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SUMO enables substrate selectivity by mitogen-activated protein kinases to regulate immunity in plants

Verma, Vivek; Srivastava, Anjil K.; Gough, Catherine; Campanaro, Alberto; Srivastava, Moumita; Morrell, Rebecca; Joyce, Joshua; Bailey, Mark; Zhang, Cunjin; Krysan, Patrick J.; Sadanandom, Ari

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Authors

Vivek Verma

Anjil K. Srivastava

Alberto Campanaro

Moumita Srivastava

Rebecca Morrell rebecca.e.morrell@durham.ac.uk
PGR Student Doctor of Philosophy

Joshua Joyce

Mark Bailey

Patrick J. Krysan



Abstract

The versatility of mitogen-activated protein kinases (MAPKs) in translating exogenous and endogenous stimuli into appropriate cellular responses depends on its substrate specificity. In animals, several mechanisms have been proposed about how MAPKs maintain specificity to regulate distinct functional pathways. However, little is known of mechanisms that enable substrate selectivity in plant MAPKs. Small ubiquitin-like modifier (SUMO), a posttranslational modification system, plays an important role in plant development and defense by rapid reprogramming of cellular events. In this study we identified a functional SUMO interaction motif (SIM) in Arabidopsis MPK3 and MPK6 that reveals a mechanism for selective interaction of MPK3/6 with SUMO-conjugated WRKY33, during defense. We show that WRKY33 is rapidly SUMOylated in response to Botrytis cinerea infection and flg22 elicitor treatment. SUMOylation mediates WRKY33 phosphorylation by MPKs and consequent transcription factor activity. Disruption of either WRKY33 SUMO or MPK3/6 SIM sites attenuates their interaction and inactivates WRKY33-mediated defense. However, MPK3/6 SIM mutants show normal interaction with a non-SUMOylated form of another transcription factor, SPEECHLESS, unraveling a role for SUMOylation in differential substrate selectivity by MPKs. We reveal that the SUMO proteases, SUMO PROTEASE RELATED TO FERTILITY1 (SPF1) and SPF2 control WRKY33 SUMOylation and demonstrate a role for these SUMO proteases in defense. Our data reveal a mechanism by which MPK3/6 prioritize molecular pathways by differentially selecting substrates using the SUMO–SIM module during defense responses.

Citation

Verma, V., Srivastava, A. K., Gough, C., Campanaro, A., Srivastava, M., Morrell, R., …Sadanandom, A. (2021). SUMO enables substrate selectivity by mitogen-activated protein kinases to regulate immunity in plants. Proceedings of the National Academy of Sciences, 118(10), Article e2021351118. https://doi.org/10.1073/pnas.2021351118

Journal Article Type Article
Acceptance Date Jan 20, 2021
Online Publication Date Mar 1, 2021
Publication Date Mar 9, 2021
Deposit Date Jun 24, 2021
Publicly Available Date Jun 24, 2021
Journal Proceedings of the National Academy of Sciences
Print ISSN 0027-8424
Electronic ISSN 1091-6490
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 118
Issue 10
Article Number e2021351118
DOI https://doi.org/10.1073/pnas.2021351118

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