AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis

Plant Cell

Volumn 26, Issue 2, 2014, Pages 788-807

  Li, Faqiang ^a   Chung, Taijoon ^a,b   Vierstra, Richard D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; AUTOPHAGY RELATED11 PROTEIN, ARABIDOPSIS; AUTOPHAGY-RELATED11 PROTEIN, ARABIDOPSIS; VESICULAR TRANSPORT PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; AUTOPHAGY; BIOLOGICAL MODEL; CELL AGING; CELL VACUOLE; CHEMISTRY; CYTOLOGY; DARKNESS; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOPHAGY; MOLECULAR GENETICS; PHENOTYPE; PHOSPHORYLATION; PHYLOGENY; PLANT GENE; PLANT LEAF; PROTEIN BINDING; PROTEIN SUBUNIT; REVERSE GENETICS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOPHAGY; CELL AGING; DARKNESS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOTYPE; MITOCHONDRIAL DEGRADATION; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHOSPHORYLATION; PHYLOGENY; PLANT LEAVES; PROTEIN BINDING; PROTEIN SUBUNITS; REVERSE GENETICS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84897081288     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.120014     Document Type: Article

References (71)

1. Alemu, E.A., Lamark, T., Torgersen, K.M., Birgisdottir, A.B., Larsen, K.B., Jain, A., Olsvik, H., Øvervatn, A., Kirkin, V., and Johansen, T. (2012). ATG8 family proteins act as scaffolds for assembly of the ULK complex: Sequence requirements for LC3-interacting region (LIR) motifs. J. Biol. Chem. 287: 39275-39290.
2. Aoki, Y., Kanki, T., Hirota, Y., Kurihara, Y., Saigusa, T., Uchiumi, T., and Kang, D. (2011). Phosphorylation of serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22: 3206-3217.
3. Behrends, C., Sowa, M.E., Gygi, S.P., and Harper, J.W. (2010). Network organization of the human autophagy system. Nature 466: 68-76.
4. Chen, Y., and Klionsky, D.J. (2011). The regulation of autophagy: Unanswered questions. J. Cell Sci. 124: 161-170.
5. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., and Thompson, J.D. (2003). Multiple sequence alignment with the CLUSTAL series of programs. Nucleic Acids Res. 31: 3497-3500.
6. Cheong, H., Nair, U., Geng, J., and Klionsky, D.J. (2008). The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 19: 668-681.
7. Chung, T., Phillips, A.R., and Vierstra, R.D. (2010). ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. Plant J. 62: 483-493.
8. Chung, T., Suttangkakul, A., and Vierstra, R.D. (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. Colcombet, J., Lopez-Obando, M., Heurtevin, L., Bernard, C., Martin, K., Berthomé, R., and Lurin, C. (2013). Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biol. 10: 1557-1575.
10. Doelling, J.H., Walker, J.M., Friedman, E.M., Thompson, A.R., and Vierstra, R.D. (2002). The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277: 33105-33114.
11. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
12. Farmer, L.M., Rinaldi, M.A., Young, P.G., Danan, C.H., Burkhart, S.E., and Bartel, B. (2013). Disrupting autophagy restores peroxisome function to an Arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. Plant Cell 25: 4085-4100.
13. Ganley, I.G., Lam, H., Wang, J., Ding, X., Chen, S., and Jiang, X. (2009). ULK1-ATG13-FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284: 12297-12305.
14. Han, L., Qin, G., Kang, D., Chen, Z., Gu, H., and Qu, L.J. (2010). A nuclear-encoded mitochondrial gene AtCIB22 is essential for plant development in Arabidopsis. J. Genet. Genomics 37: 667-683.
15. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S., and Ohsumi, Y. (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129: 1181-1193.
16. Hara, T., Takamura, A., Kishi, C., Iemura, S., Natsume, T., Guan, J.L., and Mizushima, N. (2008). FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181: 497-510.
17. Hayward, A.P., and Dinesh-Kumar, S.P. (2011). What can plant autophagy do for an innate immune response? Annu. Rev. Phytopathol. 49: 557-576.
18. Herman, E.M., and Larkins, B.A. (1999). Protein storage bodies and vacuoles. Plant Cell 11: 601-614.
19. Hillwig, M.S., Contento, A.L., Meyer, A., Ebany, D., Bassham, D.C., and Macintosh, G.C. (2011). RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc. Natl. Acad. Sci. USA 108: 1093-1098.
