TY - JOUR

T1 - Retrograde signals from mitochondria reprogramme skoto-morphogenesis in Arabidopsis thaliana via alternative oxidase 1a

AU - Merendino, Livia

AU - Courtois, Florence

AU - Grübler, Björn

AU - Bastien, Olivier

AU - Straetmanns, Vera

AU - Chevalier, Fabien

AU - Lerbs-Mache, Silva

AU - Lurin, Claire

AU - Pfannschmidt, Thomas

N1 - Funding Information: Data accessibility. Microarray data are available at the Gene Expression Omnibus (GEO) under accession number GSE144694. Authors’ contributions. L.M. and T.P. designed research, L.M., F.Co., B.G., V.S. and F.Ch. performed experiments, O.B. performed statistical analyses, C.L. contributed analytical tools. L.M., F.Co., S.L.-M. and T.P. analysed data, L.M. and T.P. wrote the manuscript with the help of all co-authors. All authors read and approved the manuscript. Competing interests. The authors declare no conflict of interest. Funding. This work was supported by grants from the Deutsche For-schungsgemeinschaft (PF323-5-2 to T.P.) and the DFG research

PY - 2020/6/22

Y1 - 2020/6/22

N2 - The early steps in germination and development of angiosperm seedlings often occur in the dark, inducing a special developmental programme called skoto-morphogenesis. Under these conditions photosynthesis cannot work and all energetic requirements must be fulfilled by mitochondrial metabolization of storage energies. Here, we report the physiological impact of mitochondrial dysfunctions on the skoto-morphogenic programme by using the Arabidopsis rpoTmp mutant. This mutant is defective in the T7-phage-type organellar RNA polymerase shared by plastids and mitochondria. Lack of this enzyme causes a mitochondrial dysfunction resulting in a strongly reduced mitochondrial respiratory chain and a compensatory upregulation of the alternative-oxidase (AOX)-dependent respiration. Surprisingly, the mutant exhibits a triple-response-like phenotype with a twisted apical hook and a shortened hypocotyl. Highly similar phenotypes were detected in other respiration mutants (rug3 and atphb3) and in WT seedlings treated with the respiration inhibitor KCN. Further genetic and molecular data suggest that the observed skoto-morphogenic alterations are specifically dependent on the activity of the AOX1a enzyme. Microarray analyses indicated that a retrograde signal from mitochondria activates the ANAC017-dependent pathway which controls the activation of AOX1A transcription. In sum, our analysis identifies AOX as a functional link that couples the formation of a triple-response-like phenotype to mitochondrial dysfunction. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

AB - The early steps in germination and development of angiosperm seedlings often occur in the dark, inducing a special developmental programme called skoto-morphogenesis. Under these conditions photosynthesis cannot work and all energetic requirements must be fulfilled by mitochondrial metabolization of storage energies. Here, we report the physiological impact of mitochondrial dysfunctions on the skoto-morphogenic programme by using the Arabidopsis rpoTmp mutant. This mutant is defective in the T7-phage-type organellar RNA polymerase shared by plastids and mitochondria. Lack of this enzyme causes a mitochondrial dysfunction resulting in a strongly reduced mitochondrial respiratory chain and a compensatory upregulation of the alternative-oxidase (AOX)-dependent respiration. Surprisingly, the mutant exhibits a triple-response-like phenotype with a twisted apical hook and a shortened hypocotyl. Highly similar phenotypes were detected in other respiration mutants (rug3 and atphb3) and in WT seedlings treated with the respiration inhibitor KCN. Further genetic and molecular data suggest that the observed skoto-morphogenic alterations are specifically dependent on the activity of the AOX1a enzyme. Microarray analyses indicated that a retrograde signal from mitochondria activates the ANAC017-dependent pathway which controls the activation of AOX1A transcription. In sum, our analysis identifies AOX as a functional link that couples the formation of a triple-response-like phenotype to mitochondrial dysfunction. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

KW - Arabidopsis/genetics

KW - Arabidopsis Proteins/genetics

KW - Mitochondria/metabolism

KW - Mitochondrial Proteins/genetics

KW - Morphogenesis/genetics

KW - Oxidoreductases/genetics

KW - Plant Proteins/genetics

KW - Arabidopsis

KW - Retrograde signal

KW - Alternative oxidase

KW - Skoto-morphogenesis

KW - Organellar RPOTmp RNA polymerase

KW - Mitochondrial respiration

UR - http://www.scopus.com/inward/record.url?scp=85085144884&partnerID=8YFLogxK

U2 - 10.1098/rstb.2019.0567

DO - 10.1098/rstb.2019.0567

M3 - Article

C2 - 32362252

VL - 375

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0080-4622

IS - 1801

M1 - 20190567

ER -