PROHIBITIN3 forms complexes with ISOCHORISMATE SYNTHASE1 to regulate stress-induced salicylic acid biosynthesis in arabidopsis

Aldo Seguel, Joanna Jelenska, Ariel Herrera-Vásquez, Sharon K. Marr, Michael B. Joyce, Kelsey R. Gagesch, Nadia Shakoor, Shang Chuan Jiang, Alejandro Fonseca, Mary C. Wildermuth, Jean T. Greenberg, Loreto Holuigue

Research output: Contribution to journalArticlepeer-review

43 Scopus citations

Abstract

Salicylic acid (SA) is a major defense signal in plants. In Arabidopsis (Arabidopsis thaliana), the chloroplast-localized isochorismate pathway is the main source of SA biosynthesis during abiotic stress or pathogen infections. In the first step of the pathway, the enzyme ISOCHORISMATE SYNTHASE1 (ICS1) converts chorismate to isochorismate. An unknown enzyme subsequently converts isochorismate to SA. Here, we show that ICS1 protein levels increase during UV-C stress. To identify proteins that may play roles in SA production by regulating ICS1, we analyzed proteins that coimmunoprecipitated with ICS1 via mass spectrometry. The ICS1 complexes contained a large number of peptides from the PROHIBITIN (PHB) protein family, with PHB3 the most abundant. PHB proteins have diverse biological functions that include acting as scaffolds for protein complex formation and stabilization. PHB3 was reported previously to localize to mitochondria. Using fractionation, protease protection, and live imaging, we show that PHB3 also localizes to chloroplasts, where ICS1 resides. Notably, loss of PHB3 function led to decreased ICS1 protein levels in response to UV-C stress. However, ICS1 transcript levels remain unchanged, indicating that ICS1 is regulated posttranscriptionally. The phb3 mutant displayed reduced levels of SA, the SA-regulated protein PR1, and hypersensitive cell death in response to UV-C and avirulent strains of Pseudomonas syringae and, correspondingly, supported increased growth of P. syringae. The expression of a PHB3 transgene in the phb3 mutant complemented all of these phenotypes. We suggest a model in which the formation of PHB3-ICS1 complexes stabilizes ICS1 to promote SA production in response to stress.

Original languageEnglish (US)
Pages (from-to)2515-2531
Number of pages17
JournalPlant physiology
Volume176
Issue number3
DOIs
StatePublished - Mar 2018
Externally publishedYes

Bibliographical note

Funding Information:
1This work was supported by the National Commission for Science and Technology CONICYT (FONDECYT grant 1141202 to L.H.), the Millennium Science Initiative (Nucleus for Plant Synthetic and Systems Biology, grant NC130030 to Rodrigo Gutiérrez and L.H.), the National Institutes of Health (R01 GM54292 to J.T.G.), the National Science Foundation (NSF IOS-1456904 to J.T.G., NSF2010 0822393 to J.T.G. and Richard W. Michelmore, and NSF IOS-1449100 to M.C.W.). A.S. was supported by a PhD. fellowship from CONICYT, K.R.G was supported by NSF training grant 1062713, and N.S. by MCB training grant T32 GM 007183.

Funding Information:
This work was supported by the National Commission for Science and Technology CONICYT (FONDECYT grant 1141202 to L.H.), the Millennium Science Initiative (Nucleus for Plant Synthetic and Systems Biology, grant NC130030 to Rodrigo Gutiérrez and L.H.), the National Institutes of Health (R01 GM54292 to J.T.G.), the National Science Foundation (NSF IOS-1456904 to J.T.G., NSF2010 0822393 to J.T.G. and Richard W. Michelmore, and NSF IOS-1449100 to M.C.W.). A.S. was supported by a PhD. fellowship from CONICYT, K.R.G was supported by NSF training grant 1062713, and N.S. by MCB training grant T32 GM 007183. We thank Hillel Fromm (Tel Aviv University) for providing the PHB3/4 antibody, Dominique Drapier (Centre National de la Recherche Scientifique/ UPMC) for the AtpB antibody, Karl-Josef Dietz (Bielefeld University) for the Prx IIF antibody, Pradeep Kachroo (University of Kentucky) for the NOA1 antibody, Gopal Pattanayak (University of Chicago) for antibodies against Tic110 (from Masato Nakai, Osaka University) and LHCII (from Roberto Bassi, Università di Verona), Thomas Leustek (Rutgers University) for the cpHSP70 antibody, Christoph Benning (Michigan State University) for the SFR2 antibody, Andreas Nebenführ (University of Tennessee) for the COX4-mCherry marker, and Guo-Liang Wang (Ohio State University) for the COX4-dsRed marker. We also thank Jacquelyn Freeman for help with immunoprecipitation experiments and Michael Allara for help with western blots.

Publisher Copyright:
© 2018 American Society of Plant Biologists. All rights reserved.

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