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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title>Frontiers in Plant Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Plant Sci.</abbrev-journal-title>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fpls.2023.1230438</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: Plant cell wall in pathogenesis, parasitism and symbiosis, Volume II</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Vicr&#xe9;</surname>
<given-names>Ma&#xef;t&#xe9;</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/81553"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Lionetti</surname>
<given-names>Vincenzo</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/69116"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Univ Rouen Normandie, Laboratoire Glyco-MEV UR 4358</institution>, <addr-line>Rouen</addr-line>, <country>France</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Dipartimento di Biologia e Biotecnologie &#x201c;Charles Darwin&#x201d;, Sapienza Universit&#xe0; di Roma</institution>, <addr-line>Rome</addr-line>, <country>Italy</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Centro di Ricerca per le Scienze applicate alla Protezione dell&#x2019;Ambiente e dei Beni Culturali (CIABC), Sapienza Universit&#xe0; di Roma</institution>, <addr-line>Rome</addr-line>, <country>Italy</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited and Reviewed by: Prem Lal Kashyap, Indian Institute of Wheat and Barley Research (ICAR), India</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Vincenzo Lionetti, <email xlink:href="mailto:vincenzo.lionetti@uniroma1.it">vincenzo.lionetti@uniroma1.it</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>20</day>
<month>06</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>14</volume>
<elocation-id>1230438</elocation-id>
<history>
<date date-type="received">
<day>28</day>
<month>05</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>06</day>
<month>06</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2023 Vicr&#xe9; and Lionetti</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Vicr&#xe9; and Lionetti</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/27587/plant-cell-wall-in-pathogenesis-parasitism-and-symbiosis-volume-ii" ext-link-type="uri">Editorial on the Research Topic <article-title>Plant cell wall in pathogenesis, parasitism and symbiosis, Volume II</article-title>
</related-article>
<kwd-group>
<kwd>cell wall remodeling</kwd>
<kwd>symbiosis</kwd>
<kwd>cell wall integrity</kwd>
<kwd>plant immunity</kwd>
<kwd>plant parasitism</kwd>
<kwd>plant cell wall</kwd>
</kwd-group>
<counts>
<fig-count count="1"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="27"/>
<page-count count="3"/>
<word-count count="1100"/>
</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>A wide range of organisms that interact with plants must interface with the plant cell wall (CW) (<xref ref-type="bibr" rid="B16">Lionetti and Metraux, 2014</xref>). The view of the CW as only a static cellular barrier in these interactions is outdated. Cell wall polysaccharides, phenolic compounds, and proteins, in addition to regulating important growth and development processes, are also sources of elicitors that activate cell signaling pathways (<xref ref-type="bibr" rid="B21">Nguema-Ona et&#xa0;al., 2013</xref>). Surveillance mechanisms detect CW contacts with other organisms, and specific signaling pathways and responses are activated (<xref ref-type="bibr" rid="B25">Swaminathan et&#xa0;al., 2022</xref>) (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). During biotic interactions and abiotic stresses, the structure and composition of plant CW can be regulated at the biosynthetic level and through precise, continuous post-synthetic remodeling. As a consequence, the CW must be understood as a strategic space between organisms where intelligent and dynamic molecular strategies are implemented to overwhelm a fight or cooperate for specific physiological processes (<xref ref-type="bibr" rid="B2">Bacete et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B7">Castilleux et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B9">De Lorenzo et&#xa0;al., 2019</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Schematic representation of the main systems of perception and responses related to the plant cell wall (CW) in the different biotic interactions. CW can play a central role in combined biotic and abiotic stress. Symbiont-induced CW modifications can improve plant development, nutrition, and tolerance to abiotic stresses. Abiotic stresses can alter CW composition, affecting efficient parasitism. M/H/DAMPS=Microbe/Herbivore/Damage Associated Molecular Patterns.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-14-1230438-g001.tif"/>
