organic ameliorant; CS, corn straw return; CB, corn straw biochar return. Bars were SE, and letters were least significant difference (LSD) at <italic>p</italic> &lt; 0.05 (n = 3).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1517917-g004.tif"/>
</fig>
</sec>
<sec id="s3_4">
<label>3.4</label>
<title>Crop yield and its driving factors</title>
<p>Compared with CK, crop yield increased by 22% under CS (<italic>p</italic> &lt; 0.05, <xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5A</bold>
</xref>). Nevertheless, there was no difference in crop yield between CB and CS (<italic>p</italic> &gt; 0.05). The linear regression indicated that crop yield was positively correlated with SQI (<italic>p</italic> &lt; 0.05), while the relationship between crop yield and soil EMF was not significant (<italic>p</italic> &gt; 0.05, <xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5B</bold>
</xref>). The dominating factors of soil physicochemical properties related to crop yield were available P and salt content (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5C</bold>
</xref>).</p>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Crop yield <bold>(A)</bold> and its relationship with soil quality index (SQI) <bold>(B)</bold> at 0&#x2013;20-cm depth as affected by organic ameliorants. Random Forest indicates predictor importance (% of increase of MSE) of soil physicochemical properties on crop yield <bold>(C)</bold>. Organic ameliorants were as follows: CK, no organic ameliorant; CS, corn straw return; CB, corn straw biochar return. MSE, mean squared error. Bars are SE, and letters are least significant difference (LSD) at p &lt; 0.05(n = 3). *p &lt; 0.05.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1517917-g005.tif"/>
</fig>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<label>4</label>
<title>Discussion</title>
<sec id="s4_1">
<label>4.1</label>
<title>Effects of organic ameliorants on soil quality</title>
<p>Soil quality refers to the ability of soil to operate efficiently within ecosystem limits, supporting biological productivity, preserving environmental quality, and supporting the health of plants, animals, and humans (<xref ref-type="bibr" rid="B10">Doran and Parkin, 1994</xref>; <xref ref-type="bibr" rid="B23">Liu et&#xa0;al., 2023</xref>). Our results suggested that saline soil quality considerably increased under corn straw return (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). This may be due to the decreased soil salt and increased available nutrient contents (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). In the decomposition process of corn straw, organic acids were released, which subsequently displaced Na<sup>+</sup> on soil colloids, ultimately decreasing salt content (<xref ref-type="bibr" rid="B11">Fan et&#xa0;al., 2013</xref>). This was also supported by the decreased soil soluble Na<sup>+</sup> content under straw return treatment (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S2</bold>
</xref>). Furthermore, applying corn straw could enhance soil aggregation and progressively rehabilitate soil structure (<xref ref-type="bibr" rid="B53">Zhang et&#xa0;al., 2020</xref>), thereby promoting soil salt leaching (<xref ref-type="bibr" rid="B5">Benbi and Senapati, 2010</xref>; <xref ref-type="bibr" rid="B1">Abdelrhman et&#xa0;al., 2021</xref>). The improvement of soil saline environment and physical structure, on the one hand, increased soil nutrient (i.e., N, P, and K) availability by increasing crop root biomass and, on the other hand, created a suitable niche for microbial growth and subsequently enhanced enzyme activity to activate nutrient transformation and immobilization (<xref ref-type="bibr" rid="B35">Song et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B45">Wang et&#xa0;al., 2021</xref>). Moreover, the decomposition of corn straw produced organic matter, such as humus, which possessed an extensive surface area and significant adsorption capability (<xref ref-type="bibr" rid="B6">Chen et&#xa0;al., 2020</xref>). This, in turn, led to a decrease in nutrient leaching; consequently (<xref ref-type="bibr" rid="B50">Xu et&#xa0;al., 2020</xref>), an increase in soil nutrient contents was observed under straw return. Although the organic matter contained in the corn straw was continuously decomposed and released, which increased SOC and available nutrient contents (<xref ref-type="bibr" rid="B40">Tian et&#xa0;al., 2020</xref>), corn straw return could also contribute to a positive priming effect on the mineralization of persistent SOC (<xref ref-type="bibr" rid="B51">Xu et&#xa0;al., 2019</xref>). Therefore, SOC remained stable when straw was returned to the soils in our case.</p>
