Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences

Genome Biol. 2014 Jun 30;15(6):R87. doi: 10.1186/gb-2014-15-6-r87.

Abstract

Background: Mitogen-activated protein kinases (MAPKs) are key regulators of immune responses in animals and plants. In Arabidopsis, perception of microbe-associated molecular patterns (MAMPs) activates the MAPKs MPK3, MPK4 and MPK6. Increasing information depicts the molecular events activated by MAMPs in plants, but the specific and cooperative contributions of the MAPKs in these signalling events are largely unclear.

Results: In this work, we analyse the behaviour of MPK3, MPK4 and MPK6 mutants in early and late immune responses triggered by the MAMP flg22 from bacterial flagellin. A genome-wide transcriptome analysis reveals that 36% of the flg22-upregulated genes and 68% of the flg22-downregulated genes are affected in at least one MAPK mutant. So far MPK4 was considered as a negative regulator of immunity, whereas MPK3 and MPK6 were believed to play partially redundant positive functions in defence. Our work reveals that MPK4 is required for the regulation of approximately 50% of flg22-induced genes and we identify a negative role for MPK3 in regulating defence gene expression, flg22-induced salicylic acid accumulation and disease resistance to Pseudomonas syringae. Among the MAPK-dependent genes, 27% of flg22-upregulated genes and 76% of flg22-downregulated genes require two or three MAPKs for their regulation. The flg22-induced MAPK activities are differentially regulated in MPK3 and MPK6 mutants, both in amplitude and duration, revealing a highly interdependent network.

Conclusions: These data reveal a new set of distinct functions for MPK3, MPK4 and MPK6 and indicate that the plant immune signalling network is choreographed through the interplay of these three interwoven MAPK pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology*
  • Arabidopsis / immunology
  • Arabidopsis Proteins / physiology*
  • Disease Resistance
  • Flagellin / immunology
  • Gene Expression Regulation, Plant / immunology
  • Gene Regulatory Networks
  • Mitogen-Activated Protein Kinase Kinases / physiology*
  • Mitogen-Activated Protein Kinases / physiology
  • Oligonucleotide Array Sequence Analysis
  • Plant Immunity
  • Pseudomonas syringae / immunology
  • Transcriptional Activation
  • Transcriptome

Substances

  • Arabidopsis Proteins
  • Flagellin
  • AtMPK3 protein, Arabidopsis
  • AtMPK4 protein, Arabidopsis
  • MPK6 protein, Arabidopsis
  • Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase Kinases