Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

Belt, Katharina; Huang, Shaobai; Thatcher, Louise F.; Casarotto, Hayley J.; Singh, Karam B.; Aken, Olivier Van; Millar, A. Harvey

doi:10.1104/pp.16.00060

Cited by 94 publications

(68 citation statements)

References 64 publications

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Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

“…Analysis of the Arabidopsis SDH1 mutants dsr1 and sdhaf2 showed that SDH is involved in a ROS‐induced stress signaling pathway that is likely to be triggered by salicylic acid (SA) (Gleason et al ., ; Belt et al ., ). This stress signaling pathway could be partially rescued in sdhaf2 , but not in dsr1 , by supplementing plant growth media with succinate (Belt et al ., ). Kinetic characterization showed that low concentrations (10–50 μM) of either SA or UQ binding site inhibitors (TTFA or carboxin) increased SDH activity and induced mitochondrial H 2 O 2 production (Belt et al ., ).…”

Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

“…This stress signaling pathway could be partially rescued in sdhaf2 , but not in dsr1 , by supplementing plant growth media with succinate (Belt et al ., ). Kinetic characterization showed that low concentrations (10–50 μM) of either SA or UQ binding site inhibitors (TTFA or carboxin) increased SDH activity and induced mitochondrial H 2 O 2 production (Belt et al ., ). The effect of stimulation of SDH activity by low SA concentrations acting at the UQ binding site (potentially at Qp site with high affinity to TTFA) could lead to reactions between electron and oxygen to form ROS.…”

Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

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Mitochondrial complex II of plants: subunit composition, assembly, and function in respiration and signaling

et al. 2019

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Complex II [succinate dehydrogenase (succinate-ubiquinone oxidoreductase); EC 1.3.5.1; SDH] is the only enzyme shared by both the electron transport chain and the tricarboxylic acid (TCA) cycle in mitochondria. Complex II in plants is considered unusual because of its accessory subunits (SDH5-SDH8), in addition to the catalytic subunits of SDH found in all eukaryotes (SDH1-SDH4). Here, we review compositional and phylogenetic analysis and biochemical dissection studies to both clarify the presence and propose a role for these subunits. We also consider the wider functional and phylogenetic evidence for SDH assembly factors and the reports from plants on the control of SDH1 flavination and SDH1-SDH2 interaction. Plant complex II has been shown to influence stomatal opening, the plant defense response and reactive oxygen speciesdependent stress responses. Signaling molecules such as salicyclic acid (SA) and nitric oxide (NO) are also reported to interact with the ubiquinone (UQ) binding site of SDH, influencing signaling transduction in plants. Future directions for SDH research in plants and the specific roles of its different subunits and assembly factors are suggested, including the potential for reverse electron transport to explain the succinate-dependent production of reactive oxygen species in plants and new avenues to explore the evolution of plant mitochondrial complex II and its utility.

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Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

Section: Complex II Production Of and Response To Signaling Moleculmentioning

confidence: 97%

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Mitochondrial complex II of plants: subunit composition, assembly, and function in respiration and signaling

et al. 2019

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“…Mechanistically, at low levels, salicylic acid has been observed to uncouple respiration, activate succinate dehydrogenase in isolated mitochondria, and up-regulate alternative oxidase expression (Norman et al, 2004;Belt et al, 2017). Salicylic acid has long been known to be involved in controlling thermogenic respiration in Arum spp.…”

Section: R N Supports Biosynthesismentioning

confidence: 99%

Variation in Leaf Respiration Rates at Night Correlates with Carbohydrate and Amino Acid Supply

