The transcription factor MYB29 is a regulator of alternative oxidase1a

Xinhua Zhang; Aneta Ivanova; Klaas Vandepoele; Jordan Radomiljac; Jan Van De Velde; Oliver Berkowitz; Patrick Willems; Yue Xu; Sophia Ng; Olivier Van Aken; Owen Duncan; Botao Zhang; Veronique Storme; Kai Xun Chan; Dries Vaneechoutte; Barry James Pogson; Frank Van Breusegem; James Whelan; Inge De Clercq

doi:10.1104/pp.16.01494

The transcription factor MYB29 is a regulator of alternative oxidase1a

Xinhua Zhang, Aneta Ivanova, Klaas Vandepoele, Jordan Radomiljac, Jan Van De Velde, Oliver Berkowitz, Patrick Willems, Yue Xu, Sophia Ng, Olivier Van Aken, Owen Duncan, Botao Zhang, Veronique Storme, Kai Xun Chan, Dries Vaneechoutte, Barry James Pogson, Frank Van Breusegem, James Whelan, Inge De Clercq^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

45 Citations (Scopus)

Abstract

Plants sense and integrate a variety of signals from the environment through different interacting signal transduction pathways that involve hormones and signaling molecules. Using ALTERNATIVE OXIDASE1a (AOX1a) gene expression as a model system of retrograde or stress signaling between mitochondria and the nucleus, MYB DOMAIN PROTEIN29 (MYB29) was identified as a negative regulator (regulator of alternative oxidase1a 7 [rao7] mutant) in a genetic screen of Arabidopsis (Arabidopsis thaliana). rao7/ myb29 mutants have increased levels of AOX1a transcript and protein compared to wild type after induction with antimycin A. A variety of genes previously associated with the mitochondrial stress response also display enhanced transcript abundance, indicating that RAO7/MYB29 negatively regulates mitochondrial stress responses in general. Meta-analysis of hormoneresponsive marker genes and identification of downstream transcription factor networks revealed that MYB29 functions in the complex interplay of ethylene, jasmonic acid, salicylic acid, and reactive oxygen species signaling by regulating the expression of various ETHYLENE RESPONSE FACTOR and WRKY transcription factors. Despite an enhanced induction of mitochondrial stress response genes, rao7/myb29 mutants displayed an increased sensitivity to combined moderate light and drought stress. These results uncover interactions between mitochondrial retrograde signaling and the regulation of glucosinolate biosynthesis, both regulated by RAO7/MYB29. This common regulator can explain why perturbation of the mitochondrial function leads to transcriptomic responses overlapping with responses to biotic stress.

Original language	English
Pages (from-to)	1825-1843
Number of pages	19
Journal	Plant Physiology
Volume	173
Issue number	3
DOIs	https://doi.org/10.1104/pp.16.01494
Publication status	Published - Mar 2017

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Zhang, X., Ivanova, A., Vandepoele, K., Radomiljac, J., Van De Velde, J., Berkowitz, O., Willems, P., Xu, Y., Ng, S., Van Aken, O., Duncan, O., Zhang, B., Storme, V., Chan, K. X., Vaneechoutte, D., Pogson, B. J., Van Breusegem, F., Whelan, J., & De Clercq, I. (2017). The transcription factor MYB29 is a regulator of alternative oxidase1a. Plant Physiology, 173(3), 1825-1843. https://doi.org/10.1104/pp.16.01494

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title = "The transcription factor MYB29 is a regulator of alternative oxidase1a",

abstract = "Plants sense and integrate a variety of signals from the environment through different interacting signal transduction pathways that involve hormones and signaling molecules. Using ALTERNATIVE OXIDASE1a (AOX1a) gene expression as a model system of retrograde or stress signaling between mitochondria and the nucleus, MYB DOMAIN PROTEIN29 (MYB29) was identified as a negative regulator (regulator of alternative oxidase1a 7 [rao7] mutant) in a genetic screen of Arabidopsis (Arabidopsis thaliana). rao7/ myb29 mutants have increased levels of AOX1a transcript and protein compared to wild type after induction with antimycin A. A variety of genes previously associated with the mitochondrial stress response also display enhanced transcript abundance, indicating that RAO7/MYB29 negatively regulates mitochondrial stress responses in general. Meta-analysis of hormoneresponsive marker genes and identification of downstream transcription factor networks revealed that MYB29 functions in the complex interplay of ethylene, jasmonic acid, salicylic acid, and reactive oxygen species signaling by regulating the expression of various ETHYLENE RESPONSE FACTOR and WRKY transcription factors. Despite an enhanced induction of mitochondrial stress response genes, rao7/myb29 mutants displayed an increased sensitivity to combined moderate light and drought stress. These results uncover interactions between mitochondrial retrograde signaling and the regulation of glucosinolate biosynthesis, both regulated by RAO7/MYB29. This common regulator can explain why perturbation of the mitochondrial function leads to transcriptomic responses overlapping with responses to biotic stress.",

author = "Xinhua Zhang and Aneta Ivanova and Klaas Vandepoele and Jordan Radomiljac and {Van De Velde}, Jan and Oliver Berkowitz and Patrick Willems and Yue Xu and Sophia Ng and {Van Aken}, Olivier and Owen Duncan and Botao Zhang and Veronique Storme and Chan, {Kai Xun} and Dries Vaneechoutte and Pogson, {Barry James} and {Van Breusegem}, Frank and James Whelan and {De Clercq}, Inge",

year = "2017",

month = mar,

doi = "10.1104/pp.16.01494",

language = "English",

volume = "173",

pages = "1825--1843",

journal = "Plant Physiology",

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publisher = "American Society of Plant Biologists",

