Plant mitochondria under pathogen attack: A sigh of relief or a last breath?

Mitochondrion

Volumn 19, Issue PB, 2014, Pages 238-244

  Colombatti, Francisco ^a   Gonzalez, Daniel H ^a   Welchen, Elina ^a  

^a Universidad Nacional del Litoral   (Argentina)

Author keywords

Alternative oxidase; Biotic stress; Cytochrome c; Defense response; Pathogen; Plant mitochondria

Indexed keywords

NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID;

APOPTOSIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MITOCHONDRION; OXIDATION REDUCTION REACTION; PLANT;

APOPTOSIS; GENE EXPRESSION REGULATION, PLANT; MITOCHONDRIA; NITRIC OXIDE; OXIDATION-REDUCTION; PLANTS; REACTIVE OXYGEN SPECIES; SALICYLIC ACID;

EID: 84914172856     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2014.03.006     Document Type: Article

References (93)

1. Abramovitch R.B., Anderson J.C., Martin G.B. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 2006, 7:601-611.
2. Alfano J.R., Collmer A. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 2004, 42:385-414.
3. Amirsadeghi S., Robson C.A., Vanlerberghe G.C. The role of the mitochondrion in plant responses to biotic stress. Physiol. Plant. 2007, 129:253-266.
4. Attallah C.V., Welchen E., Gonzalez D.H. The promoters of Arabidopsis thaliana genes AtCOX17-1 and -2, encoding a copper chaperone involved in cytochrome c oxidase biogenesis, are preferentially active in roots and anthers and induced by biotic and abiotic stress. Physiol. Plant. 2007, 129:123-134.
5. Attallah C.V., Welchen E., Pujol C., Bonnard G., Gonzalez D.H. Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol. Biol. 2007, 65:343-355.
6. Balk J., Leaver C.J., McCabe P.F. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 1999, 463:151-154.
7. Bindschedler L.V., Dewdney J., Blee K.A., Stone J.M., Asai T., Plotnikov J., Denoux C., Hayes T., Gerrish C., Davies D.R., Ausubel F.M., Bolwell G.P. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 2006, 47:851-863.
8. Block A., Alfano J.R. Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys?. Curr. Opin. Microbiol. 2011, 14:39-46.
9. Block A., Li G., Fu Z.Q., Alfano J.R. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 2008, 11:396-403.
10. Block A., Guo M., Li G., Elowsky C., Clemente T.E., Alfano J.R. The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell. Microbiol. 2010, 12:318-330.
11. Boccara M., Boué C., Garmier M., De Paepe R., Boccara A.-C. Infra-red thermography revealed a role for mitochondria in pre-symptomatic cooling during harpin-induced hypersensitive response. Plant J. 2001, 28:663-670.
12. Brenner C., Grimm S. The permeability transition pore complex in cancer cell death. Oncogene 2006, 25:4744-4756.
13. Cheng D.-D., Jia Y.-J., Gao H.-Y., Zhang L.-T., Zhang Z.-S., Xue Z.-C., Meng Q.-W. Characterization of the programmed cell death induced by metabolic products of Alternaria alternata in tobacco BY-2 cells. Physiol. Plant. 2011, 141:117-129.
14. Chisholm S.T., Coaker G., Day B., Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
15. Coll N.S., Epple P., Dangl J.L. Programmed cell death in the plant immune system. Cell Death Differ. 2011, 18:1247-1256.
16. Curtis M.J., Wolpert T.J. The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J. 2004, 38:244-259.
17. Cvetkovska M., Vanlerberghe G.C. Coordination of a mitochondrial superoxide burst during the hypersensitive response to bacterial pathogen in Nicotiana tabacum. Plant Cell Environ. 2012, 35:1121-1136.
18. Cvetkovska M., Vanlerberghe G.C. Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 2013, 36:721-732.
19. Cvetkovska M., Alber N.A., Vanlerberghe G.C. The signaling role of a mitochondrial superoxide burst during stress. Plant Signal. Behav. 2012, 8:e22749.
20. Dangl J.L., Jones J.D. Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
21. del Pozo O., Lam E. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 1998, 8:1129-1132.
22. Fernández-Ocaña A., Chaki M., Luque F., Gómez-Rodríguez M.V., Carreras A., Valderrama R., Begara-Morales J.C., Hernández L.E., Corpas F.J., Barroso J.B. Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions. Identification of two new genes of mitochondrial Mn-SOD. J. Plant Physiol. 2011, 168:1303-1308.
23. Florez-Sarasa I., Flexas J., Rasmusson A.G., Umbach A.L., Siedow J.N., Ribas-Carbo M. In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant Cell Environ. 2011, 34:1373-1383.
24. Gardner P.R. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 2005, 99:247-266.
25. Gleason C., Huang S., Thatcher L.F., Foley R.C., Anderson C.R., Carroll A.J., Millar A.H., Singh K.B. Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10768-10773.
26. Greenberg J.T., Vinatzer B.A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 2003, 6:20-28.
