The rab GTPase rabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis

Plant Physiology

Volumn 161, Issue 4, 2013, Pages 1722-1736

  Kwon, Soon Il ^a   Cho, Hong Joo ^a   Kim, Sung Ryul ^a   Park, Ohkmae K ^a  

^a Korea University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84875738550     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.208108     Document Type: Article

References (74)

1. Balagué C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15: 365-379
2. Bassham DC (2007) Plant autophagy: more than a starvation response. Curr Opin Plant Biol 10: 587-593
3. Berry DL, Baehrecke EH (2007) Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131: 1137-1148
4. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744
5. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573-1584
6. Century KS, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92: 6597-6601
7. Chung T (2011) See how I eat my green: autophagy in plant cells. J Plant Biol 54: 339-350
8. Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8- lipid adduct are regulated by development and nutrient availability. Plant Physiol 149: 220-234
9. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101
10. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97: 9323-9328
11. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247-1256
12. Devadas SK, Raina R (2002) Preexisting systemic acquired resistance suppresses hypersensitive response-associated cell death in Arabidopsis hrl1 mutant. Plant Physiol 128: 1234-1244
13. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548
14. González-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquère S, Eskelinen EL, Pierron G, Saftig P, Kroemer G (2005) The apoptosis/ autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 118: 3091-3102
15. Gunawardena AH (2008) Programmed cell death and tissue remodelling in plants. J Exp Bot 59: 445-451
16. Gutierrez MG, Munafó DB, Berón W, Colombo MI (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117: 2687-2697
17. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki- Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, et al (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889
18. Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8: 404-408
19. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I (2009) A novel membrane fusionmediated plant immunity against bacterial pathogens. Genes Dev 23: 2496-2506
20. Hayward AP, Dinesh-Kumar SP (2011) What can plant autophagy do for an innate immune response? Annu Rev Phytopathol 49: 557-576
21. Hirota Y, Tanaka Y (2009) A small GTPase, human Rab32, is required for the formation of autophagic vacuoles under basal conditions. Cell Mol Life Sci 66: 2913-2932
22. Hofius D, Munch D, Bressendorff S, Mundy J, Petersen M (2011) Role of autophagy in disease resistance and hypersensitive response-associated cell death. Cell Death Differ 18: 1257-1262
23. Hofius D, Schultz-Larsen T, Joensen J, Tsitsigiannis DI, Petersen NH, Mattsson O, Jørgensen LB, Jones JD, Mundy J, Petersen M (2009) Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137: 773-783
24. Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M (2008) Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19: 2916-2925
25. Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15: 2503-2513
26. Jäger S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen EL (2004) Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117: 4837-4848
27. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329
28. Joubert PE, Meiffren G, Grégoire IP, Pontini G, Richetta C, Flacher M, Azocar O, Vidalain PO, Vidal M, Lotteau V, et al (2009) Autophagy induction by the pathogen receptor CD46. Cell Host Microbe 6: 354-366
29. Jurkowski GI, Smith RK Jr, Yu IC, Ham JH, Sharma SB, Klessig DF, Fengler KA, Bent AF (2004) Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the "defense, no death" phenotype. Mol Plant Microbe Interact 17: 511-520
30. Kang C, You YJ, Avery L (2007) Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes Dev 21: 2161-2171
31. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 147: 435-446
32. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, et al (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884
33. Kourtis N, Tavernarakis N (2009) Autophagy and cell death in model organisms. Cell Death Differ 16: 21-30
34. Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5: 568-573
35. Kwon SI, Cho HJ, Bae K, Jung JH, Jin HC, Park OK (2009) Role of an Arabidopsis Rab GTPase RabG3b in pathogen response and leaf senescence. J Plant Biol 52: 79-87
36. Kwon SI, Cho HJ, Jung JH, Yoshimoto K, Shirasu K, Park OK (2010a) The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J 64: 151-164
