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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.2024.1481110</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Editorial</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Editorial: Study on plant differentiation between beneficial and pathogenic microorganisms</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Carrillo-Tripp</surname>
<given-names>Jimena</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2114864"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>de los Santos-Villalobos</surname>
<given-names>Sergio</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1042347"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Sep&#xfa;lveda</surname>
<given-names>Edgardo</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/175012"/>
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<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
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<contrib contrib-type="author" corresp="yes">
<name>
<surname>Mart&#xed;nez-Soto</surname>
<given-names>Domingo</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
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<aff id="aff1">
<sup>1</sup>
<institution>Departamento de Microbiolog&#xed;a, Centro de Investigaci&#xf3;n Cient&#xed;fica y de Educaci&#xf3;n Superior de Ensenada (CICESE)</institution>, <addr-line>Ensenada, BC</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Departamento de Ciencias Agron&#xf3; micas y Veterinarias, Instituto Tecnol&#xf3;gico de Sonora (ITSON)</institution>, <addr-line>Obreg&#xf3;n</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Consejo Nacional de Humanidades, Ciencias y Tecnolog&#xed;as (CONAHCYT) - Departamento de Microbiolog&#xed;a, Centro de Investigaci&#xf3;n Cient&#xed;fica y de Educaci&#xf3;n Superior de Ensenada (CICESE)</institution>, <addr-line>Ensenada, BC</addr-line>, <country>Mexico</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited and Reviewed by: Brigitte Mauch-Mani, Universit&#xe9; de Neuch&#xe2;tel, Switzerland</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Domingo Mart&#xed;nez-Soto, <email xlink:href="mailto:dmartinez@cicese.edu.mx">dmartinez@cicese.edu.mx</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>10</day>
<month>09</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1481110</elocation-id>
<history>
<date date-type="received">
<day>15</day>
<month>08</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>19</day>
<month>08</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Carrillo-Tripp, de los Santos-Villalobos, Sep&#xfa;lveda and Mart&#xed;nez-Soto</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Carrillo-Tripp, de los Santos-Villalobos, Sep&#xfa;lveda and Mart&#xed;nez-Soto</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/52898/study-on-plant-differentiation-between-beneficial-and-pathogenic-microorganisms/overview" ext-link-type="uri">Editorial on the Research Topic <article-title>Study on plant differentiation between beneficial and pathogenic microorganisms</article-title>
</related-article>
<kwd-group>
<kwd>phytopathogenic microorganisms</kwd>
<kwd>beneficial microorganisms</kwd>
<kwd>friends and foes</kwd>
<kwd>microbial communities</kwd>
<kwd>fungi</kwd>
<kwd>bacteria</kwd>
<kwd>virus</kwd>
</kwd-group>
<counts>
<fig-count count="1"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="2"/>
<page-count count="3"/>
<word-count count="1206"/>
</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>
<p>How do plants differentiate friend from foe?. Answering this question is critical to understanding how plants recognize and allow their colonization by beneficial microorganisms, which improve their fitness, adaptation, and survival in hostile environments while deploying a multilayer immune system that thwarts pathogen colonization and avoids diseases (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). The multidisciplinary works published in this Research Topic contribute to answering this burning question in the plant interaction with fungi, bacteria, viruses, and microbial communities.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Friends or foes? Graphical representation of beneficial (friends) and detrimental (foes) interactions of plants with microorganisms. The beneficial interactions established by plants with endophytic bacteria, endophytic fungi, mycorrhizae, or microbial communities, improve the plant-priming effect and fitness. Beneficial microorganisms can colonize aboveground tissues, such as stems or leaves, although most beneficial interactions are established belowground with the roots or rhizomes. Detrimental interactions are established between plants and pathogenic bacteria, pathogenic fungi, or viruses. The evident result of these detrimental interactions are disease symptoms shown by the plants as consequences of the attack of the phytopathogen and the plant defense mechanisms. Volatile organic compounds (VOCs) play a key role in the plant-microbe interactions. One of the main questions without a clear response in the plant-microbe interaction is: How do the plants establish interactions with beneficial microorganisms but defy the colonization of pathogens? (reviewed by <xref ref-type="bibr" rid="B1">Harris et&#xa0;al., 2020</xref>).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1481110-g001.tif"/>