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Zhang, X, Ivanova, A, Vandepoele, K, Radomiljac, J, Van De Velde, J, Berkowitz, O, Willems, P, Xu, Y, Ng, S, Van Aken, O, Duncan, O, Zhang, B, Storme, V, Chan, KX, Vaneechoutte, D, Pogson, BJ, Van Breusegem, F, Whelan, J & De Clercq, I 2017, 'The transcription factor MYB29 is a regulator of alternative oxidase1a', Plant Physiology, vol. 173, no. 3, pp. 1825-1843. https://doi.org/10.1104/pp.16.01494

TY - JOUR

T1 - The transcription factor MYB29 is a regulator of alternative oxidase1a

AU - Zhang, Xinhua

AU - Ivanova, Aneta

AU - Vandepoele, Klaas

AU - Radomiljac, Jordan

AU - Van De Velde, Jan

AU - Berkowitz, Oliver

AU - Willems, Patrick

AU - Xu, Yue

AU - Ng, Sophia

AU - Van Aken, Olivier

AU - Duncan, Owen

AU - Zhang, Botao

AU - Storme, Veronique

AU - Chan, Kai Xun

AU - Vaneechoutte, Dries

AU - Pogson, Barry James

AU - Van Breusegem, Frank

AU - Whelan, James

AU - De Clercq, Inge

PY - 2017/3

Y1 - 2017/3

N2 - Plants sense and integrate a variety of signals from the environment through different interacting signal transduction pathways that involve hormones and signaling molecules. Using ALTERNATIVE OXIDASE1a (AOX1a) gene expression as a model system of retrograde or stress signaling between mitochondria and the nucleus, MYB DOMAIN PROTEIN29 (MYB29) was identified as a negative regulator (regulator of alternative oxidase1a 7 [rao7] mutant) in a genetic screen of Arabidopsis (Arabidopsis thaliana). rao7/ myb29 mutants have increased levels of AOX1a transcript and protein compared to wild type after induction with antimycin A. A variety of genes previously associated with the mitochondrial stress response also display enhanced transcript abundance, indicating that RAO7/MYB29 negatively regulates mitochondrial stress responses in general. Meta-analysis of hormoneresponsive marker genes and identification of downstream transcription factor networks revealed that MYB29 functions in the complex interplay of ethylene, jasmonic acid, salicylic acid, and reactive oxygen species signaling by regulating the expression of various ETHYLENE RESPONSE FACTOR and WRKY transcription factors. Despite an enhanced induction of mitochondrial stress response genes, rao7/myb29 mutants displayed an increased sensitivity to combined moderate light and drought stress. These results uncover interactions between mitochondrial retrograde signaling and the regulation of glucosinolate biosynthesis, both regulated by RAO7/MYB29. This common regulator can explain why perturbation of the mitochondrial function leads to transcriptomic responses overlapping with responses to biotic stress.

AB - Plants sense and integrate a variety of signals from the environment through different interacting signal transduction pathways that involve hormones and signaling molecules. Using ALTERNATIVE OXIDASE1a (AOX1a) gene expression as a model system of retrograde or stress signaling between mitochondria and the nucleus, MYB DOMAIN PROTEIN29 (MYB29) was identified as a negative regulator (regulator of alternative oxidase1a 7 [rao7] mutant) in a genetic screen of Arabidopsis (Arabidopsis thaliana). rao7/ myb29 mutants have increased levels of AOX1a transcript and protein compared to wild type after induction with antimycin A. A variety of genes previously associated with the mitochondrial stress response also display enhanced transcript abundance, indicating that RAO7/MYB29 negatively regulates mitochondrial stress responses in general. Meta-analysis of hormoneresponsive marker genes and identification of downstream transcription factor networks revealed that MYB29 functions in the complex interplay of ethylene, jasmonic acid, salicylic acid, and reactive oxygen species signaling by regulating the expression of various ETHYLENE RESPONSE FACTOR and WRKY transcription factors. Despite an enhanced induction of mitochondrial stress response genes, rao7/myb29 mutants displayed an increased sensitivity to combined moderate light and drought stress. These results uncover interactions between mitochondrial retrograde signaling and the regulation of glucosinolate biosynthesis, both regulated by RAO7/MYB29. This common regulator can explain why perturbation of the mitochondrial function leads to transcriptomic responses overlapping with responses to biotic stress.

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U2 - 10.1104/pp.16.01494

DO - 10.1104/pp.16.01494

M3 - Article

SN - 0032-0889

VL - 173

SP - 1825

EP - 1843

JO - Plant Physiology

JF - Plant Physiology

IS - 3

ER -

The transcription factor MYB29 is a regulator of alternative oxidase1a

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