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Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis

Ho, Lois H M; Giraud, Estelle; Uggalla, Vindya; Lister, Ryan; Clifton, Rachel; Glen, Angela; Thirkettle-Watts, Dave; Van Aken, Olivier LU and Whelan, James (2008) In Plant Physiology 147(4). p.73-1858
Abstract

In this study we analyzed transcript abundance and promoters of genes encoding mitochondrial proteins to identify signaling pathways that regulate stress-induced gene expression. We used Arabidopsis (Arabidopsis thaliana) alternative oxidase AOX1a, external NADP H-dehydrogenase NDB2, and two additional highly stress-responsive genes, At2g21640 and BCS1. As a starting point, the promoter region of AOX1a was analyzed and functional analysis identified 10 cis-acting regulatory elements (CAREs), which played a role in response to treatment with H(2)O(2), rotenone, or both. Six of these elements were also functional in the NDB2 promoter. The promoter region of At2g21640, previously defined as a hallmark of oxidative stress, shared two... (More)

In this study we analyzed transcript abundance and promoters of genes encoding mitochondrial proteins to identify signaling pathways that regulate stress-induced gene expression. We used Arabidopsis (Arabidopsis thaliana) alternative oxidase AOX1a, external NADP H-dehydrogenase NDB2, and two additional highly stress-responsive genes, At2g21640 and BCS1. As a starting point, the promoter region of AOX1a was analyzed and functional analysis identified 10 cis-acting regulatory elements (CAREs), which played a role in response to treatment with H(2)O(2), rotenone, or both. Six of these elements were also functional in the NDB2 promoter. The promoter region of At2g21640, previously defined as a hallmark of oxidative stress, shared two functional CAREs with AOX1a and was responsive to treatment with H(2)O(2) but not rotenone. Microarray analysis further supported that signaling pathways induced by H(2)O(2) and rotenone are not identical. The promoter of BCS1 was not responsive to H(2)O(2) or rotenone, but highly responsive to salicylic acid (SA), whereas the promoters of AOX1a and NDB2 were unresponsive to SA. Analysis of transcript abundance of these genes in a variety of defense signaling mutants confirmed that BCS1 expression is regulated in a different manner compared to AOX1a, NDB2, and At2g21640. These mutants also revealed a pathway associated with programmed cell death that regulated AOX1a in a manner distinct from the other genes. Thus, at least three distinctive pathways regulate mitochondrial stress response at a transcriptional level, an SA-dependent pathway represented by BCS1, a second pathway that represents a convergence point for signals generated by H(2)O(2) and rotenone on multiple CAREs, some of which are shared between responsive genes, and a third pathway that acts via EDS1 and PAD4 regulating only AOX1a. Furthermore, posttranscriptional regulation accounts for changes in transcript abundance by SA treatment for some genes.

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published
subject
keywords
Arabidopsis, Arabidopsis Proteins, Cells, Cultured, Gene Expression Regulation, Plant, Hydrogen Peroxide, Mitochondrial Proteins, Oligonucleotide Array Sequence Analysis, Oxidoreductases, Plant Proteins, Promoter Regions, Genetic, RNA, Messenger, Rotenone, Signal Transduction, Uncoupling Agents
in
Plant Physiology
volume
147
issue
4
pages
16 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:51449101034
ISSN
0032-0889
DOI
10.1104/pp.108.121384
language
English
LU publication?
no
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01ab4596-a8d2-4ea2-8ac4-f9435abcad57
date added to LUP
2017-05-09 10:10:02
date last changed
2017-09-03 05:22:00
@article{01ab4596-a8d2-4ea2-8ac4-f9435abcad57,
  abstract     = {<p>In this study we analyzed transcript abundance and promoters of genes encoding mitochondrial proteins to identify signaling pathways that regulate stress-induced gene expression. We used Arabidopsis (Arabidopsis thaliana) alternative oxidase AOX1a, external NADP H-dehydrogenase NDB2, and two additional highly stress-responsive genes, At2g21640 and BCS1. As a starting point, the promoter region of AOX1a was analyzed and functional analysis identified 10 cis-acting regulatory elements (CAREs), which played a role in response to treatment with H(2)O(2), rotenone, or both. Six of these elements were also functional in the NDB2 promoter. The promoter region of At2g21640, previously defined as a hallmark of oxidative stress, shared two functional CAREs with AOX1a and was responsive to treatment with H(2)O(2) but not rotenone. Microarray analysis further supported that signaling pathways induced by H(2)O(2) and rotenone are not identical. The promoter of BCS1 was not responsive to H(2)O(2) or rotenone, but highly responsive to salicylic acid (SA), whereas the promoters of AOX1a and NDB2 were unresponsive to SA. Analysis of transcript abundance of these genes in a variety of defense signaling mutants confirmed that BCS1 expression is regulated in a different manner compared to AOX1a, NDB2, and At2g21640. These mutants also revealed a pathway associated with programmed cell death that regulated AOX1a in a manner distinct from the other genes. Thus, at least three distinctive pathways regulate mitochondrial stress response at a transcriptional level, an SA-dependent pathway represented by BCS1, a second pathway that represents a convergence point for signals generated by H(2)O(2) and rotenone on multiple CAREs, some of which are shared between responsive genes, and a third pathway that acts via EDS1 and PAD4 regulating only AOX1a. Furthermore, posttranscriptional regulation accounts for changes in transcript abundance by SA treatment for some genes.</p>},
  author       = {Ho, Lois H M and Giraud, Estelle and Uggalla, Vindya and Lister, Ryan and Clifton, Rachel and Glen, Angela and Thirkettle-Watts, Dave and Van Aken, Olivier and Whelan, James},
  issn         = {0032-0889},
  keyword      = {Arabidopsis,Arabidopsis Proteins,Cells, Cultured,Gene Expression Regulation, Plant,Hydrogen Peroxide,Mitochondrial Proteins,Oligonucleotide Array Sequence Analysis,Oxidoreductases,Plant Proteins,Promoter Regions, Genetic,RNA, Messenger,Rotenone,Signal Transduction,Uncoupling Agents},
  language     = {eng},
  number       = {4},
  pages        = {73--1858},
  publisher    = {American Society of Plant Biologists},
  series       = {Plant Physiology},
  title        = {Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis},
  url          = {http://dx.doi.org/10.1104/pp.108.121384},
  volume       = {147},
  year         = {2008},
}