YODA MAP3K kinase regulates plant immune responses conferring broad-spectrum disease resistance
Mitogen-activated protein kinases (MAPKs) cascades play essential roles in plants by trans-ducing developmental cues and environmental signals into cellular responses. Among the latter are microbe-associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity...
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Veröffentlicht in: | The New phytologist 2018-04, Vol.218 (2), p.661-680 |
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creator | Sopeña-Torres, Sara Jordá, Lucía Sánchez-Rodríguez, Clara Miedes, Eva Escudero, Viviana Swami, Sanjay López, Gemma Piślewska-Bednarek, Mariola Lassowskat, Ines Lee, Justin Gu, Yangnan Haigis, Sabine Alexander, Danny Pattathil, Sivakumar Muñoz-Barrios, Antonio Bednarek, Pawel Somerville, Shauna Schulze-Lefert, Paul Hahn, Michael G Scheel, Dierk Molina, Antonio |
description | Mitogen-activated protein kinases (MAPKs) cascades play essential roles in plants by trans-ducing developmental cues and environmental signals into cellular responses. Among the latter are microbe-associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity.
We found that YODA (YDA) – a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning – also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA-YDA) protein show broad-spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor-Like Kinase, regulating both immunity and stomatal patterning.
ER-YDA-mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA-YDA plants exhibit altered cell-wall integrity and constitutively express defense-associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA-YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates.
Our results suggest that, in addition to stomata development, the ER-YDA pathway regulates an immune surveillance system conferring broad-spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones. |
doi_str_mv | 10.1111/nph.15007 |
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We found that YODA (YDA) – a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning – also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA-YDA) protein show broad-spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor-Like Kinase, regulating both immunity and stomatal patterning.
ER-YDA-mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA-YDA plants exhibit altered cell-wall integrity and constitutively express defense-associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA-YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates.
Our results suggest that, in addition to stomata development, the ER-YDA pathway regulates an immune surveillance system conferring broad-spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15007</identifier><identifier>PMID: 29451312</identifier><language>eng</language><publisher>England: New Phytologist Trust</publisher><subject>alleles ; Arabidopsis ; bacteria ; cell wall ; disease resistance ; ERECTA ; fungi ; hormones ; immune response ; mitogen-activated protein kinase ; mitogen-activated protein kinase kinase ; mitogen-activated protein kinase kinase kinase ; mitogen‐activated protein kinases (MAPKs) ; monitoring ; Oomycetes ; pathogens ; pattern recognition receptor (PRR) ; peptides ; phenotype ; plant hormones ; plant immunity ; proteome ; receptors ; receptor‐like kinase (RLK) ; stomata</subject><ispartof>The New phytologist, 2018-04, Vol.218 (2), p.661-680</ispartof><rights>Copyright © 2018 New Phytologist Trust</rights><rights>2018 Universidad Politécnica de Madrid (UPM) New Phytologist © 2018 New Phytologist Trust</rights><rights>2018 Universidad Politécnica de Madrid (UPM) New Phytologist © 2018 New Phytologist Trust.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4817-5aefc68cc241f5e816f6ab3b52ef59605cd1c6e79832f373f2833e9af887031e3</citedby><cites>FETCH-LOGICAL-c4817-5aefc68cc241f5e816f6ab3b52ef59605cd1c6e79832f373f2833e9af887031e3</cites><orcidid>0000-0003-3137-7938 ; 0000-0002-3064-7775 ; 0000-0001-8269-7494</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90019940$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90019940$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,1411,1427,27901,27902,45550,45551,46384,46808,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29451312$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sopeña-Torres, Sara</creatorcontrib><creatorcontrib>Jordá, Lucía</creatorcontrib><creatorcontrib>Sánchez-Rodríguez, Clara</creatorcontrib><creatorcontrib>Miedes, Eva</creatorcontrib><creatorcontrib>Escudero, Viviana</creatorcontrib><creatorcontrib>Swami, Sanjay</creatorcontrib><creatorcontrib>López, Gemma</creatorcontrib><creatorcontrib>Piślewska-Bednarek, Mariola</creatorcontrib><creatorcontrib>Lassowskat, Ines</creatorcontrib><creatorcontrib>Lee, Justin</creatorcontrib><creatorcontrib>Gu, Yangnan</creatorcontrib><creatorcontrib>Haigis, Sabine</creatorcontrib><creatorcontrib>Alexander, Danny</creatorcontrib><creatorcontrib>Pattathil, Sivakumar</creatorcontrib><creatorcontrib>Muñoz-Barrios, Antonio</creatorcontrib><creatorcontrib>Bednarek, Pawel</creatorcontrib><creatorcontrib>Somerville, Shauna</creatorcontrib><creatorcontrib>Schulze-Lefert, Paul</creatorcontrib><creatorcontrib>Hahn, Michael G</creatorcontrib><creatorcontrib>Scheel, Dierk</creatorcontrib><creatorcontrib>Molina, Antonio</creatorcontrib><title>YODA MAP3K kinase regulates plant immune responses conferring broad-spectrum disease resistance</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Mitogen-activated protein kinases (MAPKs) cascades play essential roles in plants by trans-ducing developmental cues and environmental signals into cellular responses. Among the latter are microbe-associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity.