27. Gupta K.J., Kaiser V.M. Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol. 2010, 51:576-584.
28. Gupta K.J., Igamberdiev A.U., Manjunatha G., Segu S., Moran J.F., Neelawarne B., Bauwe H., Kaiser W.M. The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci. 2011, 181:520-526.
29. Hoeberichts F.A., Woltering E.J. Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 2002, 25:47-57.
30. Homble F., Krammer E.M., Prevost M. Plant VDAC: facts and speculations. Biochim. Biophys. Acta 2012, 1818:1486-1501.
31. Huang Y., Chen X., Liu Y., Roth C., Copeland C., McFarlane H.E., Huang S., Lipka V., Wiermer M., Li X. Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity. Nat. Commun. 2013, 4:2558.
32. Jelenska J., van Hal J.A., Greenberg J.T. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:13177-13182.
33. Jones A. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?. Trends Plant Sci. 2000, 5:225-230.
34. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
35. Kawai-Yamada M., Jin L., Yoshinaga K., Hirata A., Uchimiya H. Mammalian Bax-induced plant cell death can be downregulated by overexpression of Arabidopsis Bax inhibitor-1 (AtBI-1). Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12295-12300.
36. Kawai-Yamada M., Ohori Y., Uchimiya H. Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax, hydrogen peroxide and salicylic acid-induced cell death. Plant Cell 2004, 16:21-32.
37. Kiba A., Takata O., Ohnishi K., Hikichi Y. Comparative analysis of induction pattern of programmed cell death and defense-related responses during hypersensitive cell death and development of bacterial necrotic leaf spots in eggplant. Planta 2006, 224:981-994.
38. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275(5303):1132-1136.
39. Krause M., Durner J. Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol. Plant Microbe Interact. 2004, 17:131-139.
40. Kusano T., Tateda C., Berberich T., Takahashi Y. Voltage-dependent anion channels: their roles in plant defense and cell death. Plant Cell Rep. 2009, 28:1301-1308.
41. Lacomme C., Santa Cruz S. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7956-7961.
42. Laloi C., Apel K., Danon A. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 2004, 7:323-328.
43. Lam E., Kato N., Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 2001, 411:848-853.
44. Lamb C., Dixon R.A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48:251-275.
45. Lee W.-S., Fu S.-F., Verchot-Lubicz J., Carr J. Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biol. 2011, 11:1-10.
46. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86(1):147-157.
47. Lorrain S., Vailleau F., Balague C., Roby D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?. Trends Plant Sci. 2003, 8:263-271.
48. Maxwell D.P., Wang Y., McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8271-8276.
49. Maxwell D.P., Nickels R., McIntosh L. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 2002, 29:269-279.
50. Mitsuhara I., Malik K.A., Miura M., Ohashi Y. Animal cell death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 1999, 9:775-778.
51. Modolo L.V., Augusto O., Almeida I.M., Magalhaes J.R., Salgado I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 2005, 579:3814-3820.
52. Møller I.M. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:561-591.
53. Møller I.M., Sweetlove L.J. ROS signalling-specificity is required. Trends Plant Sci. 2010, 15:370-374.
54. Morgan M.J., Lehmann M., Schwarzländer M., Baxter C.J., Sienkiewicz-Porzucek A., Williams T.C.R., Schauer N., Fernie A.R., Fricker M.D., Ratcliffe R.G., Sweetlove L.J., Finkemeier I. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 2008, 147:101-114.
55. Mur L.A., Carver T.L., Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 2006, 7:489-505.
56. Mur L.A., Kenton P., Lloyd A.J., Ougham H., Prats E. The hypersensitive response; the centenary is upon us but how much do we know?. J. Exp. Bot. 2008, 59:501-520.
57. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R.J., Matsuda H., Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14681-14688.
58. Navrot N., Rouhier N., Gelhaye E., Jacquot J.P. Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol. Plant. 2007, 129:185-195.
59. Norman C., Howell K.A., Millar A., Whelan J.M., Day D.A. Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 2004, 134:492-501.
60. Ordog S.H., Higgins V.J., Vanlerberghe G.C. Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol. 2002, 129:1858-1865.
61. Planchet E., Jagadis Gupta K., Sonoda M., Kaiser W.M. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 2005, 41:732-743.
