Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense

Abstract

Mitochondria are both a source of ATP and a site of reactive oxygen species (ROS) production. However, there is little information on the sites of mitochondrial ROS (mROS) production or the biological role of such mROS in plants. We provide genetic proof that mitochondrial complex II (Complex II) of the electron transport chain contributes to localized mROS that regulates plant stress and defense responses. We identify an Arabidopsis mutant in the Complex II subunit, SDH1-1, through a screen for mutants lacking GSTF8 gene expression in response to salicylic acid (SA). GSTF8 is an early stressresponsive gene whose transcription is induced by biotic and abiotic stresses, and its expression is commonly used as a marker of early stress and defense responses. Transcriptional analysis of this mutant, disrupted in stress responses 1 (dsr1), showed that it had altered SA-mediated gene expression for specific downstream stress and defense genes, and it exhibited increased susceptibility to specific fungal and bacterial pathogens. The dsr1 mutant also showed significantly reduced succinate dehydrogenase activity. Using in vivo fluorescence assays, we demonstrated that root cell ROS production occurred primarily from mitochondria and was lower in the mutant in response to SA. In addition, leaf ROS production was lower in the mutant after avirulent bacterial infection. This mutation, in a conserved region of SDH1-1, is a unique plant mitochondrial mutant that exhibits phenotypes associated with lowered mROS production. It provides critical insights into Complex II function with implications for understanding Complex II's role in mitochondrial diseases across eukaryotes.plant defense | respiration | Pseudomonas syringae | Rhizoctonia solani

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

“…This limitation changed when a point mutation of SDH1-1 (dsr1) was identified that did not knockout SDH, but instead lowered SDH activity and decreased mitochondrial ROS production. It was first identified as a mutant that had lost salicylic acid (SA)-but not H 2 O 2 -dependent stress response using a GST GSTF8 promoter stress response assay (Gleason et al, 2011). The dsr1 mutant showed steadystate decrease expression of peroxidases, glutaredoxins, and trypsin and protease inhibitor family genes and reduced expression on SA induction of a set of SA-responsive genes normally induced in response to exposure of Arabidopsis to bacterial, fungal, or viral pathogens (Gleason et al, 2011).…”

“…It was first identified as a mutant that had lost salicylic acid (SA)-but not H 2 O 2 -dependent stress response using a GST GSTF8 promoter stress response assay (Gleason et al, 2011). The dsr1 mutant showed steadystate decrease expression of peroxidases, glutaredoxins, and trypsin and protease inhibitor family genes and reduced expression on SA induction of a set of SA-responsive genes normally induced in response to exposure of Arabidopsis to bacterial, fungal, or viral pathogens (Gleason et al, 2011). The dsr1 mutant also had higher susceptibility to fungal and bacterial pathogens, indicating that mitochondrial SDH is involved in response to biotic stress in vivo in plants.…”

“…The dsr1 mutant also had higher susceptibility to fungal and bacterial pathogens, indicating that mitochondrial SDH is involved in response to biotic stress in vivo in plants. However, despite this evidence for the involvement of a mutated SDH1 and recovery of signaling when wild-type SDH1 was overexpressed (Gleason et al, 2011), it was still unclear how a mutation in SDH such as dsr1 could affect mitochondrial ROS production and the downstream stress response induced by SA.…”

Modulation of Protein Phosphorylation, N-Glycosylation and Lys-Acetylation in Grape (Vitis vinifera) Mesocarp and Exocarp Owing to Lobesia botrana Infection

“…These studies demonstrate the importance of the complex modulation of plant metabolism and defense responses during pathogen infection. These changes activate a series of biological signaling mechanisms such as Ca 2ϩ influx (8,9), kinase cascades (10,11), reactive oxygen species (12,13), and phytohormone signaling pathways (14). However, so far none of these studies has addressed quantitative changes of grapevine protein post-translational modifications (PTMs) 1 upon pathogen infection, which we believe would provide novel insights into the underlying molecular processes that may eventually yield novel strategies for pathogen control in the field.…”

Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity

“…Mitochondria are among the multiple organelles that contribute to ROS production. Mutants defective in mitochondrial ROS (mROS) generation exhibit enhanced disease susceptibility to specific fungal and bacterial pathogens 34 . All these studies point to a positive regulatory role of mitochondria during immune responses through ROS generation.…”