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

Nicolas Frei dit Frey12, Ana Victoria Garcia1, Jean Bigeard1, Rim Zaag1, Eduardo Bueso1, Marie Garmier3, Stéphanie Pateyron14, Marie-Ludivine de Tauzia-Moreau1, Véronique Brunaud1, Sandrine Balzergue14, Jean Colcombet1, Sébastien Aubourg1, Marie-Laure Martin-Magniette156 and Heribert Hirt17*

Author Affiliations

1 Unité de Recherche en Génomique Végétale (URGV), UMR INRA 1165 - Université d’Evry Val d’Essonne - ERL CNRS 8196 - Saclay Plant Sciences, 2 rue Gaston Crémieux, Evry 91057, France

2 Present address: Laboratoire de Recherche en Sciences Végétales (LRSV), UMR 5546, Université Paul Sabatier/CNRS, 24, chemin de Borde Rouge B.P. 42617 Auzeville, Castanet-Tolosan 31326, France

3 Institut de Biologie des Plantes (IBP), CNRS-Université Paris-Sud - UMR 8618 - Saclay Plant Sciences, Orsay, Cedex 91405, France

4 Unité de Recherche en Génomique Végétale (URGV), Plateforme Transcriptome, UMR INRA 1165 - Université d’Evry Val d’Essonne - ERL CNRS 8196, 2 rue Gaston Crémieux, Evry 91057, France

5 AgroParisTech, UMR 518 MIA, Paris 75005, France

6 INRA, UMR 518 MIA, Paris 75005, France

7 Center for Desert Agriculture, 4700 King Abdullah University of Sciences and Technology, Thuwal 23955-6900, Saudi Arabia

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Genome Biology 2014, 15:R87  doi:10.1186/gb-2014-15-6-r87

Published: 30 June 2014

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.