62. Podgorska A., Gieczewska K., Lukawska-Kuzma K., Rasmusson A.G., Gardestrom P., Szal B. Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)(+) ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant Cell Environ. 2013, 36:2034-2045.
63. Rasmusson A.G., Møller I.M. Mitochondrial electron transport and plant stress. Plant Mitochondria 2011, vol. 1:357-381. Springer, New York. F. Kempken (Ed.).
64. Rasmusson A.G., Soole K.L., Elthon T.E. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 2004, 55:23-39.
65. Rasmusson A.G., Geisler D.A., Møller I.M. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 2008, 8:47-60.
66. Robson C.A., Vanlerberghe G.C. Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol. 2002, 129:1908-1920.
67. Senthil-Kumar M., Mysore K.S. Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant Cell Environ. 2012, 35:1329-1343.
68. Siedow J.N., Umbach A.L. Plant mitochondrial electron transfer and molecular biology. Plant Cell 1995, 7:821-831.
69. Simons B.H., Millenaar F.F., Mulder L., Van Loon L.C., Lambers H. Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv tomato. Plant Physiol. 1999, 120:529-538.
70. Solovieva A.D., Frolova O.Y., Solovyev A.G., Morozov S.Y., Zamyatnin A.A. Effect of mitochondria-targeted antioxidant SkQ1 on programmed cell death induced by viral proteins in tobacco plants. Biochemistry (Mosc) 2013, 78:1006-1012.
71. Sun Y., Zhao Y., Hong X., Zhai Z. Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett. 1999, 462:317-321.
72. Takahashi Y., Tateda C. The functions of voltage-dependent anion channels in plants. Apoptosis 2013, 18:917-924.
73. Takahashi Y., Berberich T., Miyazaki A., Seo S., Ohashi Y., Kusano T. Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J. 2003, 36:820-829.
74. Tateda C., Yamashita K., Takahashi F., Kusano T., Takahashi Y. Plant voltage-dependent anion channels are involved in host defense against Pseudomonas cichorii and in Bax-induced cell death. Plant Cell Rep. 2009, 28:41-51.
75. Torres M.A. ROS in biotic interactions. Physiol. Plant. 2010, 138:414-429.
76. Torres M.A., Dangl J.L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 2005, 8:397-403.
77. Torres M.A., Jones J.D.G., Dangl J.L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 2006, 141:373-378.
78. Van Aken O., Zhang B., Law S., Narsai R., Whelan J. AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins. Plant Physiol. 2013, 162:254-271.
79. Vanlerberghe G.C., Robson C.A., Yip J.Y. Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol. 2002, 129:1829-1842.
80. Vanlerberghe G.C., Cvetkovska M., Wang J. Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase?. Physiol. Plant. 2009, 137:392-406.
81. Vianello A., Zancani M., Peresson C., Petrussa E., Casolo V., Krajňáková J., Patui S., Braidot E., Macrì F. Plant mitochondrial pathway leading to programmed cell death. Physiol. Plant. 2007, 129:242-252.
82. Vidal G., Ribas-Carbo M., Garmier M., Dubertret G., Rasmusson A.G., Mathieu C., Foyer C.H., De Paepe R. Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 2007, 19:640-655.
83. Wallström S.V., Florez-Sarasa I., Araújo W.L., Aidemark M., Fernández-Fernández M., Fernie A.R., Ribas-Carbó M., Rasmusson A.G. Suppression of the external mitochondrial NADPH dehydrogenase, NDB1, in Arabidopsis thaliana affects central metabolism and vegetative growth. Mol. Plant 2014, 7:356-368.
84. Welchen E., García L., Mansilla N., Gonzalez D.H. Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements. Front. Plant Sci. 2014, 4:551.
85. Xie Z., Chen Z. Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. Plant Physiol. 1999, 120:217-226.
86. Xie Z., Chen Z. Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells. Mol. Plant Microbe Interact. 2000, 13:183-190.
87. Yao N., Greenberg J.T. Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 2006, 18:397-411.
88. Yao N., Tada Y., Sakamoto M., Nakayashiki H., Park P., Tosa Y., Mayama S. Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J. 2002, 30:567-579.
89. Yao N., Eisfelder B.J., Marvin J., Greenberg J.T. The mitochondrion - an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J. 2004, 40:596-610.
90. Yip J.Y., Vanlerberghe G.C. Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol. Plant. 2001, 112:327-333.
91. Zhang L., Oh Y., Li H., Baldwin I.T., Galis I. Alternative oxidase in resistance to biotic stresses: Nicotiana attenuata AOX contributes to resistance to a pathogen and a piercing-sucking insect but not Manduca sexta larvae. Plant Physiol. 2012, 160:1453-1467.
92. Zipfel C., Robatzek S., Navarro L., Oakeley E.J., Jones J.D., Felix G., Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428:764-767.
93. Zurbriggen M.D., Carrillo N., Tognetti V.B., Melzer M., Peisker M., Hause B., Hajirezaei M.R. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 2009, 60:962-973.