Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species

Cell Research

Volumn 25, Issue 5, 2015, Pages 621-633

  Wu, Jian ^a   Sun, Yuefeng ^a,b   Zhao, Yannan ^a   Zhang, Jian ^a   Luo, Lilan ^a   Li, Meng ^a   Wang, Jinlong ^a   Yu, Hong ^a   Liu, Guifu ^a   Yang, Liusha ^a   Xiong, Guosheng ^a   Zhou, Jian Min ^a   Zuo, Jianru ^a   Wang, Yonghong ^a   Li, Jiayang ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Arabidopsis thaliana; cell death; chloroplasts; ETC; mitochondria; PPR protein; ROS

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS PROTEIN; ENOYL ACYL CARRIER PROTEIN REDUCTASE (NADH); REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARABIDOPSIS; CELL DEATH; CHLOROPLAST; GENETICS; METABOLISM; MITOCHONDRION; PATHOGENICITY; PHYSIOLOGY; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DEATH; CHLOROPLASTS; ENOYL-(ACYL-CARRIER-PROTEIN) REDUCTASE (NADH); MITOCHONDRIA; NADPH OXIDASE; PSEUDOMONAS SYRINGAE; REACTIVE OXYGEN SPECIES;

EID: 84928929868     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2015.46     Document Type: Article

References (67)

