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Mitochondrial Complex II Has a Key Role in Mitochondrial-Derived Reactive Oxygen Species Influence on Plant Stress Gene Regulation and Defense

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Mitochondrial Complex II Has a Key Role in Mitochondrial-Derived Reactive Oxygen Species Influence on Plant Stress Gene Regulation and Defense Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense Cynthia Gleasona,1, Shaobai Huangb,1, Louise F. Thatchera,c, Rhonda C. Foleya, Carol R. Andersona,2, Adam J. Carrolld, A. Harvey Millarb,3, and Karam B. Singha,e,3 aCommonwealth Scientific and Industrial Research Organisation (CSIRO) Plant Industry, Wembley, WA 6913, Australia; bAustralian Research Council (ARC) Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia; cQueensland Bioscience Precinct, CSIRO Plant Industry, St Lucia, QLD 4067, Australia; dARC Centre of Excellence in Plant Energy Biology, Australian National University, Canberra, ACT 2600, Australia; and eUniversity of Western Australia Institute of Agriculture, University of Western Australia, Crawley, WA 6009, Australia Edited* by Bob B. Buchanan, University of California, Berkeley, CA, and approved May 20, 2011 (received for review October 27, 2010) Mitochondria are both a source of ATP and a site of reactive oxygen information about the regulation of gene expression such as novel species (ROS) production. However, there is little information on the transcription factors or other upstream regulatory components sites of mitochondrial ROS (mROS) production or the biological role with roles in plant defense and/or stress responses. of such mROS in plants. We provide genetic proof that mitochon- To gain insights into conserved aspects of biotic, abiotic, and drial complex II (Complex II) of the electron transport chain contrib- chemical signaling pathways, we conducted a forward genetic utes to localized mROS that regulates plant stress and defense screen to identify mutants with changes in GSTF8 promoter ac- responses. We identify an Arabidopsis mutant in the Complex II tivity. In this work, we have characterized an Arabidopsis mutant subunit, SDH1-1, through a screen for mutants lacking GSTF8 gene that showed loss of inducible GSTF8 expression in response to expression in response to salicylic acid (SA). GSTF8 is an early stress- stresses and increased susceptibility to fungal and bacterial path- responsive gene whose transcription is induced by biotic and abiotic ogens. In mitochondrial complex II (Complex II), also known as stresses, and its expression is commonly used as a marker of early succinate dehydrogenase (SDH), we mapped the mutation to the stress and defense responses. Transcriptional analysis of this mu- catalytic subunit (SDH1-1), providing genetic proof that the PLANT BIOLOGY tant, disrupted in stress responses 1 (dsr1), showed that it had al- mitochondrial respiratory electron transport chain (10, 11) con- tered SA-mediated gene expression for specific downstream stress tributes to the propagation of plant stress and defense responses. and defense genes, and it exhibited increased susceptibility to spe- cific fungal and bacterial pathogens. The dsr1 mutant also show- Results ed significantly reduced succinate dehydrogenase activity. Using Identification of an Arabidopsis Mutant with Altered Stress Gene in vivo fluorescence assays, we demonstrated that root cell ROS Responsiveness. GSTF8 promoter activity can be monitored with production occurred primarily from mitochondria and was lower an Arabidopsis thaliana (Columbia-0) transgenic line (JC66) in in the mutant in response to SA. In addition, leaf ROS produc- which 791 bp of the GSTF8 promoter has been fused to a luciferase tion was lower in the mutant after avirulent bacterial infection. This (LUC) reporter (12, 13). Approximately 100,000 M2 seedlings mutation, in a conserved region of SDH1-1, is a unique plant mito- from ethyl methanesulfonate-mutagenized seeds of JC66 were chondrial mutant that exhibits phenotypes associated with lowered screened for altered SA induction of the GSTF8 promoter by mROS production. It provides critical insights into Complex II func- monitoring whole-plant luminescence 4 h after SA treatment. tion with implications for understanding Complex II’s role in mito- Strong promoter activity was observed primarily in the roots of WT chondrial diseases across eukaryotes. (JC66) plants in response to SA (Fig. 1A). We focused our at- tention to a loss-of-function mutant, which showed almost no SA- plant defense | respiration | Pseudomonas syringae | Rhizoctonia solani induced GSTF8 promoter activity, and called this mutant dis- rupted in stress responses 1 (dsr1). lants are barraged by biotic and abiotic stresses that can cause To further characterize the dsr1 mutation, the GSTF8::LUC Plarge annual losses to global food production, and, as a result, response to SA was monitored over a 14-h time course (Fig. 1A). plants have evolved mechanisms to quickly perceive and respond In WT, there was GSTF8 promoter activity after SA treatment, to these external stresses (1, 2). At the gene-expression level, peaking at 8–12 h