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

Zhang, Botao; Van Aken, Olivier LU ; Thatcher, Louise F.; De Clercq, Inge; Duncan, Owen; Law, Simon R; Murcha, Monika W; van der Merwe, Margaretha; Seifi, Hamed Soren and Carrie, Chris, et al. (2014) In Plant Journal 80(4). p.27-709
Abstract

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... (More)

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.

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@article{634aa8c6-29ab-4b30-a88c-bdfbe046bfe0,
  abstract     = {<p>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.</p>},
  author       = {Zhang, Botao and Van Aken, Olivier and Thatcher, Louise F. and De Clercq, Inge and Duncan, Owen and Law, Simon R and Murcha, Monika W and van der Merwe, Margaretha and Seifi, Hamed Soren and Carrie, Chris and Cazzonelli, Christopher and Radomiljac, Jordan and Höfte, Monica and Singh, Karam B. and Van Breusegem, Frank and Whelan, James},
  issn         = {1365-313X},
  keyword      = {Arabidopsis,Arabidopsis Proteins,Botrytis,Cell Death,Cyclopentanes,Droughts,Gene Expression Regulation, Plant,Host-Pathogen Interactions,Mitochondrial Membranes,Mitochondrial Proteins,Multiprotein Complexes,Mutation,Oxylipins,Phenotype,Plant Diseases,Plant Leaves,Plants, Genetically Modified,Pseudomonas syringae,Salicylic Acid,Stress, Physiological},
  language     = {eng},
  number       = {4},
  pages        = {27--709},
  publisher    = {Wiley-Blackwell},
  series       = {Plant Journal},
  title        = {The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana},
  url          = {http://dx.doi.org/10.1111/tpj.12665},
  volume       = {80},
  year         = {2014},
}