<p>The application of straw biochar, with its porous structure, large surface area, and strong hydroxyl group adsorption capacity, could enhance the leaching of both salts and sodium (<xref ref-type="bibr" rid="B19">Lakhdar et&#xa0;al., 2009</xref>) and, as a consequence, decreased soil salt content under straw biochar return (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). The reduced soil soluble Na<sup>+</sup> content under straw biochar return treatment also supported this point (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S2</bold>
</xref>). Nevertheless, the changes in available nutrients and SOC contents were not significant after biochar addition (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). This may be due to the addition of corn straw biochar that stimulated the oxidation of volatile substances and surface functional groups (<xref ref-type="bibr" rid="B33">Singh et&#xa0;al., 2010</xref>). Subsequently, the passivated corn straw biochar interacted with the soil, forming a protective matrix (<xref ref-type="bibr" rid="B33">Singh et&#xa0;al., 2010</xref>). The C contained in corn straw biochar could also alter the abundance, composition, and activities of specific microorganisms, leading to the mineralization of native SOC. Afterward, there was no remarkable variation in SOC content under corn straw biochar return. Overall, corn straw return could quickly improve soil quality by decreasing soil salt and improving available nutrient contents, while biochar application could not improve soil quality in saline soils in the short term.</p>
<p>Here, it should be noted that the higher availability of mineral elements (available N and P) with the application of organic ameliorants may lead to environmental pollution such as nitrate leaching and N<sub>2</sub>O emissions. Further studies are required to evaluate the effect of organic ameliorants on greenhouse gas emissions and nitrate leaching.</p>
</sec>
<sec id="s4_2">
<label>4.2</label>
<title>Effects of organic ameliorants on soil EMF</title>
<p>Understanding soil functions is essential for assessing the ecological benefits of various agricultural management strategies (<xref ref-type="bibr" rid="B46">Wittwer et&#xa0;al., 2021</xref>). In our study, corn straw return enhanced soil EMF compared with CK (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>), which indicated that corn straw return may mitigate some of the adverse impacts associated with chemical fertilization (<xref ref-type="bibr" rid="B46">Wittwer et&#xa0;al., 2021</xref>). This result could be attributed to the application of labile C sources under corn straw return, which enhanced the activities of enzymes involved in C and N acquisition (<xref ref-type="bibr" rid="B55">Zhou et&#xa0;al., 2024</xref>). This, in turn, stimulated the secretion of enzymes by microbes and ultimately led to the increase of soil EMF (<xref ref-type="bibr" rid="B15">Jia et&#xa0;al., 2022</xref>). Additionally, enzyme activities were significantly influenced by environmental factors such as soil salt content and nutrient availability (<xref ref-type="bibr" rid="B22">Liang et&#xa0;al., 2005</xref>). The increase in microbial activity caused by decreasing salt content and improving nutrient availability under organic ameliorants also led to the enhancement of enzyme activity of nutrient transformation to further increase nutrient immobilization (<xref ref-type="bibr" rid="B35">Song et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B45">Wang et&#xa0;al., 2021</xref>). The linear model showing that enzyme activities were positively related to available nutrient contents and negatively related to salt content supported these points (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3B</bold>
</xref>). Therefore, the improvement of soil salt and available nutrient contents under corn straw return could greatly influence microbial metabolism (<xref ref-type="bibr" rid="B53">Zhang et&#xa0;al., 2020</xref>), thus promoting the utilization and assimilation of nutrients by microorganisms through the production of enzymes (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>), and then had a positive effect on soil EMF (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>; <xref ref-type="bibr" rid="B53">Zhang et&#xa0;al., 2020</xref>). This was also confirmed by a significant positive correlation between soil quality and EMF (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3B</bold>
</xref>). Nevertheless, there was no remarkable variation in soil EMF under corn straw biochar return (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>). The potential explanation was that corn straw biochar had the ability to reduce microbial growth and turnover by fixing soil nutrients, which in turn inhibited the increase of enzyme activities and soil EMF (<xref ref-type="bibr" rid="B16">Kalu et&#xa0;al., 2024</xref>).</p>
</sec>
<sec id="s4_3">
<label>4.3</label>
<title>Effects of organic ameliorants on crop yield</title>
<p>The primary objective of improving saline soil is to elevate soil quality and, more importantly, to attain a higher crop yield within a shorter term (<xref ref-type="bibr" rid="B32">Shrivastava and Kumar, 2015</xref>). In our study, corn straw return remarkably improved crop yield (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5A</bold>
