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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id>
<journal-title>Frontiers in Microbiology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Microbiol.</abbrev-journal-title>
<issn pub-type="epub">1664-302X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
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<article-meta>
<article-id pub-id-type="doi">10.3389/fmicb.2023.1237534</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Microbiology</subject>
<subj-group>
<subject>Editorial</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Editorial: New insights into the influences of soil nutrients on plant-fungal symbiosis in agro- and forest ecosystems</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name><surname>Sun</surname> <given-names>Kai</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="corresp" rid="c001"><sup>&#x0002A;</sup></xref>
<xref ref-type="author-notes" rid="fn002"><sup>&#x02020;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/334154/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Zhan</surname> <given-names>Fang-Dong</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1910306/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Shi</surname> <given-names>Yu</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1648392/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Zhou</surname> <given-names>Jiayu</given-names></name>
<xref ref-type="aff" rid="aff6"><sup>6</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1820123/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Zhou</surname> <given-names>Jun</given-names></name>
<xref ref-type="aff" rid="aff7"><sup>7</sup></xref>
<xref ref-type="author-notes" rid="fn003"><sup>&#x02020;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/242271/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Peng</surname> <given-names>Long</given-names></name>
<xref ref-type="aff" rid="aff8"><sup>8</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/1851710/overview"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University, Nanjing</institution>, <addr-line>Jiangsu</addr-line>, <country>China</country></aff>
<aff id="aff2"><sup>2</sup><institution>College of Resources and Environment, Yunnan Agricultural University</institution>, <addr-line>Kunming</addr-line>, <country>China</country></aff>
<aff id="aff3"><sup>3</sup><institution>State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University</institution>, <addr-line>Kaifeng</addr-line>, <country>China</country></aff>
<aff id="aff4"><sup>4</sup><institution>Henan Dabieshan National Field Observation and Research Station of Forest Ecosystem</institution>, <addr-line>Zhengzhou</addr-line>, <country>China</country></aff>
<aff id="aff5"><sup>5</sup><institution>Xinyang Academy of Ecological Research</institution>, <addr-line>Xinyang</addr-line>, <country>China</country></aff>
<aff id="aff6"><sup>6</sup><institution>Institute of Botany, Jiangsu Province and Chinese Academy of Sciences</institution>, <addr-line>Nanjing</addr-line>, <country>China</country></aff>
<aff id="aff7"><sup>7</sup><institution>Chrono-Environnement UMR 6249, CNRS, Universit&#x000E9; Bourgogne Franche-Comt&#x000E9;</institution>, <addr-line>Besan&#x000E7;on</addr-line>, <country>France</country></aff>
<aff id="aff8"><sup>8</sup><institution>Research Institute of Subtropical Forestry, Chinese Academy of Forestry</institution>, <addr-line>Hangzhou</addr-line>, <country>China</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited and reviewed by: Trevor Carlos Charles, University of Waterloo, Canada</p></fn>
<corresp id="c001">&#x0002A;Correspondence: Kai Sun <email>sunkainnu&#x00040;sina.cn</email></corresp>
<fn fn-type="other" id="fn002"><p>&#x02020;ORCID: Kai Sun <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0003-2746-4131">orcid.org/0000-0003-2746-4131</ext-link></p></fn>
<fn fn-type="other" id="fn003"><p>Jun Zhou <ext-link ext-link-type="uri" xlink:href="https://orcid.org/0000-0003-3618-1037">orcid.org/0000-0003-3618-1037</ext-link></p></fn></author-notes>
<pub-date pub-type="epub">
<day>18</day>
<month>07</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>14</volume>
<elocation-id>1237534</elocation-id>
<history>
<date date-type="received">
<day>09</day>
<month>06</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>05</day>
<month>07</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2023 Sun, Zhan, Shi, Zhou, Zhou and Peng.</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Sun, Zhan, Shi, Zhou, Zhou and Peng</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>
<related-article id="RA1" related-article-type="commentary-article" xlink:href="https://www.frontiersin.org/research-topics/43603/new-insights-into-the-influences-of-soil-nutrients-on-plant-fungal-symbiosis-in-agro-and-forest-ecosystems" ext-link-type="uri">Editorial on the Research Topic <article-title>New insights into the influences of soil nutrients on plant-fungal symbiosis in agro- and forest ecosystems</article-title></related-article>
<kwd-group>
<kwd>soil nutrient availability</kwd>
<kwd>nutrient forms</kwd>
<kwd>symbiotic fungi</kwd>
<kwd>arbuscular mycorrhizal fungi</kwd>
<kwd>fungal endophyte</kwd>
<kwd>fungal community</kwd>
<kwd>plant-fungal symbiosis</kwd>
<kwd>agroecosystem and forest ecosystem</kwd>
</kwd-group>
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<fig-count count="0"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="24"/>
<page-count count="3"/>