</fig>
<p>Cell wall enzymes and their inhibitors play key roles in apoplastic metabolism (<xref ref-type="bibr" rid="B23">Rui and Dinneny, 2020</xref>). Invertases (INVs) and pectin methylesterases (PMEs) play essential roles in carbohydrate metabolism, stress responses, and sugar signaling (<xref ref-type="bibr" rid="B5">Bellincampi et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B26">Tauzin and Giardina, 2014</xref>; <xref ref-type="bibr" rid="B8">Del Corpo et&#xa0;al., 2020</xref>). In this collection, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.863892">Coculo and Lionetti</ext-link> reviewed the roles of invertase inhibitors (INVI) and pectin methylesterase inhibitors (PMEI) belonging to the &#x201c;Plant Invertase/Pectin Methylesterase Inhibitor Superfamily&#x201d; (<xref ref-type="bibr" rid="B15">Lionetti et&#xa0;al., 2017</xref>). An updated overview of the specific activity of the characterized isoforms, their specific functions in plant physiology, and their applications in biotechnology is provided. After the pioneering work in 2007 (<xref ref-type="bibr" rid="B17">Lionetti et&#xa0;al., 2007</xref>), several piece of evidence supported the role of PMEIs in plant resistance to stresses (<xref ref-type="bibr" rid="B1">An et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B19">Liu et&#xa0;al., 2018</xref>). With a genome-wide analysis and transcriptomics of the <italic>PMEI</italic> genes in <italic>Brassica napus</italic>, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.940284">Wang et&#xa0;al</ext-link>. identified several <italic>BnPMEIs</italic> as resistance gene candidates in response to <italic>Sclerotinia sclerotiorum</italic>, suggesting them as possible tools to breed new and improved genotypes more resistant to <italic>Sclerotinia</italic> stem rot.</p>
<p>Specific CW changes can occur in the vicinity of plasmodesmata during viral infection (<xref ref-type="bibr" rid="B18">Lionetti et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B24">Stavolone and Lionetti, 2017</xref>). Viruses can modify pectin, callose, and structural proteins near plasmodesmata by increasing their size exclusion limit (<xref ref-type="bibr" rid="B14">Kozie&#x142; et&#xa0;al., 2021</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/fpls.2021.741050">L&#xf3;pez-Gonz&#xe1;lez et&#xa0;al.</ext-link> addressed the little-explored impact of virus infections on secondary CW and plant development. The authors found a correlation between the developmental alterations induced in Arabidopsis by specific strains of turnip mosaic virus and specific changes in xylan and lignin biosynthesis. Although callose deposition is a response to both elicitors and pathogens, the mechanisms involved in its biosynthesis and degradation remain to be unraveled (<xref ref-type="bibr" rid="B11">German et&#xa0;al., 2023</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/fpls.2023.1183402">Li et&#xa0;al</ext-link>. summarized the research progress on plant callose and its synthesizing enzymes in plant physiology.</p>
<p>Microfungi are also important etiological agents for plants (<xref ref-type="bibr" rid="B10">Doehlemann et&#xa0;al., 2017</xref>). The fungal pathogen <italic>Sphaerulina musiva</italic> causes stem canker with the consequent mortality of Populus trees. <italic>Populus deltoides</italic> can induce a lignified periderm to contain the pathogen, but the precise characterization of lignin changes in response to <italic>S. musiva</italic> infection is unknown. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2023.1089011">Bryant et&#xa0;al.</ext-link>identified a higher syringyl:guaiacil ratio, a higher Klason lignin content and lower p-hydroxybenzoate content in Septoria-infected <italic>P. deltoides</italic> trees compared to the healthy plant. This knowledge can favor biotechnological approaches aimed at improving the resilience and increasing the biomass yield of Populus for biofuel production.</p>