We found that YODA (YDA) – a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning – also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA-YDA) protein show broad-spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor-Like Kinase, regulating both immunity and stomatal patterning.
ER-YDA-mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA-YDA plants exhibit altered cell-wall integrity and constitutively express defense-associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA-YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates.
Our results suggest that, in addition to stomata development, the ER-YDA pathway regulates an immune surveillance system conferring broad-spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones.</description><subject>alleles</subject><subject>Arabidopsis</subject><subject>bacteria</subject><subject>cell wall</subject><subject>disease resistance</subject><subject>ERECTA</subject><subject>fungi</subject><subject>hormones</subject><subject>immune response</subject><subject>mitogen-activated protein kinase</subject><subject>mitogen-activated protein kinase kinase</subject><subject>mitogen-activated protein kinase kinase kinase</subject><subject>mitogen‐activated protein kinases (MAPKs)</subject><subject>monitoring</subject><subject>Oomycetes</subject><subject>pathogens</subject><subject>pattern recognition receptor (PRR)</subject><subject>peptides</subject><subject>phenotype</subject><subject>plant hormones</subject><subject>plant immunity</subject><subject>proteome</subject><subject>receptors</subject><subject>receptor‐like kinase (RLK)</subject><subject>stomata</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNqNkEtP3TAQRq0KVC7QRX9AqyxhERjbsWMvr3iUClpYUKldWb6-YxrIC08ixL9vaIAdErMZaXTmjOZj7DOHAz7VYdv_PeAKoPzAFrzQNjdclhtsASBMrgv9e4ttE90CgFVafGRbwhaKSy4WzP25PF5mP5ZX8jy7q1pPmCW8GWs_IGV97dshq5pmbJ_G1HctTePQtRFTqtqbbJU6v86pxzCkscnWFeGsoIoG3wbcZZvR14SfnvsO-3V6cn10ll9cfvt-tLzIQ2F4mSuPMWgTgih4VGi4jtqv5EoJjMpqUGHNg8bSGimiLGUURkq0PhpTguQod9je7O1Tdz8iDa6pKGA9fYDdSE6ALoUtlS7egYKEAqajE7o_oyF1RAmj61PV-PToOLin6N0Uvfsf_cR-fdaOqwbXr-RL1hNwOAMPVY2Pb5vcz6uzF-WXeeOWhi69blgAbm0B8h93hJbl</recordid><startdate>201804</startdate><enddate>201804</enddate><creator>Sopeña-Torres, Sara</creator><creator>Jordá, Lucía</creator><creator>Sánchez-Rodríguez, Clara</creator><creator>Miedes, Eva</creator><creator>Escudero, Viviana</creator><creator>Swami, Sanjay</creator><creator>López, Gemma</creator><creator>Piślewska-Bednarek, Mariola</creator><creator>Lassowskat, Ines</creator><creator>Lee, Justin</creator><creator>Gu, Yangnan</creator><creator>Haigis, Sabine</creator><creator>Alexander, Danny</creator><creator>Pattathil, Sivakumar</creator><creator>Muñoz-Barrios, Antonio</creator><creator>Bednarek, Pawel</creator><creator>Somerville, Shauna</creator><creator>Schulze-Lefert, Paul</creator><creator>Hahn, Michael G</creator><creator>Scheel, Dierk</creator><creator>Molina, Antonio</creator><general>New Phytologist Trust</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-3137-7938</orcidid><orcidid>https://orcid.org/0000-0002-3064-7775</orcidid><orcidid>https://orcid.org/0000-0001-8269-7494</orcidid></search><sort><creationdate>201804</creationdate><title>YODA MAP3K kinase regulates plant immune responses conferring broad-spectrum disease resistance</title><author>Sopeña-Torres, Sara ; Jordá, Lucía ; Sánchez-Rodríguez, Clara ; Miedes, Eva ; Escudero, Viviana ; Swami, Sanjay ; López, Gemma ; Piślewska-Bednarek, Mariola ; Lassowskat, Ines ; Lee, Justin ; Gu, Yangnan ; Haigis, Sabine ; Alexander, Danny ; Pattathil, Sivakumar ; Muñoz-Barrios, Antonio ; Bednarek, Pawel ; Somerville, Shauna ; Schulze-Lefert, Paul ; Hahn, Michael G ; Scheel, Dierk ; Molina, Antonio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4817-5aefc68cc241f5e816f6ab3b52ef59605cd1c6e79832f373f2833e9af887031e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>alleles</topic><topic>Arabidopsis</topic><topic>bacteria</topic><topic>cell wall</topic><topic>disease resistance</topic><topic>ERECTA</topic><topic>fungi</topic><topic>hormones</topic><topic>immune response</topic><topic>mitogen-activated protein kinase</topic><topic>mitogen-activated protein kinase kinase</topic><topic>mitogen-activated protein kinase kinase kinase</topic><topic>mitogen‐activated