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Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance

Van Aken, Olivier LU ; Ford, Ethan; Lister, Ryan; Huang, Shaobai and Millar, A. Harvey (2016) In Plant Journal 88(4). p.542-558
Abstract

Mitochondria are crucial for plant viability and are able to communicate information on their functional status to the cellular nucleus via retrograde signalling, thereby affecting gene expression. It is currently unclear if retrograde signalling in response to constitutive mitochondrial biogenesis defects is mediated by the same pathways as those triggered during acute mitochondrial dysfunction. Furthermore, it is unknown if retrograde signalling can effectively improve plant performance when mitochondrial function is constitutively impaired. Here we show that retrograde signalling in mutants defective in mitochondrial proteins RNA polymerase rpotmp or prohibitin atphb3 can be suppressed by knocking out the transcription factor... (More)

Mitochondria are crucial for plant viability and are able to communicate information on their functional status to the cellular nucleus via retrograde signalling, thereby affecting gene expression. It is currently unclear if retrograde signalling in response to constitutive mitochondrial biogenesis defects is mediated by the same pathways as those triggered during acute mitochondrial dysfunction. Furthermore, it is unknown if retrograde signalling can effectively improve plant performance when mitochondrial function is constitutively impaired. Here we show that retrograde signalling in mutants defective in mitochondrial proteins RNA polymerase rpotmp or prohibitin atphb3 can be suppressed by knocking out the transcription factor ANAC017. Genome-wide RNA-seq expression analysis revealed that ANAC017 is almost solely responsible for the most dramatic transcriptional changes common to rpotmp and atphb3 mutants, regulating classical marker genes such as alternative oxidase 1a (AOX1a) and also previously-uncharacterised DUF295 genes that appear to be new retrograde markers. In contrast, ANAC017 does not regulate intra-mitochondrial gene expression or transcriptional changes unique to either rpotmp or atphb3 genotype, suggesting the existence of currently unknown signalling cascades. The data show that ANAC017 function extends beyond common retrograde transcriptional responses and affects downstream protein abundance and enzyme activity of alternative oxidase, as well as steady-state energy metabolism in atphb3 plants. Furthermore, detailed growth analysis revealed that ANAC017-dependent retrograde signalling provides benefits for growth and productivity in plants with mitochondrial defects. In conclusion, ANAC017 plays a key role in both biogenic and operational mitochondrial retrograde signalling, and improves plant performance when mitochondrial function is constitutively impaired.

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author
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Arabidopsis thaliana, Mitochondria, retrograde signalling, stress signalling
in
Plant Journal
volume
88
issue
4
pages
17 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:84995687611
ISSN
1365-313X
DOI
10.1111/tpj.13276
language
English
LU publication?
no
id
7866e19c-595f-4851-b843-7bebceac36fc
date added to LUP
2017-05-08 10:42:56
date last changed
2017-07-09 05:00:43
@article{7866e19c-595f-4851-b843-7bebceac36fc,
  abstract     = {<p>Mitochondria are crucial for plant viability and are able to communicate information on their functional status to the cellular nucleus via retrograde signalling, thereby affecting gene expression. It is currently unclear if retrograde signalling in response to constitutive mitochondrial biogenesis defects is mediated by the same pathways as those triggered during acute mitochondrial dysfunction. Furthermore, it is unknown if retrograde signalling can effectively improve plant performance when mitochondrial function is constitutively impaired. Here we show that retrograde signalling in mutants defective in mitochondrial proteins RNA polymerase rpotmp or prohibitin atphb3 can be suppressed by knocking out the transcription factor ANAC017. Genome-wide RNA-seq expression analysis revealed that ANAC017 is almost solely responsible for the most dramatic transcriptional changes common to rpotmp and atphb3 mutants, regulating classical marker genes such as alternative oxidase 1a (AOX1a) and also previously-uncharacterised DUF295 genes that appear to be new retrograde markers. In contrast, ANAC017 does not regulate intra-mitochondrial gene expression or transcriptional changes unique to either rpotmp or atphb3 genotype, suggesting the existence of currently unknown signalling cascades. The data show that ANAC017 function extends beyond common retrograde transcriptional responses and affects downstream protein abundance and enzyme activity of alternative oxidase, as well as steady-state energy metabolism in atphb3 plants. Furthermore, detailed growth analysis revealed that ANAC017-dependent retrograde signalling provides benefits for growth and productivity in plants with mitochondrial defects. In conclusion, ANAC017 plays a key role in both biogenic and operational mitochondrial retrograde signalling, and improves plant performance when mitochondrial function is constitutively impaired.</p>},
  author       = {Van Aken, Olivier and Ford, Ethan and Lister, Ryan and Huang, Shaobai and Millar, A. Harvey},
  issn         = {1365-313X},
  keyword      = {Arabidopsis thaliana,Mitochondria,retrograde signalling,stress signalling},
  language     = {eng},
  number       = {4},
  pages        = {542--558},
  publisher    = {Wiley-Blackwell},
  series       = {Plant Journal},
  title        = {Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance},
  url          = {http://dx.doi.org/10.1111/tpj.13276},
  volume       = {88},
  year         = {2016},
}