The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis

The proteome and phosphoproteome of CEP5 overexpressing Arabidopsis seedlings have been determined. This revealed that CEP5 impacts abiotic stress-related processes. Subsequent genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for...

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Veröffentlicht in:Molecular & cellular proteomics 2020-08, Vol.19 (8), p.1248-1262
Hauptverfasser: Smith, Stephanie, Zhu, Shanshuo, Joos, Lisa, Roberts, Ianto, Nikonorova, Natalia, Vu, Lam Dai, Stes, Elisabeth, Cho, Hyunwoo, Larrieu, Antoine, Xuan, Wei, Goodall, Benjamin, van de Cotte, Brigitte, Waite, Jessic Marie, Rigal, Adeline, Ramans Harborough, Sigurd, Persiau, Geert, Vanneste, Steffen, Kirschner, Gwendolyn K., Vandermarliere, Elien, Martens, Lennart, Stahl, Yvonne, Audenaert, Dominique, Friml, Jirí, Felix, Georg, Simon, Rüdiger, Bennett, Malcolm J., Bishopp, Anthony, De Jaeger, Geert, Ljung, Karin, Kepinski, Stefan, Robert, Stephanie, Nemhauser, Jennifer, Hwang, Ildoo, Gevaert, Kris, Beeckman, Tom, De Smet, Ive
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container_issue 8
container_start_page 1248
container_title Molecular & cellular proteomics
container_volume 19
creator Smith, Stephanie
Zhu, Shanshuo
Joos, Lisa
Roberts, Ianto
Nikonorova, Natalia
Vu, Lam Dai
Stes, Elisabeth
Cho, Hyunwoo
Larrieu, Antoine
Xuan, Wei
Goodall, Benjamin
van de Cotte, Brigitte
Waite, Jessic Marie
Rigal, Adeline
Ramans Harborough, Sigurd
Persiau, Geert
Vanneste, Steffen
Kirschner, Gwendolyn K.
Vandermarliere, Elien
Martens, Lennart
Stahl, Yvonne
Audenaert, Dominique
Friml, Jirí
Felix, Georg
Simon, Rüdiger
Bennett, Malcolm J.
Bishopp, Anthony
De Jaeger, Geert
Ljung, Karin
Kepinski, Stefan
Robert, Stephanie
Nemhauser, Jennifer
Hwang, Ildoo
Gevaert, Kris
Beeckman, Tom
De Smet, Ive
description The proteome and phosphoproteome of CEP5 overexpressing Arabidopsis seedlings have been determined. This revealed that CEP5 impacts abiotic stress-related processes. Subsequent genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis. Furthermore, CEP5 specifically counteracts auxin effects by stabilizing AUX/IAA transcriptional repressors. [Display omitted] Highlights •Quantitative Arabidopsis (phospho)proteomes of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5).•CEP5 impacts abiotic stress-related processes and counteracts auxin effects.•CEP5 signaling stabilizes AUX/IAA transcriptional repressors.•Novel peptide-dependent control mechanism that tunes auxin signaling. Peptides derived from non-functional precursors play important roles in various developmental processes, but also in (a)biotic stress signaling. Our (phospho)proteome-wide analyses of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5)-mediated changes revealed an impact on abiotic stress-related processes. Drought has a dramatic impact on plant growth, development and reproduction, and the plant hormone auxin plays a role in drought responses. Our genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis, and that CEP5 specifically counteracts auxin effects. Specifically, we found that CEP5 signaling stabilizes AUX/IAA transcriptional repressors, suggesting the existence of a novel peptide-dependent control mechanism that tunes auxin signaling. These observations align with the recently described role of AUX/IAAs in stress tolerance and provide a novel role for CEP5 in osmotic and drought stress tolerance.