</fig>
<sec id="s1">
<label>1</label>
<title>Fungi-plant interaction</title>
<p>In this Research Topic, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2023.1253741">L&#xf3;pez-Coria et&#xa0;al.</ext-link> reported the plant growth promotion and biocontrol activity of <italic>Trichoderma asperellum</italic> against <italic>Fusarium verticillioides</italic>, and the role of this microbial interaction on the expression of the maize diffusional sugar transporters. Thus, in dual confrontation assays, <italic>T. asperellum</italic> showed antagonist activity against the studied phytopathogen, and in the primed plants the infection disease was delayed, and the upregulation of defense-related genes was observed. Additionally, the <italic>T. asperellum</italic> primed plants had longer stems than the non-primed plants. Finally, six maize diffusional sugar transporters increased their expression in the leaves and two at the roots of plants inoculated with <italic>T. asperellum</italic>. On the contrary, <italic>F. verticillioides</italic> downregulated the expression of these transporters on the leaves.</p>
<p>Also related to the fungal-plant interaction, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2023.1257098">Razo-Belm&#xe1;n et&#xa0;al.</ext-link> presented a review of the fungal volatile organic compounds (FVOCs) as airborne signals perceived by plants, affecting their development, physiology, and priming effect. FOVCs influence the response of plants to microbes. However, despite different plant colonization by beneficial or pathogenic fungi (<xref ref-type="bibr" rid="B2">Mart&#xed;nez-Soto et&#xa0;al., 2023</xref>), it is unclear whether plants distinguish VOCs from friends or foes fungi. The authors also discussed five main aspects of FVOCs: <italic>i</italic>) the synthesis of FVOCs, <italic>ii</italic>) sensing of FVOCs by plants, <italic>iii</italic>) plant response to FVOCs from beneficial or pathogenic fungi, <italic>iv</italic>) functions of FVOCs on plants, and <italic>v</italic>) application of FVOCs in agriculture. Being this last point the most important aspect of FVOCs study nowadays.</p>
</sec>
<sec id="s2">
<label>2</label>
<title>Bacteria-plant interaction</title>
<p>Due to their unique microbiome, suppressive soils (SS) prevent plant diseases from developing, even in the presence of pathogens like <italic>Ralstonia solanacearum</italic> and favorable conditions. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2024.1360173">Meng et&#xa0;al.</ext-link> compared bacterial communities in suppressive and conducive soils for Tobacco bacterial wilt (TBW) and found that SS had higher concentrations of <italic>Bacillus</italic>. They identified <italic>Bacillus velezensis</italic> B4-7, which showed significant suppression of <italic>Ralstonia solanacearum</italic> under acidic conditions. Greenhouse and field trials demonstrated that B4-7 reduced TBW severity, improved tobacco growth, and enhanced plant disease resistance while increasing the beneficial bacterial population in the soil. This work demonstrates how a single bacterial species can contribute to disease suppression through a diverse array of microbial mechanisms, both at the soil and at the plant level.</p>
<p>Similarly, in order to identify beneficial bacteria associated with seeds, by using NGS tools, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2023.1247814">De-la-Vega-Camarillo et&#xa0;al.</ext-link> present a research work where they identified the bacterial diversity associated with seeds from three Mexican teosinte species: <italic>Zea mays</italic>, <italic>Zea diploperennis</italic>, and <italic>Zea perennis</italic>. The authors identified a core of 38 bacteria related to the teosinte seeds, including <italic>Burkholderia</italic>, <italic>Agrobacterium</italic>, <italic>Erwinia</italic>, <italic>Pseudomonas</italic>, <italic>inter alia</italic>. The bioinformatic analysis of the metabolic pathways in the identified bacteria led the authors to suggest that those bacteria can be involved in plant growth, environmental adaptation, and biological control. Finally, the authors highlight the importance of those growth-promoting bacteria (PGPB) reservoirs from seeds and their putative applications in sustainable agriculture.</p>
