Project 1: Integrative analysis of stress responses

Abstract:

The project aim was to understand the molecular mechanisms occurring in time and space to control gene expression of plants in response to environmental challenges. For this purpose, we developed a phosphoproteomics pipeline to analyze signaling events in response to stress and analyzed the early events upon pathogen-associated molecular pattern (PAMP) signaling in Arabidopsis. In the framework of the project, we could identify a large set of novel chromatin proteins that become phosphorylated in response to PAMP signaling. Several of these factors were identified as MAPK targets and further characterized in the context of PAMP-triggered immunity.

Publications:

Berriri S., Garcia A.V., Frey N.F.D., Rozhon W., Pateyron S., Leonhardt N., Montillet J.-L., Leung J., Hirt H., Colcombet J. (2012). Constitutively Active Mitogen-Activated Protein Kinase Versions Reveal Functions of Arabidopsis MPK4 in Pathogen Defense Signaling. Plant Cell 24(10): 4281-4293.

Bigeard J., Rayapuram N., Bonhomme L., Hirt H., Pflieger D. (2014). Proteomic and phosphoproteomic analyses of chromatin-associated proteins from Arabidopsis thaliana. Proteomics 14(19): 2141-2155.

Bigeard J., Rayapuram N., Pflieger D., Hirt H. (2014). Phosphorylation-dependent regulation of plant chromatin and chromatin-associated proteins. Proteomics 14(19): 2127-2140.

Bigeard J., Colcombet J., Hirt H. (2015). Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant. 8(4):521-539.

Frey N.F.D., Garcia A.V., Bigeard J., Zaag R., Bueso E., Garmier M., Pateyron S., de Tauzia-Moreau M.-L., Brunaud V., Balzergue S., Colcombet J., Aubourg S., Martin-Magniette M.-L., Hirt H. (2014). Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences. Genome Biology 15(6): R87.

Genot B, Lang J, Berriri S, Garmier M, Gilard F, Pateyron S, Haustraete K, Van Der Straeten D, Hirt H, Colcombet J*. (2017) Constitutively active Arabidopsis MAP Kinase 3 triggers defense responses involving salicylic acid and SUMM2 resistance protein. Plant Physiol. 174:1238

Jegu T., Latrasse D., Delarue M., Hirt H., Domenichini S., Ariel F., Crespi M., Bergounioux C., Raynaud C., Benhamed M. (2014). The BAF60 Subunit of the SWI/SNF Chromatin-Remodeling Complex Directly Controls the Formation of a Gene Loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26(2): 538-551.

Jiang Y, Han B, Zhang H., Mariappan K, Bigeard J, Colcombet J, Hirt H (2019). MAP4K4 associates with BIK1 to regulate plant innate immunity. EMBO reports 20(11):e47965

Latrasse D., Jegu T., Meng P.-H., Mazubert C., Hudik E., Delarue M., Charon C., Crespi M., Hirt H., Raynaud C., Bergounioux C., Benhamed M. (2013). Dual function of MIPS1 as a metabolic enzyme and transcriptional regulator. Nucleic Acids Research 41(5): 2907-2917.

Latrasse D., Jégu T., Li H., de Zelicourt A., Raynaud C., Legras S., Gust A., Samajova O., Veluchamy A., Rayapuram N., Ramirez-Prado J., Kulikova O., Colcombet J., Bigeard J., Genot B., Bisseling T., Benhamed M., Hirt H. (2017). MAPK-triggered chromatin reprogramming by histone deacetylase in plant innate immunity. Genome Biology 18: 131.

Rayapuram N., Bonhomme L., Bigeard J., Haddadou K., Przybylski C., Hirt H., Pflieger D. (2014). Identification of Novel PAMP-Triggered Phosphorylation and Dephosphorylation Events in Arabidopsis thaliana by Quantitative Phosphoproteomic Analysis. Journal of Proteome Research 13(4): 2137-2151.

Rayapuram N, Bigeard J, Alhoraibi H, Bonhomme L, Hesse AM, Vinh J, Hirt H, Pflieger D. (2018) Quantitative Phosphoproteomic Analysis Reveals Shared and Specific Targets of Arabidopsis Mitogen-Activated Protein Kinases (MAPKs) MPK3, MPK4, and MPK6. Mol Cell Proteomics. 17(1):61-80.

Rayapuram N., Jarad M., Alhoraibi H., Bigeard J., Abulfaraj A., Völz R., Mariappan K., Almeida-Trapp M., Schlöffel M., Lastrucci E.,  Bonhomme L., Gust A., Mithöfer A., Arold S., Pflieger D., Hirt H. (2021) Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity.  Proc Natl Acad Sci U S A. 118(3):e2004670118.

Vandenbogaert M., Hourdel V., Jardin-Mathe O., Bigeard J., Bonhomme L., Legros V., Hirt H., Schwikowski B., Pflieger D. (2012). Automated Phosphopeptide Identification Using Multiple MS/MS Fragmentation Modes. Journal of Proteome Research 11(12): 5695-5703.

Völz R, Kim SK, Mi J, Mariappan KG, Guo X, Bigeard J, Alejandro S, Pflieger D, Rayapuram N, Al-Babili S, Hirt H. (2018) The Trihelix transcription factor GT2-like 1 (GTL1) promotes salicylic acid metabolism, and regulates bacterial-triggered immunity. PLoS Genet. 14(10):e1007708

Communications in conferences:

Heribert Hirt – “Signal transduction and gene expression at the chromatin level” - Gordon Research Conferences: Posttranslational Modification Networks - Phosphosignaling, The Hong Kong University of Science and Technology, Hong Kong, July 28 – August 2, 2013

Delphine Pflieger - “Phosphoproteomics of the chromatin in Arabidopsis thaliana subjected to biotic stress” - 3rd European Plant Chromatin Workshop, Madrid, August 29 – 30, 2013

Heribert Hirt – “Post-translational proteomic approaches to investigate signal transduction of plant-pathogen interactions” - Plant Biology Lectures, Buenos Aires, Argentina, November 13-15, 2013

Heribert Hirt – “From signal to chromatin” - Plant Signaling Meeting, Cologne, Germany, March 25-27, 2014

Heribert Hirt – “Post-translational signal transduction mechanisms in plant microbe interactions” -- Plant Signaling and Networks, Gordon Conference, New Hampshire, USA, July 20-25, 2015

Naganand Rayapuram – “Identification of MPK3, MPK4 and MPK6 target by phosphoproteomics” – Gordon Conference on Post-Translational Modification Networks, Hong Kong, China, August 11-18, 2017

Heribert Hirt – “From signaling to chromatin” – Taiwan Academy of Sciences, Taipei, Taiwan, August 21, 2017

Heribert Hirt – “From signaling to chromatin” – Biotic Stress Conference, Shanghai, China, August 22-24, 2017

Other outputs:

The developed program is available at: http://proteomics.fr/FragMixer/