Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity
Abulfaraj, Aala A.
Gust, Andrea A.
Arold, Stefan T.
KAUST DepartmentBiological and Environmental Sciences and Engineering (BESE) Division
Desert Agriculture Initiative
Red Sea Research Center (RSRC)
Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia.
Computational Bioscience Research Center (CBRC)
Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division
Computational Bioscience Research Center, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia.
KAUST Grant NumberBAS/1/1062-01-01
Embargo End Date2021-07-08
Permanent link to this recordhttp://hdl.handle.net/10754/666869
MetadataShow full item record
AbstractIn many eukaryotic systems during immune responses, mitogen-activated protein kinases (MAPKs) link cytoplasmic signaling to chromatin events by targeting transcription factors, chromatin remodeling complexes, and the RNA polymerase machinery. So far, knowledge on these events is scarce in plants and no attempts have been made to focus on phosphorylation events of chromatin-associated proteins. Here we carried out chromatin phosphoproteomics upon elicitor-induced activation of Arabidopsis. The events in WT were compared with those in mpk3, mpk4, and mpk6 mutant plants to decipher specific MAPK targets. Our study highlights distinct signaling networks involving MPK3, MPK4, and MPK6 in chromatin organization and modification, as well as in RNA transcription and processing. Among the chromatin targets, we characterized the AT-hook motif containing nuclear localized (AHL) DNA-binding protein AHL13 as a substrate of immune MAPKs. AHL13 knockout mutant plants are compromised in pathogen-associated molecular pattern (PAMP)-induced reactive oxygen species production, expression of defense genes, and PAMP-triggered immunity. Transcriptome analysis revealed that AHL13 regulates key factors of jasmonic acid biosynthesis and signaling and affects immunity toward Pseudomonas syringae and Botrytis cinerea pathogens. Mutational analysis of the phosphorylation sites of AHL13 demonstrated that phosphorylation regulates AHL13 protein stability and thereby its immune functions.
CitationRayapuram, N., Jarad, M., Alhoraibi, H. M., Bigeard, J., Abulfaraj, A. A., Völz, R., … Hirt, H. (2021). Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity. Proceedings of the National Academy of Sciences, 118(3), e2004670118. doi:10.1073/pnas.2004670118
SponsorsWe thank Véronique Legros, Huma Khurram, and Huoming Zhang for technical assistance in mass spectometry; Stéphanie Pateyron and Alexandra Avon for technical support in molecular biology; and Jean Colcombet for kindly providing the constitutively active MAPK vectors. This work was supported by Agence Nationale de la Recherche ANR-2010-JCJC-1608 and ANR-14-CE19-0014 (to D.P.); Investissement d’Avenir Infrastructures Nationales en Biologie et Santé program (ProFI project, ANR10-INBS-08); and by King Abdullah University of Science and Technology BAS/1/1062-01-01 (to H.H.). The Institute of Plant Sciences Paris-Saclay benefits from the support of the LabEx Saclay Plant Sciences (ANR-10-LABX-0040-SPS). M.A.-T. was supported by a Humboldt-Capes fellowship.
CollectionsArticles; Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC); Bioscience Program; Computational Bioscience Research Center (CBRC); Desert Agriculture Initiative; Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division
- Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences.
- Authors: Frei dit Frey N, Garcia AV, Bigeard J, Zaag R, Bueso E, Garmier M, Pateyron S, de Tauzia-Moreau ML, Brunaud V, Balzergue S, Colcombet J, Aubourg S, Martin-Magniette ML, Hirt H
- Issue date: 2014 Jun 30
- A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity.
- Authors: Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S
- Issue date: 2014 Jan
- MAP kinase signalling: interplays between plant PAMP- and effector-triggered immunity.
- Authors: Thulasi Devendrakumar K, Li X, Zhang Y
- Issue date: 2018 Aug
- Role of MPK4 in pathogen-associated molecular pattern-triggered alternative splicing in Arabidopsis.
- Authors: Bazin J, Mariappan K, Jiang Y, Blein T, Voelz R, Crespi M, Hirt H
- Issue date: 2020 Apr
- Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance.
- Authors: Meng X, Xu J, He Y, Yang KY, Mordorski B, Liu Y, Zhang S
- Issue date: 2013 Mar