after treatment. In contrast, the dsr1 mutant plant responses to many biotic and abiotic stresses share con- had significantly less promoter activity induced by SA (Fig. 1A). siderable overlap, particularly during the early stages of the re- sponse, and these responses are controlled by overlapping sets of signaling molecules that include plant hormones, calcium, nitric Author contributions: C.G., S.H., C.R.A., A.J.C., A.H.M., and K.B.S. designed research; C.G., oxide, and reactive oxygen species (ROS) (3–5). The interplay S.H., L.F.T., R.C.F., and C.R.A. performed research; K.B.S. contributed new reagents/ana- lytic tools; C.G., S.H., A.J.C., A.H.M., and K.B.S. analyzed data; and C.G., A.H.M., and K.B.S. between these signaling molecules and their respective down- wrote the paper. stream networks is complex and not fully understood. The authors declare no conflict of interest. One group of genes that are induced by combinations of stress *This Direct Submission article had a prearranged editor. signaling pathways are the glutathione S-transferases (GSTs). GSTs encode ubiquitous enzymes found in both animals and Freely available online through the PNAS open access option. Data deposition: The microarray data reported in this paper have been deposited in the plants that protect tissues against oxidative damage or from toxins Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. produced during xenobiotic metabolism (6). In plants, the tran- GSE22942). scriptional activation of diverse GSTs can be triggered by chem- 1C.G. and S.H. contributed equally to this work. icals [salicylic acid (SA)], auxinic herbicides (e.g., dicamba), and 2Deceased January 24, 2009. ROS (H2O2) as well as both biotic (fungal and bacterial elicitors) 3To whom correspondence may be addressed. E-mail: [email protected], or and abiotic stresses (6). A good example is GSTF8, which has [email protected]. – been used as a marker for early stress/defense gene induction (7 This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 9). Mutants with altered GSTF8 expression could provide critical 1073/pnas.1016060108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1016060108 PNAS Early Edition | 1of6 Downloaded by guest on October 1, 2021 might explain the mannitol-induced osmotic stress tolerance of A 60 WT SA 50 dsr1 (Fig. S2). dsr1 40 Interestingly, there were a greater number of genes specifically 30 20 repressed than induced in SA-induced dsr1 plants compared with 10 WT. When looking at repressed genes in SA-treated dsr1 plants, 140 120 D a large number of genes were involved in plant development and 100 80 biotic stress responses. Peroxidases, glutaredoxins, and trypsin 60 and protease inhibitor family genes comprised some of the biotic 40 20 stress-responsive genes that were significantly repressed in the mutant (Dataset S1, Table S1B). 70 H2O2 Average light units / units seedling light Average 50 In an alternative means of analysis, we considered the 100 most 30 SA-induced genes in WT whose fold induction ranged from 6.7 to 10 163 and looked at the transcriptional response of these genes in 0 2 4 6 8 10 12 14 dsr1 (Dataset S1, Table S1C). Although many responded similarly, Time (hr) a subset of 18 exhibited significantly lower or no induction in dsr1 B 140 (Fig. S3 and Dataset S1, Table S1C). This set of genes contained WT 120 dsr1 largely known SA-responsive genes from published reports, and 100 expression 80 more than half are normally induced in response to exposure of * 60 Arabidopsis to bacterial, fungal, or viral pathogens based on GSTF8 40 * analysis of Genevestigator datasets (Dataset S1, Table S1D). 20 0 Relative Relative mock SA D dsr1 Is More Susceptible to Fungal and Virulent Bacterial Pathogens. Fig. 1. dsr1 shows altered GSTF8 induction in response to certain stresses. Because the dsr1 plants have altered SA-regulated gene expres- (A) Average of the total bioluminescence generated by each seedling (n = sion and SA is an important plant defense signaling molecule, 20) per hour after treatment with SA, dicamba (D), or H2O2.(B) Relative these plants may have altered defense responses to pathogens. expression of GSTF8 in WT and dsr1 plants at 10 h after treatment with Therefore, we challenged dsr1 with different plant pathogens. water (mock), SA, or dicamba (D). Gene-expression experiments using three The necrotrophic root fungus Rhizoctonia solani, which causes biological and two technical repeats were repeated twice with similar bare patches and seedling dampening off, is divided into anas- ’ < results. [Error bars: standard error (SEM); Student s t test, *P 0.05.] tomosis groups (AG) based on the ability of the fungal strains to fuse (15). Previously, we found that WT (Columbia-0) plants are resistant to strain AG8 and susceptible to strain AG2 (16). In- Furthermore, the SA analog 2,6-dichloroisonicotinic acid and the terestingly, although GSTF8 was induced after inoculation with SA precursor benzoic acid also induced GSTF8 promoter activity the nonpathogenic strain AG8, its induction was absent after in- in WT plants to much higher levels than in the dsr1 mutant (Fig.
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