protein kinases (MAPKs)</topic><topic>monitoring</topic><topic>Oomycetes</topic><topic>pathogens</topic><topic>pattern recognition receptor (PRR)</topic><topic>peptides</topic><topic>phenotype</topic><topic>plant hormones</topic><topic>plant immunity</topic><topic>proteome</topic><topic>receptors</topic><topic>receptor‐like kinase (RLK)</topic><topic>stomata</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sopeña-Torres, Sara</creatorcontrib><creatorcontrib>Jordá, Lucía</creatorcontrib><creatorcontrib>Sánchez-Rodríguez, Clara</creatorcontrib><creatorcontrib>Miedes, Eva</creatorcontrib><creatorcontrib>Escudero, Viviana</creatorcontrib><creatorcontrib>Swami, Sanjay</creatorcontrib><creatorcontrib>López, Gemma</creatorcontrib><creatorcontrib>Piślewska-Bednarek, Mariola</creatorcontrib><creatorcontrib>Lassowskat, Ines</creatorcontrib><creatorcontrib>Lee, Justin</creatorcontrib><creatorcontrib>Gu, Yangnan</creatorcontrib><creatorcontrib>Haigis, Sabine</creatorcontrib><creatorcontrib>Alexander, Danny</creatorcontrib><creatorcontrib>Pattathil, Sivakumar</creatorcontrib><creatorcontrib>Muñoz-Barrios, Antonio</creatorcontrib><creatorcontrib>Bednarek, Pawel</creatorcontrib><creatorcontrib>Somerville, Shauna</creatorcontrib><creatorcontrib>Schulze-Lefert, Paul</creatorcontrib><creatorcontrib>Hahn, Michael G</creatorcontrib><creatorcontrib>Scheel, Dierk</creatorcontrib><creatorcontrib>Molina, Antonio</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sopeña-Torres, Sara</au><au>Jordá, Lucía</au><au>Sánchez-Rodríguez, Clara</au><au>Miedes, Eva</au><au>Escudero, Viviana</au><au>Swami, Sanjay</au><au>López, Gemma</au><au>Piślewska-Bednarek, Mariola</au><au>Lassowskat, Ines</au><au>Lee, Justin</au><au>Gu, Yangnan</au><au>Haigis, Sabine</au><au>Alexander, Danny</au><au>Pattathil, Sivakumar</au><au>Muñoz-Barrios, Antonio</au><au>Bednarek, Pawel</au><au>Somerville, Shauna</au><au>Schulze-Lefert, Paul</au><au>Hahn, Michael G</au><au>Scheel, Dierk</au><au>Molina, Antonio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>YODA MAP3K kinase regulates plant immune responses conferring broad-spectrum disease resistance</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2018-04</date><risdate>2018</risdate><volume>218</volume><issue>2</issue><spage>661</spage><epage>680</epage><pages>661-680</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Mitogen-activated protein kinases (MAPKs) cascades play essential roles in plants by trans-ducing developmental cues and environmental signals into cellular responses. Among the latter are microbe-associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity.
We found that YODA (YDA) – a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning – also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA-YDA) protein show broad-spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor-Like Kinase, regulating both immunity and stomatal patterning.
ER-YDA-mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA-YDA plants exhibit altered cell-wall integrity and constitutively express defense-associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA-YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates.
Our results suggest that, in addition to stomata development, the ER-YDA pathway regulates an immune surveillance system conferring broad-spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones.</abstract><cop>England</cop><pub>New Phytologist Trust</pub><pmid>29451312</pmid><doi>10.1111/nph.15007</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0003-3137-7938</orcidid><orcidid>https://orcid.org/0000-0002-3064-7775</orcidid><orcidid>https://orcid.org/0000-0001-8269-7494</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | alleles Arabidopsis bacteria cell wall disease resistance ERECTA fungi hormones immune response mitogen-activated protein kinase mitogen-activated protein kinase kinase mitogen-activated protein kinase kinase kinase mitogen‐activated protein kinases (MAPKs) monitoring Oomycetes pathogens pattern recognition receptor (PRR) peptides phenotype plant hormones plant immunity proteome receptors receptor‐like kinase (RLK) stomata |
title | YODA MAP3K kinase regulates plant immune responses conferring broad-spectrum disease resistance |
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