Phytosulfokine downregulates defense‐related WRKY transcription factors and attenuates pathogen‐associated molecular pattern‐triggered immunity

Liu, Dian; Jelenska, Joanna; Morgan, Jessica M.; Greenberg, Jean T.

doi:10.1111/tpj.17115

Title: Phytosulfokine downregulates defense‐related WRKY transcription factors and attenuates pathogen‐associated molecular pattern‐triggered immunity

Journal Article · 10 December 2024 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.17115 · OSTI ID:2480979

^[1]; Jelenska, Joanna ^[2]; Morgan, Jessica M. ^[3]; Greenberg, Jean T. ^[2]

Biochemistry and Molecular Biophysics The University of Chicago Chicago Illinois 60637 USA
Department of Molecular Genetics and Cell Biology The University of Chicago Chicago Illinois 60637 USA
Biophysical Sciences The University of Chicago Chicago Illinois 60637 USA

SUMMARY Phytosulfokine (PSK) is a plant growth‐promoting peptide hormone that is perceived by its cell surface receptors PSKR1 and PSKR2 in Arabidopsis. Plants lacking the PSK receptors show phenotypes consistent with PSK signaling repressing some plant defenses. To gain further insight into the PSK signaling mechanism, comprehensive transcriptional profiling of Arabidopsis treated with PSK was performed, and the effects of PSK treatment on plant defense readouts were monitored. Our study indicates that PSK's major effect is to downregulate defense‐related genes; it has a more modest effect on the induction of growth‐related genes. WRKY transcription factors (TFs) emerged as key regulators of PSK‐responsive genes, sharing commonality with a pathogen‐associated molecular pattern (PAMP) responses, flagellin 22 (flg22), but exhibiting opposite regulatory directions. These PSK‐induced transcriptional changes were accompanied by biochemical and physiological changes that reduced PAMP responses, notably mitogen‐activated protein kinase (MPK) phosphorylation (previously implicated in WRKY activation) and the cell wall modification of callose deposition. Comparison with previous studies using other growth stimuli (the sulfated plant peptide containing sulfated tyrosine [PSY] and Pseudomonas simiae strain WCS417) also reveals WRKY TFs' overrepresentations in these pathways, suggesting a possible shared mechanism involving WRKY TFs for plant growth–defense trade‐off.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0019104

OSTI ID:: 2480979

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 6 Vol. 120; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (68)