<word-count count="2439"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Microbe and Virus Interactions with Plants</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<p>Symbiotic fungi are widely distributed and form associations with over 90% of terrestrial plant species, playing an essential role in global agro- and forest ecosystems (Behie and Bidochka, <xref ref-type="bibr" rid="B1">2014</xref>). These symbionts provide various benefits to host plants, including increased biomass accumulation (Hiruma et al., <xref ref-type="bibr" rid="B8">2016</xref>), enhanced nutrient uptake (Guether et al., <xref ref-type="bibr" rid="B6">2009</xref>; Fochi et al., <xref ref-type="bibr" rid="B5">2017</xref>), and improved environmental adaptation (Sui et al., <xref ref-type="bibr" rid="B21">2019</xref>). In return, host plants offer suitable habitats and accessible photosynthate for fungal survival and reproduction (Siegel et al., <xref ref-type="bibr" rid="B19">1987</xref>; Jiang et al., <xref ref-type="bibr" rid="B9">2017</xref>). However, in natural ecosystems, plant-fungal symbioses often face changing soil conditions, particularly variations in nutrient status (Sun et al., <xref ref-type="bibr" rid="B23">2020</xref>, <xref ref-type="bibr" rid="B22">2022</xref>). Different nutrient availabilities, forms, and compositions can significantly affect plant metabolism, growth, and immunity, which are crucial for maintaining the interplay between plants and fungi (Saikkonen et al., <xref ref-type="bibr" rid="B16">2004</xref>; S&#x000E1;nchez-Bel et al., <xref ref-type="bibr" rid="B17">2018</xref>). Conversely, soil nutrient status can influence the community composition of soil fungi, thereby impacting the establishment of symbionts.</p>
<p>The goal of this Research Topic is to showcase the latest studies focusing on the global effects of soil nutrients on plant-fungi interactions, enhancing our understanding of the mechanisms underlying the colonization and community dynamics of symbiotic fungi during their interaction with host plants across various species/genotypes, soil types, and nutrient levels and forms. The Research Topic covers studies on arbuscular mycorrhizal fungi (AMF), fungal endophytes and the plant-associated fungal community.</p>
<sec id="s1">
<title>Insights into the impact of soil nutrients on AMF symbiosis</title>
<p>Ancient AMF symbioses can be seen as the bridge between plants and soils (Saia and Jansa, <xref ref-type="bibr" rid="B15">2022</xref>; Kuyper and Jansa, <xref ref-type="bibr" rid="B10">2023</xref>). The AMF symbionts are influenced by the forms and levels of nutrients in the soil, including nitrogen (N), phosphorus (P), and potassium (K). <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2022.906818">Yu et al.</ext-link> pointed out that AMF are sensitive to N addition over short timescales (1 year). Beneficial AMF associations are promoted under N-deficient conditions (Bonfante and Genre, <xref ref-type="bibr" rid="B2">2010</xref>; Sanchez-Bel et al., <xref ref-type="bibr" rid="B18">2016</xref>; S&#x000E1;nchez-Bel et al., <xref ref-type="bibr" rid="B17">2018</xref>). Additionally, ammonium reduced AMF colonization levels in numerous plant species compared to nitrate (Pattinson et al., <xref ref-type="bibr" rid="B14">2000</xref>).</p>
<p>Two noteworthy perspectives highlight the important roles of AMF symbiosis in plant invasion in agro-ecosystems based on greenhouse experiments. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2023.1131797">Du et al.</ext-link> revealed that the AMF <italic>Septoglomus constrictum</italic> provides host plants with higher N and P accumulation, conferring invasive plants with greater advantages over native congeners. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2023.1160631">Chen et al.</ext-link>, through the analysis of AMF community associated with the invasive species <italic>Solidago canadensis</italic> and its native congener <italic>S. decurrens</italic>, clarified that AMF could confer invasive plants with greater advantages over native congeners, dependent on the forms of P in the soil.</p>
<p>Inorganic orthophosphate (Pi) is the available form of P that plants can acquire and utilize. However, Pi is often insufficient in the field due to its low solubility and relative immobilization (Nagy et al., <xref ref-type="bibr" rid="B13">2009</xref>). Under P starvation, AMF can efficiently promote Pi uptake and homeostasis in host plants (Dierks et al., <xref ref-type="bibr" rid="B3">2021</xref>). In this Research Topic, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2022.1114089">Zhang et al.</ext-link> identify a HLH domain containing transcription factor, <italic>RiPho4</italic>, from <italic>Rhizophagus irregularis</italic>. Through subcellular localization, yeast one-hybrid experiments, and using virus-induced gene silencing approaches, the authors demonstrated that <italic>RiPho4</italic> acts as a transcriptional activator in AMF to maintain arbuscule development and regulate Pi uptake in host plants during Pi starvation. This study provides new insights into the mechanisms underlying how AMF regulates Pi uptake in host plants under Pi deficiency.</p>
<p>Apart from N and Pi, the AMF-plant interaction is also sensitive to changes in soil K nutrient (Han et al., <xref ref-type="bibr" rid="B7">2023</xref>). In a greenhouse experiment, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2022.1075957">Yuan et al.</ext-link> investigated sweet potato (<italic>Ipomoea batatas</italic> (L.) Lam.]), a versatile crop with high K requirements for enhanced yield. Their study showed that K application and the presence of AMF <italic>Claroideoglomus etunicatum</italic> exhibited a synergistic effect on the root development and K acquisition of the &#x0201C;Xu28&#x0201D; variety of sweet potato, which has high K use efficiency, resulting in significant yield promotion. These results, combined with previous studies, expand our knowledge of the influences of soil nutrients on plant-AMF symbiosis.</p></sec>
