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

Botao Zhang, Olivier Van Aken, L. Thatcher, I. De Clercq, Owen Duncan, Simon Law, Monika Murcha, Marna Van Der Merwe, H.S. Seifi, Christopher Carrie, C. Cazzonelli, Jordan Radomiljac, M. Hofte, Karam Singhe, F. Van Breusegem, James Whelan

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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 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.
LanguageEnglish
Pages709-727
Number of pages19
JournalThe Plant Journal
Volume80
Issue number4
DOIs
StatePublished - 27 Oct 2014

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Mitochondrial Membranes
Arabidopsis
Salicylic Acid
adenosinetriphosphatase
Adenosine Triphosphatases
cell death
Cell Death
Arabidopsis thaliana
Mitochondrial Proteins
salicylic acid
pathogens
Proteins
proteins
Genes
Pseudomonas syringae
Botrytis
Electron Transport Complex III
Genetically Modified Plants
Droughts
leaf curling

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Zhang, B., Van Aken, O., Thatcher, L., De Clercq, I., Duncan, O., Law, S., ... Whelan, J. (2014). The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. The Plant Journal, 80(4), 709-727. DOI: 10.1111/tpj.12665
Zhang, Botao ; Van Aken, Olivier ; Thatcher, L. ; De Clercq, I. ; Duncan, Owen ; Law, Simon ; Murcha, Monika ; Van Der Merwe, Marna ; Seifi, H.S. ; Carrie, Christopher ; Cazzonelli, C. ; Radomiljac, Jordan ; Hofte, M. ; Singhe, Karam ; Van Breusegem, F. ; Whelan, James. / The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. In: The Plant Journal. 2014 ; Vol. 80, No. 4. pp. 709-727
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author = "Botao Zhang and {Van Aken}, Olivier and L. Thatcher and {De Clercq}, I. and Owen Duncan and Simon Law and Monika Murcha and {Van Der Merwe}, Marna and H.S. Seifi and Christopher Carrie and C. Cazzonelli and Jordan Radomiljac and M. Hofte and Karam Singhe and {Van Breusegem}, F. and James Whelan",
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Zhang, B, Van Aken, O, Thatcher, L, De Clercq, I, Duncan, O, Law, S, Murcha, M, Van Der Merwe, M, Seifi, HS, Carrie, C, Cazzonelli, C, Radomiljac, J, Hofte, M, Singhe, K, Van Breusegem, F & Whelan, J 2014, 'The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana' The Plant Journal, vol 80, no. 4, pp. 709-727. DOI: 10.1111/tpj.12665

The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. / Zhang, Botao; Van Aken, Olivier; Thatcher, L.; De Clercq, I.; Duncan, Owen; Law, Simon; Murcha, Monika; Van Der Merwe, Marna; Seifi, H.S.; Carrie, Christopher; Cazzonelli, C.; Radomiljac, Jordan; Hofte, M.; Singhe, Karam; Van Breusegem, F.; Whelan, James.

In: The Plant Journal, Vol. 80, No. 4, 27.10.2014, p. 709-727.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana

AU - Zhang,Botao

AU - Van Aken,Olivier

AU - Thatcher,L.

AU - De Clercq,I.

AU - Duncan,Owen

AU - Law,Simon

AU - Murcha,Monika

AU - Van Der Merwe,Marna

AU - Seifi,H.S.

AU - Carrie,Christopher

AU - Cazzonelli,C.

AU - Radomiljac,Jordan

AU - Hofte,M.

AU - Singhe,Karam

AU - Van Breusegem,F.

AU - Whelan,James

PY - 2014/10/27

Y1 - 2014/10/27

N2 - 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.

AB - 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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DO - 10.1111/tpj.12665

M3 - Article

VL - 80

SP - 709

EP - 727

JO - PLANT JOURNAL

T2 - PLANT JOURNAL

JF - PLANT JOURNAL

SN - 0960-7412

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Zhang B, Van Aken O, Thatcher L, De Clercq I, Duncan O, Law S et al. The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. The Plant Journal. 2014 Oct 27;80(4):709-727. Available from, DOI: 10.1111/tpj.12665