doi_str_mv 10.1074/mcp.RA119.001826
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This revealed that CEP5 impacts abiotic stress-related processes. Subsequent genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis. Furthermore, CEP5 specifically counteracts auxin effects by stabilizing AUX/IAA transcriptional repressors. [Display omitted] Highlights •Quantitative Arabidopsis (phospho)proteomes of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5).•CEP5 impacts abiotic stress-related processes and counteracts auxin effects.•CEP5 signaling stabilizes AUX/IAA transcriptional repressors.•Novel peptide-dependent control mechanism that tunes auxin signaling. Peptides derived from non-functional precursors play important roles in various developmental processes, but also in (a)biotic stress signaling. Our (phospho)proteome-wide analyses of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5)-mediated changes revealed an impact on abiotic stress-related processes. Drought has a dramatic impact on plant growth, development and reproduction, and the plant hormone auxin plays a role in drought responses. Our genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis, and that CEP5 specifically counteracts auxin effects. Specifically, we found that CEP5 signaling stabilizes AUX/IAA transcriptional repressors, suggesting the existence of a novel peptide-dependent control mechanism that tunes auxin signaling. 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This revealed that CEP5 impacts abiotic stress-related processes. Subsequent genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis. Furthermore, CEP5 specifically counteracts auxin effects by stabilizing AUX/IAA transcriptional repressors. [Display omitted] Highlights •Quantitative Arabidopsis (phospho)proteomes of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5).•CEP5 impacts abiotic stress-related processes and counteracts auxin effects.•CEP5 signaling stabilizes AUX/IAA transcriptional repressors.•Novel peptide-dependent control mechanism that tunes auxin signaling. Peptides derived from non-functional precursors play important roles in various developmental processes, but also in (a)biotic stress signaling. Our (phospho)proteome-wide analyses of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5)-mediated changes revealed an impact on abiotic stress-related processes. Drought has a dramatic impact on plant growth, development and reproduction, and the plant hormone auxin plays a role in drought responses. Our genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis, and that CEP5 specifically counteracts auxin effects. Specifically, we found that CEP5 signaling stabilizes AUX/IAA transcriptional repressors, suggesting the existence of a novel peptide-dependent control mechanism that tunes auxin signaling. These observations align with the recently described role of AUX/IAAs in stress tolerance and provide a novel role for CEP5 in osmotic and drought stress tolerance.</description><subject>Adaptation, Physiological - genetics</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biochemistry and Molecular Biology</subject><subject>Biokemi och molekylärbiologi</subject><subject>Biological Transport - genetics</subject><subject>developmental biology</subject><subject>Droughts</subject><subject>Gene Expression Regulation, Plant</subject><subject>hormones</subject><subject>Indoleacetic Acids - metabolism</subject><subject>label-free quantification</subject><subject>mass spectrometry</subject><subject>Osmosis</subject><subject>Peptides - metabolism</subject><subject>Phosphoproteins - metabolism</subject><subject>phosphoproteome</subject><subject>Plant biology</subject><subject>Proteasome Endopeptidase