<sec id="s2">
<title>Impact of heavy metal contamination on plant-fungal interactions</title>
<p>Heavy metal contamination in soil is a pressing global issue (Marrugo-Negrete et al., <xref ref-type="bibr" rid="B11">2017</xref>) that affects plant-fungal interactions (Motaharpoor et al., <xref ref-type="bibr" rid="B12">2019</xref>). Dark septate endophytes (DSEs) are ubiquitous colonizers of plant roots in various terrestrial ecosystems, often found in stressful environments, especially heavy metal-polluted soils (Su et al., <xref ref-type="bibr" rid="B20">2021</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2023.1165131">Wang et al.</ext-link> highlighted the ability of <italic>Exophiala pisciphila</italic> H93, a beneficial dark septate endophyte which colonizes maize roots, to withstand cadmium exposure without compromising its growth-promotion effect on maize. They found that H93 colonization enhances plant resistance to heavy metal by influencing the expression of genes involved in signal transduction, hormonal pathway, and glutathione metabolism.</p></sec>
<sec id="s3">
<title>Influence of soil nutrients on plant-associated fungal communities</title>
<p>The response of the plant-associated fungal community to global changes plays a crucial role in understanding carbon and N cycling processes in agro- and forest ecosystems (Falkowski et al., <xref ref-type="bibr" rid="B4">2008</xref>). In this Research Topic, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2022.906818">Yu et al.</ext-link> demonstrated that the interaction between N addition and rainfall patterns has significant effects on soil fungal diversity in a grassland ecosystem. Similarly, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2023.1106888">Zhao et al.</ext-link> showed in a forest ecosystem that climate factors, such as temperature and precipitation, significantly influence dominant fungal genera and functional guilds in soil, particularly ectomycorrhizal fungi. Furthermore, fungal diversity and composition are strongly influenced by seasonal variation in soil nutrients, including total N and available P. The effect of vegetation type on rhizosphere microbes is also of great interest across different ecosystems. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2023.1129471">Liu et al.</ext-link> compared fungal communities in the rhizosphere of three typical vegetation types (herb, shrubs, and arbors). They discovered that the fungal community structure in the rhizosphere can vary across vegetation types and is primarily governed by deterministic processes. Additionally, plant metabolism has a significant impact on the plant-associated microbiome (Trivedi et al., <xref ref-type="bibr" rid="B24">2020</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fmicb.2022.1015038">Zhu et al.</ext-link> demonstrated that by applying exogenous salicylic acid, beneficial rhizosphere microorganisms were selectively enriched to enhance watermelon resistance to <italic>Fusarium</italic> wilt. These community analyses provide insights into the potential of plant-associated fungi in sustainable agriculture.</p>
<p>In this Research Topic, the majority of the studies aimed to elucidate the influences of changing environmental conditions, particularly soil nutrients, on plant-fungal symbiosis. However, more efforts are needed to clarify the molecular mechanisms underlying how nutrient factors drive the maintenance and breakdown of plant-fungi symbionts. Additionally, limited studies have been conducted under field conditions, which could provide better guidance for agricultural production. We anticipate further novel discoveries in the future.</p></sec>
<sec sec-type="author-contributions" id="s4">
<title>Author contributions</title>
<p>KS wrote the manuscript. All authors reviewed and revised the manuscript.</p></sec>
</body>
<back>
<sec sec-type="funding-information" id="s5">
<title>Funding</title>
<p>KS was funded by the Jiangsu Funding Program for Excellent and Postdoctoral Talent (2022ZB357) and China Postdoctoral Science Foundation (2021M701748). FDZ was funded by the National Natural Science Foundation of China (42177381 and 42267002) and the expert workstation of Longhua Wu in Yunnan Province (202305AF150042). YS was funded by the Natural Science Foundation of Henan (222300420035) and Xinyang Academy of Ecological Research Open Foundation (2023DBS09). JYZ was funded by the Open Fund of Jiangsu Key Laboratory for the Research and Utilization of Plant Resources (JSPKLB201926). JZ was funded by the project of Sustainable Innovations for Regenerative Agriculture in the Mediterranean area-SIRAM (ANR-22-PRIM-0001).</p>
</sec>
<ack><p>The guest editors thank Dr. Madeleine Berger and Dr. Fabian Vaistij (University of York, UK) for proofreading the manuscript. The guest editors are heart fully thanks the reviewers in their aid helping this Research Topic.</p>
</ack>
<sec sec-type="COI-statement" id="conf1">
<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 sec-type="disclaimer" id="s6">
<title>Publisher&#x00027;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>
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