</xref>). This may be because the addition of straw improved soil quality and facilitated the efficient absorption and utilization of nutrients by crops, thus increasing crop yield (<xref ref-type="bibr" rid="B36">Song et&#xa0;al., 2022</xref>). It was further confirmed by the significant positive correlation between SQI and crop yield (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5B</bold>
</xref>). The Random Forest result further suggested that soil salt and available P were the main factors influencing crop yield (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5C</bold>
</xref>). First, higher salt content previously could disrupt the dynamic water balance in the crop, which in turn affects their nutrient balance. After the straw return, the improvement of soil saline environment and physical structure also increased root development and further crop yield by increasing soil nutrients (i.e., N, P, and K) (<xref ref-type="bibr" rid="B54">Zhao et&#xa0;al., 2020</xref>). Second, the straw-induced enhanced P may overwhelm the severe P deficiency caused by strong adsorption between soil particles and P elements in saline soils (<xref ref-type="bibr" rid="B21">Li and Li, 2022</xref>). Unlike soil quality, crop yield was not affected by soil EMF (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S3</bold>
</xref>). This suggested that an increase in soil enzyme activity may not necessarily be advantageous for crop growth because of the high C/N ratio in biochar, which may intensify the competition between soil microorganisms and crops for available nutrients through the secretion of enzymes, thereby potentially negatively impacting crop growth and yield under biochar addition (<xref ref-type="bibr" rid="B48">Xiao et&#xa0;al., 2022</xref>). Therefore, compared to corn straw biochar return, corn straw return was more likely to improve saline soil quality in the short term, thereby enhancing EMF and crop yield, and was more conducive to rapid improvement of saline soils.</p>
</sec>
</sec>
<sec id="s5" sec-type="conclusion">
<label>5</label>
<title>Conclusion</title>
<p>Corn straw return reduced soil salt, increased available nutrient contents, and then increased soil quality than CK and corn straw biochar return. Furthermore, soil salt (mainly soluble Na<sup>+</sup>) and available nutrient contents were negatively correlated and positively correlated with enzyme activities, respectively. Therefore, enzyme activities and soil EMF increased under corn straw return than that under CK and corn straw biochar return. Moreover, higher soil quality also led to higher crop yield. Compared to CK and straw biochar return, straw return significantly increased crop yield. The Random Forest result suggested that soil salt and available phosphorus contents were the main driving factors for improving soil quality. In conclusion, straw return was more beneficial for improving soil quality and ecosystem multifunctionality, as well as crop yield, and providing references for rapid improvement of saline soils.</p>
</sec>
</body>
<back>
<sec id="s6" sec-type="data-availability">
<title>Data availability statement</title>
<p>The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.</p>
</sec>
<sec id="s7" sec-type="author-contributions">
<title>Author contributions</title>
<p>PC: Data curation, Formal analysis, Investigation, Project administration, Resources, Visualization, Writing &#x2013; original draft. JS: Data curation, Formal analysis, Investigation, Visualization, Writing &#x2013; original draft. JD: Investigation, Writing &#x2013; original draft. WS: Investigation, Writing &#x2013; original draft. WF: Investigation, Writing &#x2013; original draft. HZ: Conceptualization, Methodology, Project administration, Supervision, Validation, Writing &#x2013; review &amp; editing.</p>
</sec>
<sec id="s8" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the National Natural Science Foundation of China (No. U24A20359; 32301969), the National Key Research and Development Plan of China (2021YFD1901002), the Natural Science Foundation of Shandong Province (No. ZR2021QD036), the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAAS-ZDRW202407), the earmarked fund for CARS-02-24, and the open project of State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, the Institute of Agricultural Resources, and Regional Planning, Chinese Academy of Agricultural Sciences (No. EUAL-2023-05).</p>
</sec>
<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.2024.1517917/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fpls.2024.1517917/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="DataSheet1.docx" id="SM1" mimetype="application/vnd.openxmlformats-officedocument.wordprocessingml.document"/>
</sec>
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