Complex - metabolism</subject><subject>protein degradation</subject><subject>Proteome - metabolism</subject><subject>Proteomics</subject><subject>Seedlings - growth &amp; development</subject><subject>signal transduction</subject><subject>stress response</subject><subject>Stress, Physiological - genetics</subject><subject>Transcription, Genetic</subject><issn>1535-9476</issn><issn>1535-9484</issn><issn>1535-9484</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNp1kU9v1DAQxSMEoqVw54R85NDd2o6TOByQotXSVqrEUrYSN8t_JtQoiVPb2aofg2-MtykresCXseT33oznl2XvCV4SXLGzXo_L64aQeokx4bR8kR2TIi8WNePs5eFelUfZmxB-YUwxqYrX2VFOGWaM8-Ps9_YW0Gq9KdAGxmgNoI13vYsQUKOsi1aj79FDCGjrOvBy0HCKmoCuYQeyA4PUA_o2ySHaKKPdPdojuN7qcIrkYFATIwyT3AfG1Kq5-XF22TRofTfZzipvpx7ZATVeKmvcGGx4m71qZRfg3VM9yW6-rLeri8XV1_PLVXO10EVB46JNh5paUUYlK6kuCdd1RRgwrYGXlLWlIZi3WhlOSVoCA5wXrVQlb5Ws2_wkW8654R7GSYnR2176B-GkFaGblPT7IgIIgssC58nweTYkdQ9GwxC97J75nr8M9lb8dDvBMSFFhVPAx6cA7-4mCFH0NmjoOjmAm4JIUHJMeV7vpXiWau9C8NAe2hAs9uhFQi8e0YsZfbJ8-He8g-Ev6yT4NAsgbXVnIf1PW0hAjfWgozDO_j_9D30hwUA</recordid><startdate>20200801</startdate><enddate>20200801</enddate><creator>Smith, Stephanie</creator><creator>Zhu, Shanshuo</creator><creator>Joos, Lisa</creator><creator>Roberts, Ianto</creator><creator>Nikonorova, Natalia</creator><creator>Vu, Lam Dai</creator><creator>Stes, Elisabeth</creator><creator>Cho, Hyunwoo</creator><creator>Larrieu, Antoine</creator><creator>Xuan, Wei</creator><creator>Goodall, Benjamin</creator><creator>van de Cotte, Brigitte</creator><creator>Waite, Jessic Marie</creator><creator>Rigal, Adeline</creator><creator>Ramans Harborough, Sigurd</creator><creator>Persiau, Geert</creator><creator>Vanneste, Steffen</creator><creator>Kirschner, Gwendolyn K.</creator><creator>Vandermarliere, Elien</creator><creator>Martens, Lennart</creator><creator>Stahl, Yvonne</creator><creator>Audenaert, Dominique</creator><creator>Friml, Jirí</creator><creator>Felix, Georg</creator><creator>Simon, Rüdiger</creator><creator>Bennett, Malcolm J.</creator><creator>Bishopp, Anthony</creator><creator>De Jaeger, Geert</creator><creator>Ljung, Karin</creator><creator>Kepinski, Stefan</creator><creator>Robert, Stephanie</creator><creator>Nemhauser, Jennifer</creator><creator>Hwang, Ildoo</creator><creator>Gevaert, Kris</creator><creator>Beeckman, Tom</creator><creator>De Smet, Ive</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-0013-3239</orcidid><orcidid>https://orcid.org/0000-0001-5078-7532</orcidid><orcidid>https://orcid.org/0000-0002-1317-7716</orcidid><orcidid>https://orcid.org/0000-0003-4607-8893</orcidid><orcidid>https://orcid.org/0000-0003-2901-189X</orcidid><orcidid>https://orcid.org/0000-0002-9351-1170</orcidid><orcidid>https://orcid.org/0000-0002-4237-0283</orcidid></search><sort><creationdate>20200801</creationdate><title>The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis</title><author>Smith, Stephanie ; Zhu, Shanshuo ; Joos, Lisa ; Roberts, Ianto ; Nikonorova, Natalia ; Vu, Lam Dai ; Stes, Elisabeth ; Cho, Hyunwoo ; Larrieu, Antoine ; Xuan, Wei ; Goodall, Benjamin ; van de Cotte, Brigitte ; Waite, Jessic Marie ; Rigal, Adeline ; Ramans Harborough, Sigurd ; Persiau, Geert ; Vanneste, Steffen ; Kirschner, Gwendolyn K. ; Vandermarliere, Elien ; Martens, Lennart ; Stahl, Yvonne ; Audenaert, Dominique ; Friml, Jirí ; Felix, Georg ; Simon, Rüdiger ; Bennett, Malcolm J. ; Bishopp, Anthony ; De Jaeger, Geert ; Ljung, Karin ; Kepinski, Stefan ; Robert, Stephanie ; Nemhauser, Jennifer ; Hwang, Ildoo ; Gevaert, Kris ; Beeckman, Tom ; De Smet, Ive</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c552t-ffff2d9b242a462c618c9714e4cce8624f6d108fcbd8219474e035fab68fba9f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adaptation, Physiological - genetics</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biochemistry and Molecular Biology</topic><topic>Biokemi och molekylärbiologi</topic><topic>Biological Transport - genetics</topic><topic>developmental biology</topic><topic>Droughts</topic><topic>Gene Expression Regulation, Plant</topic><topic>hormones</topic><topic>Indoleacetic Acids - metabolism</topic><topic>label-free quantification</topic><topic>mass spectrometry</topic><topic>Osmosis</topic><topic>Peptides - metabolism</topic><topic>Phosphoproteins - metabolism</topic><topic>phosphoproteome</topic><topic>Plant biology</topic><topic>Proteasome Endopeptidase Complex - metabolism</topic><topic>protein degradation</topic><topic>Proteome - metabolism</topic><topic>Proteomics</topic><topic>Seedlings - growth &amp; development</topic><topic>signal transduction</topic><topic>stress response</topic><topic>Stress, Physiological - genetics</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Smith, Stephanie</creatorcontrib><creatorcontrib>Zhu, Shanshuo</creatorcontrib><creatorcontrib>Joos, Lisa</creatorcontrib><creatorcontrib>Roberts, Ianto</creatorcontrib><creatorcontrib>Nikonorova, Natalia</creatorcontrib><creatorcontrib>Vu, Lam Dai</creatorcontrib><creatorcontrib>Stes, Elisabeth</creatorcontrib><creatorcontrib>Cho, Hyunwoo</creatorcontrib><creatorcontrib>Larrieu, Antoine</creatorcontrib><creatorcontrib>Xuan, Wei</creatorcontrib><creatorcontrib>Goodall, Benjamin</creatorcontrib><creatorcontrib>van de Cotte, Brigitte</creatorcontrib><creatorcontrib>Waite, Jessic Marie</creatorcontrib><creatorcontrib>Rigal, Adeline</creatorcontrib><creatorcontrib>Ramans Harborough, Sigurd</creatorcontrib><creatorcontrib>Persiau, Geert</creatorcontrib><creatorcontrib>Vanneste, Steffen</creatorcontrib><creatorcontrib>Kirschner, Gwendolyn K.</creatorcontrib><creatorcontrib>Vandermarliere, Elien</creatorcontrib><creatorcontrib>Martens, Lennart</creatorcontrib><creatorcontrib>Stahl, Yvonne</creatorcontrib><creatorcontrib>Audenaert, Dominique</creatorcontrib><creatorcontrib>Friml, Jirí</creatorcontrib><creatorcontrib>Felix, Georg</creatorcontrib><creatorcontrib>Simon, Rüdiger</creatorcontrib><creatorcontrib>Bennett, Malcolm J.</creatorcontrib><creatorcontrib>Bishopp, Anthony</creatorcontrib><creatorcontrib>De Jaeger, Geert</creatorcontrib><creatorcontrib>Ljung, Karin</creatorcontrib><creatorcontrib>Kepinski, Stefan</creatorcontrib><creatorcontrib>Robert, Stephanie</creatorcontrib><creatorcontrib>Nemhauser, Jennifer</creatorcontrib><creatorcontrib>Hwang, Ildoo</creatorcontrib><creatorcontrib>Gevaert, Kris</creatorcontrib><creatorcontrib>Beeckman, Tom</creatorcontrib><creatorcontrib>De Smet, Ive</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>Molecular &amp; cellular proteomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Smith, Stephanie</au><au>Zhu, Shanshuo</au><au>Joos, Lisa</au><au>Roberts, Ianto</au><au>Nikonorova, Natalia</au><au>Vu, Lam Dai</au><au>Stes, Elisabeth</au><au>Cho, Hyunwoo</au><au>Larrieu, Antoine</au><au>Xuan, Wei</au><au>Goodall, Benjamin</au><au>van de Cotte, Brigitte</au><au>Waite, Jessic Marie</au><au>Rigal, Adeline</au><au>Ramans Harborough, Sigurd</au><au>Persiau, Geert</au><au>Vanneste, Steffen</au><au>Kirschner, Gwendolyn K.</au><au>Vandermarliere, Elien</au><au>Martens, Lennart</au><au>Stahl, Yvonne</au><au>Audenaert, Dominique</au><au>Friml, Jirí</au><au>Felix, Georg</au><au>Simon, Rüdiger</au><au>Bennett, Malcolm J.