37. Kwon SI, Cho HJ, Lee JS, Jin H, Shin SJ, Kwon M, Noh EW, Park OK (2011) Overexpression of constitutively active Arabidopsis RabG3b promotes xylem development in transgenic poplars. Plant Cell Environ 34: 2212-2224
38. Kwon SI, Cho HJ, Park OK (2010b) Role of Arabidopsis RabG3b and autophagy in tracheary element differentiation. Autophagy 6: 1187-1189
39. Lai Z, Wang F, Zheng Z, Fan B, Chen Z (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66: 953-968
40. Lam D, Kosta A, Luciani MF, Golstein P (2008) The inositol 1,4,5-trisphosphate receptor is required to signal autophagic cell death. Mol Biol Cell 19: 691-700
41. Leivar P, González VM, Castel S, Trelease RN, López-Iglesias C, Arró M, Boronat A, Campos N, Ferrer A, Fernàndez-Busquets X (2005) Subcellular localization of Arabidopsis 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Plant Physiol 137: 57-69
42. Lenz HD, Haller E, Melzer E, Kober K, Wurster K, Stahl M, Bassham DC, Vierstra RD, Parker JE, Bautor J, et al (2011) Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66: 818-830
43. Levine B (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120: 159-162
44. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469: 323-335
45. Levine B, Sinha S, Kroemer G (2008) Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4: 600-606
46. Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17: 526-537
47. Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63: 215-237
48. Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121: 567-577
49. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389
50. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and selfkilling: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8: 741-752
51. Naito K, Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact 21: 1165-1174
52. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S (2009) Discovery of Atg5/ Atg7-independent alternative macroautophagy. Nature 461: 654-658
53. Oh IS, Park AR, Bae MS, Kwon SJ, Kim YS, Lee JE, Kang NY, Lee S, Cheong H, Park OK (2005) Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17: 2832-2847
54. Patel S, Dinesh-Kumar SP (2008) Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4: 20-27
55. Ravikumar B, Imarisio S, Sarkar S, O'Kane CJ, Rubinsztein DC (2008) Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J Cell Sci 121: 1649-1660
56. Samara C, Syntichaki P, Tavernarakis N (2008) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15: 105-112
57. Scarlatti F, Granata R, Meijer AJ, Codogno P (2009) Does autophagy have a license to kill mammalian cells? Cell Death Differ 16: 12-20
58. Schmid D, Münz C (2007) Innate and adaptive immunity through autophagy. Immunity 27: 11-21
59. Shapiro AD, Zhang C (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol 127: 1089-1101
60. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Tsujimoto Y (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228
61. Surpin M, Zheng H, Morita MT, Saito C, Avila E, Blakeslee JJ, Bandyopadhyay A, Kovaleva V, Carter D, Murphy A, et al (2003) The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15: 2885-2899
62. Takacs-Vellai K, Vellai T, Puoti A, Passannante M, Wicky C, Streit A, Kovacs AL, Müller F (2005) Inactivation of the autophagy gene bec- 1 triggers apoptotic cell death in C. elegans. Curr Biol 15: 1513-1517
63. Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8: 165-173
64. Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13: 459-465
65. van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara- Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, et al (2011) Morphological classification of plant cell deaths. Cell Death Differ 18: 1241-1246
66. Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, Deretic V (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111: 897-905
67. Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45: 884-894
68. Xia K, Liu T, Ouyang J, Wang R, Fan T, Zhang M (2011) Genome-wide identification, classification, and expression analysis of autophagyassociated gene homologues in rice (Oryza sativa L.). DNA Res 18: 363-377
69. Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42: 535-546
70. Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143: 291-299
71. Yamaguchi H, Nakagawa I, Yamamoto A, Amano A, Noda T, Yoshimori T (2009) An initial step of GAS-containing autophagosome-like vacuoles formation requires Rab7. PLoS Pathog 5: e1000670
72. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16: 2967-2983
73. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21: 2914-2927
74. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502