Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress

PLoS Genet. 2015 Jul 21;11(7):e1005373. doi: 10.1371/journal.pgen.1005373. eCollection 2015 Jul.

Abstract

Cysteine-rich receptor-like kinases (CRKs) are transmembrane proteins characterized by the presence of two domains of unknown function 26 (DUF26) in their ectodomain. The CRKs form one of the largest groups of receptor-like protein kinases in plants, but their biological functions have so far remained largely uncharacterized. We conducted a large-scale phenotyping approach of a nearly complete crk T-DNA insertion line collection showing that CRKs control important aspects of plant development and stress adaptation in response to biotic and abiotic stimuli in a non-redundant fashion. In particular, the analysis of reactive oxygen species (ROS)-related stress responses, such as regulation of the stomatal aperture, suggests that CRKs participate in ROS/redox signalling and sensing. CRKs play general and fine-tuning roles in the regulation of stomatal closure induced by microbial and abiotic cues. Despite their great number and high similarity, large-scale phenotyping identified specific functions in diverse processes for many CRKs and indicated that CRK2 and CRK5 play predominant roles in growth regulation and stress adaptation, respectively. As a whole, the CRKs contribute to specificity in ROS signalling. Individual CRKs control distinct responses in an antagonistic fashion suggesting future potential for using CRKs in genetic approaches to improve plant performance and stress tolerance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics*
  • Arabidopsis / enzymology
  • Arabidopsis / genetics*
  • Arabidopsis / immunology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Ascomycota / immunology
  • DNA, Bacterial / genetics
  • Gene Expression Regulation, Plant
  • Oxidative Stress / immunology*
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Pseudomonas syringae / immunology
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / genetics
  • Xanthine Oxidase / metabolism

Substances

  • Arabidopsis Proteins
  • DNA, Bacterial
  • Reactive Oxygen Species
  • T-DNA
  • Xanthine Oxidase
  • RLK5 protein, Arabidopsis
  • Protein Serine-Threonine Kinases
  • receptor-like protein kinase 2, Arabidopsis

Grants and funding

This work has been performed in an ERA-PG consortium “PROSIG” (http://www.erapg.org/). GB was supported by a grant of the Deutsche Forschungsgemeinschaft (http://dfg.de/; ERA-PG PROSIG), DTA by an ERASMUS fellowship. Research of the SR laboratory is supported by the Gatsby Charitable Foundation (http://www.gatsby.org.uk/) and a grant by the European Research Council (http://erc.europa.eu/; ERC STORM). LN was supported by a grant from the Netherlands Organization for Scientific Research (ERA-PG research grant NWO-PROSIG, (www.nwo.nl; 855.50.018). Ska and his group members acknowledge the support of the Welcome2008/1 program operated within the framework of the Foundation for Polish Science (https://www.fnp.org.pl/en/), co-financed by the European Regional Development Fund (http://ec.europa.eu/regional_policy/index.cfm/en/funding/erdf/), of the REGPOT project FP7-286093 WULS-PLANT HEALTH, and of the Polish National Science Centre (https://www.ncn.gov.pl/) Maestro6 project UMO-2014/14/A/NZ1/00218. KO acknowledges the support of the Polish National Science Centre (https://www.ncn.gov.pl/) Sonata2 project UMO-2011/03/D/NZ9/04059). DBC, MFL and CR acknowledge the Danish Research Council FTP (http://ufm.dk/forskning-og-innovation/rad-og-udvalg/det-frie-forskningsrad) for financial support via the projects “Unravelling plant regulatory networks” (09-062964), “Characterization of the barley CRK/DUF26 receptor-like protein kinase family in relation to drought, salt and cold stress” (11-117019) and “Climate change effects on plant health” (09-065066). HK was supported by Estonian Research Council (http://www.etag.ee/en/estonian-research-council/; IUT2–21) and European Regional Fund (http://ec.europa.eu/regional_policy/index.cfm/en/funding/erdf/; Center of Excellence in Environmental Adaptation). Research in the laboratory of JK was supported by the Academy of Finland (http://www.aka.fi; ERA-PG research grant #129940, Centre of Excellence program 2006–2010 #213509, #129628 and 2014–2019 #271832), Biocentrum Helsinki (http://www.helsinki.fi/biocentrum/) and the University of Helsinki (https://university.helsinki.fi/). Research in the group of MW is supported by the University of Helsinki (https://university.helsinki.fi/; Post-doctoral grant and three year fund allocation) and the Academy of Finland (http://www.aka.fi; decisions #275632 and #283139). AV is supported by the Doctoral Programme in Plant Sciences (http://www.helsinki.fi/dpps/index.htm) in the Doctoral School in Environmental, Food and Biological sciences at the University of Helsinki. AG was supported by a post-doctoral grant by the Academy of Finland (http://www.aka.fi; #140187). NI was supported by the Finnish Graduate School in Plant Biology (http://www.helsinki.fi/fdpps/). Phenotyping at Helmholtz Zentrum München is supported by the European and German Plant Phenotying Networks (EPPN http://www.plant-phenotyping-network.eu/ and DPPN http://www.dppn.de/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.