</au><au>Bishopp, Anthony</au><au>De Jaeger, Geert</au><au>Ljung, Karin</au><au>Kepinski, Stefan</au><au>Robert, Stephanie</au><au>Nemhauser, Jennifer</au><au>Hwang, Ildoo</au><au>Gevaert, Kris</au><au>Beeckman, Tom</au><au>De Smet, Ive</au><aucorp>Sveriges lantbruksuniversitet</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis</atitle><jtitle>Molecular &amp; cellular proteomics</jtitle><addtitle>Mol Cell Proteomics</addtitle><date>2020-08-01</date><risdate>2020</risdate><volume>19</volume><issue>8</issue><spage>1248</spage><epage>1262</epage><pages>1248-1262</pages><issn>1535-9476</issn><issn>1535-9484</issn><eissn>1535-9484</eissn><abstract>The proteome and phosphoproteome of CEP5 overexpressing Arabidopsis seedlings have been determined. This revealed that CEP5 impacts abiotic stress-related processes. Subsequent genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis. Furthermore, CEP5 specifically counteracts auxin effects by stabilizing AUX/IAA transcriptional repressors. [Display omitted] Highlights •Quantitative Arabidopsis (phospho)proteomes of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5).•CEP5 impacts abiotic stress-related processes and counteracts auxin effects.•CEP5 signaling stabilizes AUX/IAA transcriptional repressors.•Novel peptide-dependent control mechanism that tunes auxin signaling. Peptides derived from non-functional precursors play important roles in various developmental processes, but also in (a)biotic stress signaling. Our (phospho)proteome-wide analyses of C-TERMINALLY ENCODED PEPTIDE 5 (CEP5)-mediated changes revealed an impact on abiotic stress-related processes. Drought has a dramatic impact on plant growth, development and reproduction, and the plant hormone auxin plays a role in drought responses. Our genetic, physiological, biochemical, and pharmacological results demonstrated that CEP5-mediated signaling is relevant for osmotic and drought stress tolerance in Arabidopsis, and that CEP5 specifically counteracts auxin effects. Specifically, we found that CEP5 signaling stabilizes AUX/IAA transcriptional repressors, suggesting the existence of a novel peptide-dependent control mechanism that tunes auxin signaling. These observations align with the recently described role of AUX/IAAs in stress tolerance and provide a novel role for CEP5 in osmotic and drought stress tolerance.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32404488</pmid><doi>10.1074/mcp.RA119.001826</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-0013-3239</orcidid><orcidid>https://orcid.org/0000-0001-5078-7532</orcidid><orcidid>https://orcid.org/0000-0002-1317-7716</orcidid><orcidid>https://orcid.org/0000-0003-4607-8893</orcidid><orcidid>https://orcid.org/0000-0003-2901-189X</orcidid><orcidid>https://orcid.org/0000-0002-9351-1170</orcidid><orcidid>https://orcid.org/0000-0002-4237-0283</orcidid><oa>free_for_read</oa></addata></record>
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ispartof Molecular & cellular proteomics, 2020-08, Vol.19 (8), p.1248-1262
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1535-9484
1535-9484
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subjects Adaptation, Physiological - genetics
Arabidopsis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis - physiology
Arabidopsis Proteins - metabolism
Biochemistry and Molecular Biology
Biokemi och molekylärbiologi
Biological Transport - genetics
developmental biology
Droughts
Gene Expression Regulation, Plant
hormones
Indoleacetic Acids - metabolism
label-free quantification
mass spectrometry
Osmosis
Peptides - metabolism
Phosphoproteins - metabolism
phosphoproteome
Plant biology
Proteasome Endopeptidase Complex - metabolism
protein degradation
Proteome - metabolism
Proteomics
Seedlings - growth & development
signal transduction
stress response
Stress, Physiological - genetics
Transcription, Genetic
title The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis
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