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

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 26, 2011, Pages 10768-10773

  Gleason, Cynthia ^a   Huang, Shaobai ^b   Thatcher, Louise F ^a,c   Foley, Rhonda C ^a   Anderson, Carol R ^a   Carroll, Adam J ^d   Millar, A Harvey ^b   Singh, Karam B ^a,b  

^a CSIRO   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Plant defense; Pseudomonas syringae; Respiration; Rhizoctonia solani

Indexed keywords

DSR1 PROTEIN; PROTEIN; SALICYLIC ACID; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE 1; UNCLASSIFIED DRUG;

ABIOTIC STRESS; ARABIDOPSIS; ARTICLE; BACTERIAL INFECTION; BIOTIC STRESS; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; FLUORESCENCE ANALYSIS; GENE CONTROL; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; IN VIVO STUDY; NONHUMAN; PLANT STRESS; PRIORITY JOURNAL; ROOT CELL; TRANSCRIPTION INITIATION;

ARABIDOPSIS; BACTERIA; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX II; FUNGI; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROGEN PEROXIDE; MITOCHONDRIA; MUTATION; REACTIVE OXYGEN SPECIES; VIRULENCE;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EUKARYOTA; PSEUDOMONAS SYRINGAE; THANATEPHORUS CUCUMERIS;

EID: 79960584575     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1016060108     Document Type: Article

References (45)

1. Anderson JP, et al. (2010) Plants versus pathogens: An evolutionary arms race. Funct Plant Biol 37:499-512.
2. Dodds PN, Rathjen JP (2010) Plant immunity: Towards an integrated view of plantpathogen interactions. Nat Rev Genet 11:539-548.
3. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451-458.
4. Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3:706-718.
5. Torres MA (2010) ROS in biotic interactions. Physiol Plant 138:414-429.
6. Moons A, Gerald L (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitamins and Hormones, ed Litwack G (Academic, New York), Vol 72, pp 155-202.
7. 2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J 10:955-966.
8. Kovtun Y, Chiu W-L, Tena G, Sheen J (2000) Functional analysis of oxidative stressactivated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940-2945. (Pubitemid 30159276)
9. Sappl PG, et al. (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53-68.
10. Navrot N, Rouhier N, Gelhaye E, Jacquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185-195. (Pubitemid 44953386)
11. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357-366.
12. Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J 19:667-677.
13. Foley RC, Sappl PG, Perl-Treves R, Millar AH, Singh KB (2006) Desensitization of GSTF8 induction by a prior chemical treatment is long lasting and operates in a tissue-dependent manner. Plant Physiol 142:245-253. (Pubitemid 44412244)
14. Jiang C, et al. (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ 32:1046-1059.
15. Sneh B, Jabaiji-Hare S, Neate S, Dijst G (1996) Rhizoctonia Species: Taxonomy, Molecular Biology, Ecology, Pathology, and Disease Control (Kluwer, Dordrecht, The Netherlands).
16. Perl-Treves R, Foley RC, Chen W, Singh KB (2004) Early induction of the Arabidopsis GSTF8 promoter by specific strains of the fungal pathogen Rhizoctonia solani. Mol Plant Microbe Interact 17:70-80. (Pubitemid 38398229)
17. Sun F, et al. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121:1043-1057. (Pubitemid 40884395)
18. León G, Holuigue L, Jordana X (2007) Mitochondrial complex II Is essential for gametophyte development in Arabidopsis. Plant Physiol 143:1534-1546. (Pubitemid 46849466)
19. Huang S, et al. (2010) Functional and composition differences between mitochondrial complex II in Arabidopsis and rice are correlated with the complex genetic history of the enzyme. Plant Mol Biol 72:331-342.
20. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: Central role of complex III. J Biol Chem 278:36027-36031. (Pubitemid 37139922)
21. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT (2008) Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 28:718-731.
22. Bourgeron T, et al. (1995) Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat Genet 11:144-149.
23. Burnichon N, et al. (2010) SDHA is a tumor suppressor gene causing paraganglioma. Hum Mol Genet 19:3011-3020.
24. Baysal BE (2002) Hereditary paraganglioma targets diverse paraganglia. J Med Genet 39:617-622.
25. Chase CD (2007) Cytoplasmic male sterility: A window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81-90.
26. Moller IM (2001) PLANT MITOCHONDRIA AND OXIDATIVE STRESS: Electron Transport, NADPH Turnover, and Metabolism of Reactive Oxygen Species. Annu Rev Plant Physiol Plant Mol Biol 52:561-591.
27. Dutilleul C, et al. (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212-1226. (Pubitemid 36579979)
28. Meyer EH, et al. (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol 151:603-619.
29. Krause M, Durner J (2004) Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol Plant Microbe Interact 17:131-139. (Pubitemid 38390994)
30. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; The centenary is upon us but how much do we know? J Exp Bot 59:501-520.
31. Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101-127.
32. Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257-268. (Pubitemid 34179486)
33. Kumar V, Parkhi V, Kenerley CM, Rathore KS (2009) Defense-related gene expression and enzyme activities in transgenic cotton plants expressing an endochitinase gene from Trichoderma virens in response to interaction with Rhizoctonia solani. Planta 230:277-291.
34. Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517-522. (Pubitemid 34060393)
35. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397-403. (Pubitemid 40817382)
36. Gottlieb E, Tomlinson IP (2005) Mitochondrial tumour suppressors: A genetic and biochemical update. Nat Rev Cancer 5:857-866. (Pubitemid 41746030)
37. Møller IM, Sweetlove LJ (2010) ROS signalling - Specificity is required. Trends Plant Sci 15:370-374.
38. Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978-984. (Pubitemid 352844254)
39. Kowaltowski AJ, Vercesi AE (1999) Mitochondrial damage induced by conditions of oxidative stress. Free Rad Biol Med 26:463-471. (Pubitemid 29013479)
40. Braidot E, Petrussa E, Vianello A, Macrì F (1999) Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I or complex II substrates. FEBS Lett 451:347-350. (Pubitemid 29243805)
41. Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139:1806-1820. (Pubitemid 43899820)
42. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177-206.
43. Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673-1678.
44. Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261-270. (Pubitemid 27161898)
45. Love AJ, Milner JJ, Sadanandom A (2008) Timing is everything: Regulatory overlap in plant cell death. Trends Plant Sci 13:589-595.