Overexpression of phytosulfokine-α induces male sterility and cell growth by regulating cell wall development in Arabidopsis Yu, Liangliang; Liu, Yan; Liu, Yumin Plant Cell Reports, Vol. 35, Issue 12 https://doi.org/10.1007/s00299-016-2050-7	journal	September 2016
WRKY transcription factors and plant defense responses: latest discoveries and future prospects Wani, Shabir H.; Anand, Shruti; Singh, Balwant Plant Cell Reports, Vol. 40, Issue 7 https://doi.org/10.1007/s00299-021-02691-8	journal	April 2021
The Arabidopsis ubiquitin ligases ATL31 and ATL6 control the defense response as well as the carbon/nitrogen response Maekawa, Shugo; Sato, Takeo; Asada, Yutaka Plant Molecular Biology, Vol. 79, Issue 3 https://doi.org/10.1007/s11103-012-9907-0	journal	April 2012
Comparative analysis of PSK peptide growth factor precursor homologs Lorbiecke, René; Sauter, Margret Plant Science, Vol. 163, Issue 2 https://doi.org/10.1016/S0168-9452(02)00101-2	journal	August 2002
Peptide signalling in plant development and self/non-self perception Boller, Thomas Current Opinion in Cell Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.ceb.2005.02.007	journal	April 2005
Suppression of ETI by PTI priming to balance plant growth and defense through an MPK3/MPK6-WRKYs-PP2Cs module Wang, Dacheng; Wei, Lirong; Liu, Ting Molecular Plant, Vol. 16, Issue 5 https://doi.org/10.1016/j.molp.2023.04.004	journal	May 2023
The Arabidopsis bZIP transcription factor family — an update Dröge-Laser, Wolfgang; Snoek, Basten L.; Snel, Berend Current Opinion in Plant Biology, Vol. 45 https://doi.org/10.1016/j.pbi.2018.05.001	journal	October 2018
Microbial signature-triggered plant defense responses and early signaling mechanisms Wu, Shujing; Shan, Libo; He, Ping Plant Science, Vol. 228 https://doi.org/10.1016/j.plantsci.2014.03.001	journal	November 2014
WRKY transcription factors in plant defense Javed, Talha; Gao, San-Ji Trends in Genetics, Vol. 39, Issue 10 https://doi.org/10.1016/j.tig.2023.07.001	journal	October 2023
WRKY transcription factors Rushton, Paul J.; Somssich, Imre E.; Ringler, Patricia Trends in Plant Science, Vol. 15, Issue 5 https://doi.org/10.1016/j.tplants.2010.02.006	journal	May 2010
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke Nature, Vol. 448, Issue 7152 https://doi.org/10.1038/nature05999	journal	July 2007
Allosteric receptor activation by the plant peptide hormone phytosulfokine Wang, Jizong; Li, Hongju; Han, Zhifu Nature, Vol. 525, Issue 7568 https://doi.org/10.1038/nature14858	journal	August 2015
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
PSKR1 balances the plant growth–defence trade-off in the rhizosphere microbiome Song, Siyu; Morales Moreira, Zayda; Briggs, Annika L. Nature Plants, Vol. 9, Issue 12 https://doi.org/10.1038/s41477-023-01539-1	journal	November 2023
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
Linking the network centrality measures closeness and degree Evans, Tim S.; Chen, Bingsheng Communications Physics, Vol. 5, Issue 1 https://doi.org/10.1038/s42005-022-00949-5	journal	July 2022
Plants have a sensitive perception system for the most conserved domain of bacterial flagellin: Plants perceive a conserved domain of bacterial flagellin Felix, Georg; Duran, Juliana D.; Volko, Sigrid The Plant Journal, Vol. 18, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.00265.x	journal	May 1999
The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants Heese, A.; Hann, D. R.; Gimenez-Ibanez, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 29 https://doi.org/10.1073/pnas.0705306104	journal	July 2007
Identification of tyrosylprotein sulfotransferase in Arabidopsis Komori, Ryota; Amano, Yukari; Ogawa-Ohnishi, Mari Proceedings of the National Academy of Sciences, Vol. 106, Issue 35 https://doi.org/10.1073/pnas.0902801106	journal	September 2009
Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases Mbengue, Malick; Bourdais, Gildas; Gervasi, Fabio Proceedings of the National Academy of Sciences, Vol. 113, Issue 39 https://doi.org/10.1073/pnas.1606004113	journal	September 2016
Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Matsubayashi, Y.; Sakagami, Y. Proceedings of the National Academy of Sciences, Vol. 93, Issue 15 https://doi.org/10.1073/pnas.93.15.7623	journal	July 1996
Identification of Ligand Binding Site of Phytosulfokine Receptor by On-column Photoaffinity Labeling Shinohara, Hidefumi; Ogawa, Mari; Sakagami, Youji Journal of Biological Chemistry, Vol. 282, Issue 1 https://doi.org/10.1074/jbc.M604558200	journal	January 2007
The WRKY Transcription Factor Family in Model Plants and Crops Chen, Fei; Hu, Yue; Vannozzi, Alessandro Critical Reviews in Plant Sciences, Vol. 36, Issue 5-6 https://doi.org/10.1080/07352689.2018.1441103	journal	November 2017
Callose biosynthesis in arabidopsis with a focus on pathogen response: what we have learned within the last decade Ellinger, Dorothea; Voigt, Christian A. Annals of Botany, Vol. 114, Issue 6 https://doi.org/10.1093/aob/mcu120	journal	July 2014