</sec>
<sec id="s3">
<label>3</label>
<title>Viruses-plant interaction</title>
<p>In this Research Topic, the mechanisms of how viruses alter metabolic pathways and genetic regulation of their host, changing the cellular environment and resulting in higher viral replication, are explored. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2023.1108552">Gui et&#xa0;al.</ext-link> compare individual versus mixed infections of two tospoviruses (TSWV and HCRV). Interestingly, gene expression patterns differ in individual infections compared to coinfection. Single infections induce defense and resistance-related proteins. Meanwhile, coinfection does not, a cooperative interaction beneficial to both viruses. Besides showing the predicted function of differential genes and their expected effect on metabolism, the authors studied the expression of several miRNAs. Some are overexpressed during mixed infection and can indirectly turn down the synthesis of defense proteins such as NbPR1, increasing viral susceptibility. The fine-tuned molecular communication between the plant and the virus(es) during the early stage of infection differentiates low- and high-impact viruses.</p>
<p>The effect of viral infection on host metabolism is also thoroughly covered by <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.1099362">Jiang et&#xa0;al.</ext-link>, who studied how the potyvirus SCMV induced lactate accumulation and anaerobic glycolysis in the plant cells to its advantage, resulting in higher viral titers and more severe symptoms. Overexpressing the enzyme synthesizing lactate, LDH, results in higher viral loads; silencing it reduces virus accumulation. The authors further show how LDH interacts with viral protein 6K2 and how it relocates it to viral replication complexes. Additionally, they unveil how lactate could abolish plant defenses, which correlates with higher viral titer. This work exemplifies how viruses hijack the energy metabolism paths for their own, even when plants could recognize them initially as enemies, as inferred by the production of pathogenesis-related proteins.</p>
</sec>
<sec id="s4">
<label>4</label>
<title>Microbial-plant interactions</title>
<p>Regarding beneficial microorganisms&#x2019; consortia improving the plant fitness, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2024.1374228">Mehdi et&#xa0;al.</ext-link> reported the role of several environmental factors on sucrose accumulation and sugarcane yield, and the negative impact of insufficient water supply, temperature fluctuations, insect pests, and plant diseases. These authors propose reactive oxygen species as a main mechanism to alleviate environmental stresses in sugarcane, as well as the use of endophytic microorganisms as producers of bioactive molecules to enhance plant immune systems and regulate the environmental responses of plants.</p>
<p>On the other hand, it is well-known that Orchidaceae often rely on symbiotic relationships with microorganisms for essential nutrients and overall health. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2024.1334958">Wang et&#xa0;al.</ext-link> employed high-throughput sequencing to explore the degradation of <italic>Gastrodia elata</italic> (GeB) seedlings across multiple generations of asexual propagation. They observed that the bacterial and fungal composition of GeB seedlings and the surrounding soil changed significantly through each propagation, with a decline in beneficial microbes like <italic>Pseudomonas</italic> and an increase in pathogenic <italic>Penicillium</italic> correlating with disease outbreaks. <italic>Penicillium</italic> antagonistic strains, including <italic>Trichoderma</italic> and <italic>Paenibacillus</italic>, were also isolated from the surrounding soil of propagated GeB, suggesting potential strategies to mitigate degradation.</p>
<p>Altogether, these works shed new light on the mechanisms involved in the plant-microbe interactions and their implications for recognizing friends and resisting foes.</p>
</sec>
</body>
<back>
<sec id="s5" sec-type="author-contributions">
<title>Author contributions</title>
<p>JC-T: Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. SS-V: Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. ES: Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. DM-S: Writing &#x2013; original draft, Writing &#x2013; review &amp; editing, Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Project administration, Resources, Software, Supervision, Validation, Visualization.</p>
</sec>
<sec id="s6" 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="s7" 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>
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</article>