<p>Interesting contributions in this collection concern plant-parasite interactions. A fine-tuned re-arrangement of host CW is induced in response to infection by both plant-parasitic cyst nematodes and root-knot nematodes (<xref ref-type="bibr" rid="B27">Zhang et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B6">Bozbuga et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B20">Meidani et&#xa0;al., 2019</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.817185">Veronico et&#xa0;al</ext-link>. found that drought stress affects CW metabolism in tomato roots, limiting feeding site development and reproduction of the nematode <italic>Meloidogyne incognita</italic>. Parasitic plants, such as Cuscuta species, severely damage economically important crops (<xref ref-type="bibr" rid="B12">Jhu and Sinha, 2022</xref>). These green parasites absorb resources through an invasive organ called the haustorium, which differentiates into vascular hyphae that establish a connection with the host plant&#x2019;s vasculature. The degradation and modification of host CWs allow haustorium to effectively invade host tissues. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.904313">Yokoyama et&#xa0;al.</ext-link> propose that <italic>Cuscuta campestris</italic> APETALA2/ETHYLENE RESPONSE FACTORS (ERFs) can activate the transcription of the CW enzymatic genes in haustorium to favor its invasion of tobacco and <italic>Arabidopsis</italic> plants.</p>
<p>Plant CW is a field of molecular dialogues and agreements with symbiotic microbes to establish intimate interfaces for developmental coordination and nutrient exchange (<xref ref-type="bibr" rid="B3">Balestrini and Bonfante, 2014</xref>). Plants can establish mutualistic symbiosis with arbuscular mycorrhizal fungi, and phosphorus transfer across the CW specialized interfacial compartment is an important process in the mycorrhizal pathway (<xref ref-type="bibr" rid="B4">Begum et&#xa0;al., 2019</xref>). Exploiting the <italic>Rhizophagus irregularis-Lotus japonicus</italic> interaction, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2021.725939">Nguyen and Saito</ext-link> showed that polyphosphate in fungal CWs and apoplastic phosphatases play an important role in phosphorus transfer at the symbiotic interface in arbuscules. Mycorrhizal fungi can be involved in mutualistic interactions during orchid seed germination (<xref ref-type="bibr" rid="B22">P&#xf5;lme et&#xa0;al., 2018</xref>). <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.880600">Chen et&#xa0;al</ext-link>. identified several genes codifying CW structural proteins such as epidermis-specific secreted glycoprotein, proline-rich receptor-like protein, and leucine-rich repeat (LRR) extensin-like protein, which are particularly involved in the symbiosis of Tulasnella and Serendipita fungi with <italic>Dendrobium officinale.</italic>
</p>
<p>Bioinoculants represent an environmentally-friendly agricultural practice to alleviate drought stress in crops (<xref ref-type="bibr" rid="B13">Kour et&#xa0;al., 2022</xref>). The work presented by <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fpls.2022.958004">Wilmowitz et&#xa0;al</ext-link>. indicates that the inoculation of maize seeds with <italic>Glomus</italic> sp. and <italic>Bacillus</italic> sp. can help to cope with drought stress, preventing inhibition of photosynthesis and disruption of redox balance. <italic>Glomus</italic> sp. and <italic>Bacillus</italic> sp. can modify pectin methylesterification and hemicellulose content of maize leaves, possibly leading to alleviation of the negative effects of drought.</p>
<p>These important contributions advance our understanding of the relationships between plants and the environment at the CW interface, which will be helpful to engineer biotechnological strategies for agriculture and bioenergy fields. As a closing remark, we are grateful to the authors and reviewers for their invaluable contributions to this Research Topic.</p>
<sec id="s1" sec-type="author-contributions">
<title>Author contributions</title>
<p>VL draft the editorial text. MV revised and approved the final version of the editorial. All authors approved the submitted version.</p>
</sec>
</body>
<back>
<sec id="s2" sec-type="funding-information">
<title>Funding</title>
<p>The research was supported by Sapienza University of Rome, Grants RM120172B78CFDF2, RM11916B7A142CF1, RG12117A898EABE0, RM122181424F1F42 and - Rome Technopole&#x201d; - European Union Next-GenerationEU PNRR -RT12218451D2C509 to VL.</p>
</sec>
<sec id="s3" 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="s4" 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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