Complex heatmaps reveal patterns and correlations in multidimensional genomic data Gu, Zuguang; Eils, Roland; Schlesner, Matthias Bioinformatics, Vol. 32, Issue 18 https://doi.org/10.1093/bioinformatics/btw313	journal	May 2016
Role and mechanisms of callose priming in mycorrhiza-induced resistance Sanmartín, Neus; Pastor, Victoria; Pastor-Fernández, Julia Journal of Experimental Botany, Vol. 71, Issue 9 https://doi.org/10.1093/jxb/eraa030	journal	January 2020
Beneficial rhizobacteria Pseudomonas simiae WCS417 induce major transcriptional changes in plant sugar transport Desrut, Antoine; Moumen, Bouziane; Thibault, Florence Journal of Experimental Botany, Vol. 71, Issue 22 https://doi.org/10.1093/jxb/eraa396	journal	August 2020
Tyrosylprotein sulfotransferase-dependent and -independent regulation of root development and signaling by PSK LRR receptor kinases in Arabidopsis Kaufmann, Christine; Stührwohldt, Nils; Sauter, Margret Journal of Experimental Botany, Vol. 72, Issue 15 https://doi.org/10.1093/jxb/erab233	journal	May 2021
Message in a bottle: small signalling peptide outputs during growth and development Czyzewicz, Nathan; Yue, Kun; Beeckman, Tom Journal of Experimental Botany, Vol. 64, Issue 17 https://doi.org/10.1093/jxb/ert283	journal	September 2013
Phytosulfokine peptide signalling Sauter, Margret Journal of Experimental Botany, Vol. 66, Issue 17 https://doi.org/10.1093/jxb/erv071	journal	March 2015
Sulfated plant peptide hormones Kaufmann, Christine; Sauter, Margret Journal of Experimental Botany, Vol. 70, Issue 16 https://doi.org/10.1093/jxb/erz292	journal	June 2019
Activation of Defense Response Pathways by OGs and Flg22 Elicitors in Arabidopsis Seedlings Denoux, Carine; Galletti, Roberta; Mammarella, Nicole Molecular Plant, Vol. 1, Issue 3 https://doi.org/10.1093/mp/ssn019	journal	May 2008
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools Lamesch, Philippe; Berardini, Tanya Z.; Li, Donghui Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1090	journal	December 2011
Regulation of the NADPH Oxidase RBOHD During Plant Immunity Kadota, Yasuhiro; Shirasu, Ken; Zipfel, Cyril Plant and Cell Physiology, Vol. 56, Issue 8 https://doi.org/10.1093/pcp/pcv063	journal	May 2015
Ubiquitylation of PHYTOSULFOKINE RECEPTOR 1 modulates the defense response in tomato Hu, Zhangjian; Fang, Hanmo; Zhu, Changan Plant Physiology, Vol. 192, Issue 3 https://doi.org/10.1093/plphys/kiad188	journal	March 2023
A Suite of Receptor-Like Kinases and a Putative Mechano-Sensitive Channel Are Involved in Autoimmunity and Plasma Membrane–Based Defenses in Arabidopsis Zhang, Zhongqin; Tateda, Chika; Jiang, Shang-Chuan Molecular Plant-Microbe Interactions®, Vol. 30, Issue 2 https://doi.org/10.1094/MPMI-09-16-0184-R	journal	February 2017
Diversity of Arabidopsis Genes Encoding Precursors for Phytosulfokine, a Peptide Growth Factor Yang, Heping; Matsubayashi, Yoshikatsu; Nakamura, Kenzo Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010452	journal	November 2001
Disruption and Overexpression of Arabidopsis Phytosulfokine Receptor Gene Affects Cellular Longevity and Potential for Growth Matsubayashi, Yoshikatsu; Ogawa, Mari; Kihara, Hitomi Plant Physiology, Vol. 142, Issue 1 https://doi.org/10.1104/pp.106.081109	journal	July 2006
Auxin Signaling Leyser, Ottoline Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.00765	journal	August 2017
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors Xu, Xinping; Chen, Chunhong; Fan, Baofang The Plant Cell, Vol. 18, Issue 5 https://doi.org/10.1105/tpc.105.037523	journal	April 2006
Salicylic Acid Regulates Arabidopsis Microbial Pattern Receptor Kinase Levels and Signaling Tateda, Chika; Zhang, Zhongqin; Shrestha, Jay The Plant Cell, Vol. 26, Issue 10 https://doi.org/10.1105/tpc.114.131938	journal	October 2014
Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H⁺-ATPase, and BAK1 Ladwig, Friederike; Dahlke, Renate I.; Stührwohldt, Nils The Plant Cell, Vol. 27, Issue 6 https://doi.org/10.1105/tpc.15.00306	journal	June 2015
Induced Genome-Wide Binding of Three Arabidopsis WRKY Transcription Factors during Early MAMP-Triggered Immunity Birkenbihl, Rainer P.; Kracher, Barbara; Roccaro, Mario The Plant Cell, Vol. 29, Issue 1 https://doi.org/10.1105/tpc.16.00681	journal	December 2016
A MPK3/6-WRKY33-ALD1-Pipecolic Acid Regulatory Loop Contributes to Systemic Acquired Resistance Wang, Yiming; Schuck, Stefan; Wu, Jingni The Plant Cell, Vol. 30, Issue 10 https://doi.org/10.1105/tpc.18.00547	journal	September 2018
Proteolytic processing of a precursor protein for a growth‐promoting peptide by a subtilisin serine protease in Arabidopsis Srivastava, Renu; Liu, Jian‐Xiang; Howell, Stephen H. The Plant Journal, Vol. 56, Issue 2 https://doi.org/10.1111/j.1365-313X.2008.03598.x	journal	October 2008