et al. 2017

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Plant respiration can theoretically be fueled by and dependent upon an array of central metabolism components; however, which ones are responsible for the quantitative variation found in respiratory rates is unknown. Here, large-scale screens revealed 2-fold variation in nighttime leaf respiration rate (R N ) among mature leaves from an Arabidopsis (Arabidopsis thaliana) natural accession collection grown under common favorable conditions. R N variation was mostly maintained in the absence of genetic variation, which emphasized the low heritability of R N and its plasticity toward relatively small environmental differences within the sampling regime. To pursue metabolic explanations for leaf R N variation, parallel metabolite level profiling and assays of total protein and starch were performed. Within an accession, R N correlated strongly with stored carbon substrates, including starch and dicarboxylic acids, as well as sucrose, major amino acids, shikimate, and salicylic acid. Among different accessions, metabolite-R N correlations were maintained with protein, sucrose, and major amino acids but not stored carbon substrates. A complementary screen of the effect of exogenous metabolites and effectors on leaf R N revealed that (1) R N is stimulated by the uncoupler FCCP and high levels of substrates, demonstrating that both adenylate turnover and substrate supply can limit leaf R N , and (2) inorganic nitrogen did not stimulate R N , consistent with limited nighttime nitrogen assimilation. Simultaneous measurements of R N and protein synthesis revealed that these processes were largely uncorrelated in mature leaves. These results indicate that differences in preceding daytime metabolic activities are the major source of variation in mature leaf R N under favorable controlled conditions. Few plant metabolic fluxes are readily accessible to routine measurement. The major exceptions to this are fluxes involving gas exchange, such as respiration and photosynthesis. Measurements of respiratory gas exchange (i.e. mitochondrial oxygen uptake or CO 2 release in the absence of photorespiration) are useful from a metabolic perspective because they can be interpreted in terms of the underlying carbon fluxes and the generation of ATP by oxidative phosphorylation (Sweetlove et al., 2013). The biochemical reactions of respiration that produce CO 2 and lead to oxygen consumption are well understood (Plaxton and Podestá, 2006;Sweetlove et al., 2010;Millar et al., 2011;Tcherkez et al., 2012). The stoichiometries of the reactions and the connections between them are known, which provides us with a metabolic map of respiration that includes glycolysis, the oxidative pentose phosphate pathway, the citric acid cycle, the mitochondrial electron transport chain (mETC), ATP synthase, and several other surrounding reactions. In plants, carbohydrates are the dominant respiratory substrates, whereas lipids are rarely respired (Plaxton and Podestá, 2006). Carbohydrate oxidation proceeds via organic acids, which serve many purposes in plant...

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“…ascorbate, glutathione), an ion (e.g. Ca 2+ ) or a peptide oxidation product (Møller and Sweetlove , Foyer and Noctor , Huang et al , Kmiecik et al , Mignolet‐Spruyt et al , Noctor and Foyer , Petriacq et al , Belt et al , de Souza et al , Karpinska et al , Wagner et al ). In general, these potential signals relate to the mitochondrion's central role in energy metabolism, and hence could act as effective indicator(s) of mitochondrial status.…”

Section: Introductionmentioning

confidence: 99%

Signaling interactions between mitochondria and chloroplasts in Nicotiana tabacum leaf

Alber

Vanlerberghe

2019

Physiologia Plantarum

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Research has begun to elucidate the signal transduction pathway(s) that control cellular responses to changes in mitochondrial status. Important tools in such studies are chemical inhibitors used to initiate mitochondrial dysfunction. This study compares the effect of different inhibitors and treatment conditions on the transcript amount of nuclear genes specifically responsive to mitochondrial dysfunction in leaf of Nicotiana tabacum L. cv. Petit Havana. The Complex III inhibitors antimycin A (AA) and myxothiazol (MYXO), and the Complex V inhibitor oligomycin (OLIGO), each increased the transcript amount of the mitochondrial dysfunction genes. Transcript responses to OLIGO were greater during treatment in the dark than in the light, and the dark treatment resulted in cell death. In the dark, transcript responses to AA and MYXO were similar to one another, despite MYXO leading to cell death. In the light, transcript responses to AA and MYXO diverged, despite cell viability remaining high with either inhibitor. This divergent response may be due to differential signaling from the chloroplast because only AA also inhibited cyclic electron transport, resulting in a strong acceptor‐side limitation in photosystem I. In the light, chemical inhibition of chloroplast electron transport reduced transcript responses to AA, while having no effect on the response to MYXO, and increasing the response to OLIGO. Hence, when studying mitochondrial dysfunction signaling, different inhibitor and treatment combinations differentially affect linked processes (e.g. chloroplast function and cell fate) that then contribute to measured responses. Therefore, inhibitor and treatment conditions should be chosen to align with specific study goals.

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Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

Cited by 94 publications

References 64 publications

Mitochondrial complex II of plants: subunit composition, assembly, and function in respiration and signaling

Mitochondrial complex II of plants: subunit composition, assembly, and function in respiration and signaling

Variation in Leaf Respiration Rates at Night Correlates with Carbohydrate and Amino Acid Supply

Signaling interactions between mitochondria and chloroplasts in Nicotiana tabacum leaf

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