mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana

• Published in: The Plant journal : for cell and molecular biology Vol. 80; no. 4; pp. 709 - 727
• Main Authors: Zhang, Botao, Van Aken, Olivier, Thatcher, Louise, De Clercq, Inge, Duncan, Owen, Law, Simon R, Murcha, Monika W, Merwe, Margaretha, Seifi, Hamed Soren, Carrie, Chris, Cazzonelli, Christopher, Radomiljac, Jordan, Höfte, Monica, Singh, Karam B, Van Breusegem, Frank, Whelan, James
• Format: Journal Article
• Language: English
• Published: England Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology 01.11.2014; Blackwell Publishing Ltd
• Subjects: adenosinetriphosphatase; Apoptosis; Arabidopsis; Arabidopsis - cytology; Arabidopsis - microbiology; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; ATPase; Botrytis - pathogenicity; Botrytis cinerea; cell death; Cell Death - genetics; Cyclopentanes - metabolism; drought tolerance; Droughts; Enzymes; Gene expression; Gene Expression Regulation, Plant; genes; genetic markers; Host-Pathogen Interactions; jasmonic acid; leaf curling; mammals; membrane proteins; Membranes; Mitochondria; mitochondrial membrane; Mitochondrial Membranes - metabolism; Mitochondrial Proteins - genetics; Mitochondrial Proteins - metabolism; Multiprotein Complexes - genetics; Multiprotein Complexes - metabolism; Mutation; Oxylipins - metabolism; pathogen defence; pathogens; Phenotype; Plant Diseases - microbiology; Plant Leaves - cytology; Plant Leaves - genetics; Plant pathology; Plant resistance; Plants, Genetically Modified; protein content; Pseudomonas syringae; Pseudomonas syringae - pathogenicity; Salicylic Acid - metabolism; senescence; sequence homology; starch; stress; Stress, Physiological; transgenic plants; water stress; yeasts; stress; pathogen defence; cell death; Arabidopsis; ATPase; mitochondria
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.12665

One of the most stress‐responsive genes encoding a mitochondrial protein in Arabidopsis (At3g50930) has been annotated as AtBCS1 (cytochrome bc1 synthase 1), but was previously functionally uncharacterised. Here, we show that the protein encoded by At3g50930 is present as a homo‐multimeric protein complex on the outer mitochondrial membrane and lacks the BCS1 domain present in yeast and mammalian BCS1 proteins, with the sequence similarity restricted to the AAA ATPase domain. Thus we propose to re‐annotate this protein as AtOM66 (Outer Mitochondrial membrane protein of 66 kDa). While transgenic plants with reduced AtOM66 expression appear to be phenotypically normal, AtOM66 over‐expression lines have a distinct phenotype, showing strong leaf curling and reduced starch content. Analysis of mitochondrial protein content demonstrated no detectable changes in mitochondrial respiratory complex protein abundance. Consistent with the stress inducible expression pattern, over‐expression lines of AtOM66 are more tolerant to drought stress but undergo stress‐induced senescence earlier than wild type. Genome‐wide expression analysis revealed a constitutive induction of salicylic acid‐related (SA) pathogen defence and cell death genes in over‐expression lines. Conversely, expression of SA marker gene PR‐1 was reduced in atom66 plants, while jasmonic acid response genes PDF1.2 and VSP2 have increased transcript abundance. In agreement with the expression profile, AtOM66 over‐expression plants show increased SA content, accelerated cell death rates and are more tolerant to the biotrophic pathogen Pseudomonas syringae, but more susceptible to the necrotrophic fungus Botrytis cinerea. In conclusion, our results demonstrate a role for AtOM66 in cell death and amplifying SA signalling.