PSK‐α promotes root growth in Arabidopsis Kutschmar, Anke; Rzewuski, Guillaume; Stührwohldt, Nils New Phytologist, Vol. 181, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02710.x	journal	December 2008
Callose metabolism and the regulation of cell walls and plasmodesmata during plant mutualistic and pathogenic interactions German, Liam; Yeshvekar, Richa; Benitez‐Alfonso, Yoselin Plant, Cell & Environment, Vol. 46, Issue 2 https://doi.org/10.1111/pce.14510	journal	December 2022
The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner Mosher, Stephen; Seybold, Heike; Rodriguez, Patricia The Plant Journal, Vol. 73, Issue 3 https://doi.org/10.1111/tpj.12050	journal	November 2012
Phytosulfokine control of growth occurs in the epidermis, is likely to be non‐cell autonomous and is dependent on brassinosteroids Hartmann, Jens; Stührwohldt, Nils; Dahlke, Renate I. The Plant Journal, Vol. 73, Issue 4 https://doi.org/10.1111/tpj.12056	journal	December 2012
Kinase activity and calmodulin binding are essential for growth signaling by the phytosulfokine receptor PSKR1 Hartmann, Jens; Fischer, Cornelia; Dietrich, Petra The Plant Journal, Vol. 78, Issue 2 https://doi.org/10.1111/tpj.12460	journal	March 2014
An LRR Receptor Kinase Involved in Perception of a Peptide Plant Hormone, Phytosulfokine Matsubayashi, Yoshikatsu; Ogawa, Mari; Morita, Akiko Science, Vol. 296, Issue 5572 https://doi.org/10.1126/science.1069607	journal	May 2002
Metabolic Diversification--Independent Assembly of Operon-Like Gene Clusters in Different Plants Field, B.; Osbourn, A. E. Science, Vol. 320, Issue 5875 https://doi.org/10.1126/science.1154990	journal	April 2008
Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex Sun, Y.; Li, L.; Macho, A. P. Science, Vol. 342, Issue 6158 https://doi.org/10.1126/science.1243825	journal	October 2013
Peptide ligand-mediated trade-off between plant growth and stress response Ogawa-Ohnishi, Mari; Yamashita, Tomohide; Kakita, Mitsuru Science, Vol. 378, Issue 6616 https://doi.org/10.1126/science.abq5735	journal	October 2022
Posttranslationally Modified Small-Peptide Signals in Plants Matsubayashi, Yoshikatsu Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120122	journal	April 2014
Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences Frei dit Frey, Nicolas; Garcia, Ana; Bigeard, Jean Genome Biology, Vol. 15, Issue 6 https://doi.org/10.1186/gb-2014-15-6-r87	journal	January 2014
Calcium is the switch in the moonlighting dual function of the ligand-activated receptor kinase phytosulfokine receptor 1 Muleya, Victor; Wheeler, Janet I.; Ruzvidzo, Oziniel Cell Communication and Signaling, Vol. 12, Issue 1 https://doi.org/10.1186/s12964-014-0060-z	journal	September 2014
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Gibberellin signaling in plants Daviere, J. -M.; Achard, P. Development, Vol. 140, Issue 6 https://doi.org/10.1242/dev.087650	journal	February 2013
ESCRT-I Mediates FLS2 Endosomal Sorting and Plant Immunity Spallek, Thomas; Beck, Martina; Ben Khaled, Sara PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1004035	journal	December 2013
Phytosulfokine-α Controls Hypocotyl Length and Cell Expansion in Arabidopsis thaliana through Phytosulfokine Receptor 1 Stührwohldt, Nils; Dahlke, Renate I.; Steffens, Bianka PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0021054	journal	June 2011
Loss of Arabidopsis thaliana Dynamin-Related Protein 2B Reveals Separation of Innate Immune Signaling Pathways Smith, John M.; Leslie, Michelle E.; Robinson, Samuel J. PLoS Pathogens, Vol. 10, Issue 12 https://doi.org/10.1371/journal.ppat.1004578	journal	December 2014
Sustained mitogen-activated protein kinase activation reprograms defense metabolism and phosphoprotein profile in Arabidopsis thaliana Lassowskat, Ines; BÃ¶ttcher, Christoph; Eschen-Lippold, Lennart Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00554	journal	October 2014
Regulation of WRKY46 Transcription Factor Function by Mitogen-Activated Protein Kinases in Arabidopsis thaliana Sheikh, Arsheed H.; Eschen-Lippold, Lennart; Pecher, Pascal Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00061	journal	February 2016
Moonlighting Proteins and Their Role in the Control of Signaling Microenvironments, as Exemplified by cGMP and Phytosulfokine Receptor 1 (PSKR1) Irving, Helen R.; Cahill, David M.; Gehring, Chris Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00415	journal	March 2018
Regulation and Function of Defense-Related Callose Deposition in Plants Wang, Ying; Li, Xifeng; Fan, Baofang International Journal of Molecular Sciences, Vol. 22, Issue 5 https://doi.org/10.3390/ijms22052393	journal	February 2021
Induced Endocytosis of the Receptor Kinase FLS2 Salomon, Susanne; Robatzek, Silke Plant Signaling & Behavior, Vol. 1, Issue 6 https://doi.org/10.4161/psb.1.6.3594	journal	November 2006

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