1. Lam E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 2004; 5:305-315
2. Wang C, Youle RJ. The role of mitochondria in apoptosis. Annu Rev Genet 2009; 43:95-118
3. Marchi S, Giorgi C, Suski JM, et al. Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct 2012; 2012:329-635
4. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 2011; 14:691-699
5. Zurbriggen MD, Carrillo N, Hajirezaei MR. ROS signaling in the hypersensitive response: when, where and what for?. Plant Signal Behav 2010; 5:393-396
6. Coll NS, Epple P, Dangl JL. Programmed cell death in the plant immune system. Cell Death Differ 2011; 18:1247-1256
7. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry 2005; 70:200-214
8. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373-399
9. Fearnley IM, Carroll J, Walker JE. Proteomic analysis of the subunit composition of complex I (NADH:ubiquinone oxidoreductase) from bovine heart mitochondria. Methods Mol Biol 2007; 357:103-125
10. Carroll J, Fearnley IM, Shannon RJ, Hirst J, Walker JE. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol Cell Proteomics 2003; 2:117-126
11. Klodmann J, Sunderhaus S, Nimtz M, Jansch L, Braun HP. Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell 2010; 22:797-810
12. Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogen Evol 2003; 29:380-395
13. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 2006; 75:69-92
14. Juszczuk IM, Szal B, Rychter AM. Oxidation-reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. Plant Cell Environ 2012; 35:296-307
15. Perales M, Eubel H, Heinemeyer J, Colaneri A, Zabaleta E, Braun HP. Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I + III2 levels and alters mitochondrial physiology in Arabidopsis. J Mol Biol 2005; 350:263-277
16. Lee BH, Lee H, Xiong L, Zhu JK. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 2002; 14:1235-1251
17. Nakagawa N, Sakurai N. A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 2006; 47:772-783
18. Koprivova A, des Francs-Small CC, Calder G, et al. Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J Biol Chem 2010; 285:32192-32199
19. Pineau B, Layoune O, Danon A, De Paepe R. L-galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 2008; 283:32500-32505
20. Meyer EH, Tomaz T, Carroll AJ, et al. Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol 2009; 151:603-619
21. Dutilleul C, Garmier M, Noctor G, et al. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 2003; 15:1212-1226
22. Zhu Q, Dugardeyn J, Zhang C, et al. The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stresses and hormone responses. Mol Plant 2014; 7:290-310
23. Yuan H, Liu D. Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. Plant J 2012; 70:432-444
24. Woodson JD, Chory J. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 2008; 9:383-395
25. Small ID, Peeters N. The PPR motif -a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 2000; 25:46-47
26. Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 2008; 13:663-670
27. Lurin C, Andres C, Aubourg S, et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 2004; 16:2089-2103
28. O'Toole N, Hattori M, Andres C, et al. On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 2008; 25:1120-1128
29. Mou Z, He Y, Dai Y, Liu X, Li J. Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 2000; 12:405-418
30. Bestwick CS, Brown IR, Bennett MH, Mansfield JW. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 1997; 9:209-221
31. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 2007; 51:941-954
32. Parisi G, Perales M, Fornasari MS, et al. Gamma carbonic anhydrases in plant mitochondria. Plant Mol Biol 2004; 55:193-207
33. Meyer EH, Taylor NL, Millar AH. Resolving and identifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis. J Proteome Res 2008; 7:786-794
34. Barkan A, Rojas M, Fujii S, et al. A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 2012; 8:e1002910
35. Ichinose M, Sugita C, Yagi Y, Nakamura T, Sugita M. Two DYW subclass PPR proteins are involved in RNA editing of ccmFc and atp9 transcripts in the moss Physcomitrella patens: first complete set of PPR editing factors in plant mitochondria. Plant Cell Physiol 2013; 54:1907-1916
36. Hartel B, Zehrmann A, Verbitskiy D, Takenaka M. The longest mitochondrial RNA editing PPR protein MEF12 in Arabidopsis thaliana requires the full-length E domain. RNA Biol 2013; 10:1543-1548
37. Keren I, Tal L, des Francs-Small CC, et al. nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J 2012; 71:413-426
38. He J, Duan Y, Hua D, et al. DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 2012; 24:1815-1833
39. Earley FG, Patel SD, Ragan I, Attardi G. Photolabelling of a mitochondrially encoded subunit of NADH dehydrogenase with [3H]dihydrorotenone. FEBS Lett 1987; 219:108-112
40. Kliebenstein DJ, Monde RA, Last RL. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 1998; 118:637-650
41. Torres MA, Jones JD, Dangl JL. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 2005; 37:1130-1134
42. Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 2002; 99:517-522
43. Bent AF, Kunkel BN, Dahlbeck D, et al. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 1994; 265:1856-1860
44. Gassmann W, Hinsch ME, Staskawicz BJ. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIRNBS-LRR family of disease-resistance genes. Plant J 1999; 20:265-277
45. Mindrinos M, Katagiri F, Yu GL, Ausubel FM. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 1994; 78:1089-1099
46. Xiao Y, Savchenko T, Baidoo EE, et al. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 2012; 149:1525-1535
47. Ichinose M, Tasaki E, Sugita C, Sugita M. A PPR-DYW protein is required for splicing of a group II intron of cox1 pre-mRNA in Physcomitrella patens. Plant J 2012; 70:271-278
48. Drose S, Brandt U. The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 2008; 283:21649-21654
49. Li N, Ragheb K, Lawler G, et al. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 2003; 278:8516-8525
50. Nomura H, Komori T, Uemura S, et al. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat Commun 2012; 3:926
51. Zurbriggen MD, Carrillo N, Tognetti VB, et al. 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
52. Dangl JL, Jones JD. Plant pathogens and integrated defence responses to infection. Nature 2001; 411:826-833
53. Dayan FE, Ferreira D, Wang YH, Khan IA, McInroy JA, Pan Z. A pathogenic fungi diphenyl ether phytotoxin targets plant enoyl (acyl carrier protein) reductase. Plant Physiol 2008; 147:1062-1071
54. Green DR, Galluzzi L, Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011; 333:1109-1112
55. Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011; 147:742-758
56. Taylor RW, Turnbull DM. Mitochondrial DNA mutations in human disease. Nat Rev Genet 2005; 6:389-402
57. Hu Y, Lu W, Chen G, et al. K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res 2012; 22:399-412
58. Sun F, Zhang W, Xiong G, et al. Identification and functional analysis of the MOC1 interacting protein 1. J Genet Genomics 2010; 37:69-77
59. Zuo J, Niu QW, Frugis G, Chua NH. The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 2002; 30:349-359
60. Dai Y, Wang H, Li B, et al. Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 2006; 18:308-320
61. Liu YG, Mitsukawa N, Oosumi T, Whittier RF. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 1995; 8:457-463
62. Stone JM, Heard JE, Asai T, Ausubel FM. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 2000; 12:1811-1822
63. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 1997; 9:1573-1584
64. Ramel F, Sulmon C, Gouesbet G, Couée I. Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent responses to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 2009; 104:1323-1337
65. Hedtke B, Meixner M, Gillandt S, Richter E, Borner T, Weihe A. Green fluorescent protein as a marker to investigate targeting of organellar RNA polymerases of higher plants in vivo. Plant J 1999; 17:557-561
66. Yoo SD, Cho YH, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2007; 2:1565-1572
67. Yao J, Withers J, He SY. Pseudomonas syringae infection assays in Arabidopsis. Methods Mol Biol 2013; 1011:63-81