20. Hosokawa, N., Sasaki, T., Iemura, S., Natsume, T., Hara, T., and Mizushima, N. (2009). Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5: 973-979.
21. Hu, C.D., Chinenov, Y., and Kerppola, T.K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9: 789-798.
22. Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., Ohsumi, Y., Hanson, M.R., and Mae, T. (2008). Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 148: 142-155.
23. Itakura, E., Kishi-Itakura, C., Koyama-Honda, I., and Mizushima, N. (2012). Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J. Cell Sci. 125: 1488-1499.
24. Johansen, T., and Lamark, T. (2011). Selective autophagy mediated by autophagic adapter proteins. Autophagy 7: 279-296.
25. Journet, E.P., Bligny, R., and Douce, R. (1986). Biochemical changes during sucrose deprivation in higher plant cells. J. Biol. Chem. 261: 3193-3199.
26. Jung, C.H., Jun, C.B., Ro, S.H., Kim, Y.M., Otto, N.M., Cao, J., Kundu, M., and Kim, D.H. (2009). ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20: 1992-2003.
27. Kabeya, Y., Kamada, Y., Baba, M., Takikawa, H., Sasaki, M., and Ohsumi, Y. (2005). Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol. Biol. Cell 16: 2544-2553.
28. Kanki, T., Wang, K., Cao, Y., Baba, M., and Klionsky, D.J. (2009). Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17: 98-109.
29. Keech, O., Pesquet, E., Ahad, A., Askne, A., Nordvall, D., Vodnala, S.M., Tuominen, H., Hurry, V., Dizengremel, P., and Gardeström, P. (2007). The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant Cell Environ. 30: 1523-1534.
30. Kim, J., Lee, H., Lee, H.N., Kim, S.H., Shin, K.D., and Chung, T. (2013). Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell 25: 4956-4966.
31. Kraft, C., et al. (2012). Binding of the Atg1/ULK1 kinase to the ubiquitinlike protein Atg8 regulates autophagy. EMBO J. 31: 3691-3703.
32. Lenz, H.D., et al. (2011). Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 66: 818-830.
33. Li, F., and Vierstra, R.D. (2012). Autophagy: A multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci. 17: 526-537.
34. Liang, C.C., Wang, C., Peng, X., Gan, B., and Guan, J.L. (2010). Neural-specific deletion of FIP200 leads to cerebellar degeneration caused by increased neuronal death and axon degeneration. J. Biol. Chem. 285: 3499-3509.
35. Lin, L., Yang, P., Huang, X., Zhang, H., Lu, Q., and Zhang, H. (2013). The scaffold protein EPG-7 links cargo-receptor complexes with the autophagic assembly machinery. J. Cell Biol. 201: 113-129.
36. Liu, Y., and Bassham, D.C. (2012). Autophagy: Pathways for selfeating in plant cells. Annu. Rev. Plant Biol. 63: 215-237.
37. Liu, Y., Burgos, J.S., Deng, Y., Srivastava, R., Howell, S.H., and Bassham, D.C. (2012). Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24: 4635-4651.
38. Mao, K., Wang, K., Liu, X., and Klionsky, D.J. (2013). The scaffold protein Atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev. Cell 26: 9-18.
39. Marion, J., Bach, L., Bellec, Y., Meyer, C., Gissot, L., and Faure, J.D. (2008). Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J. 56: 169-179.
40. Martin, K., Kopperud, K., Chakrabarty, R., Banerjee, R., Brooks, R., and Goodin, M.M. (2009). Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 59: 150-162.
41. Meijer, W.H., van der Klei, I.J., Veenhuis, M., and Kiel, J.A. (2007). ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 3: 106-116.
42. Mercer, C.A., Kaliappan, A., and Dennis, P.B. (2009). A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5: 649-662.
43. Mizushima, N. (2010). The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22: 132-139.
44. Nakatogawa, H., Ohbayashi, S., Sakoh-Nakatogawa, M., Kakuta, S., Suzuki, S.W., Kirisako, H., Kondo-Kakuta, C., Noda, N.N., Yamamoto, H., and Ohsumi, Y. (2012). The autophagy-related protein kinase Atg1 interacts with the ubiquitin-like protein Atg8 via the Atg8 family interacting motif to facilitate autophagosome formation. J. Biol. Chem. 287: 28503-28507.
45. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51: 1126-1136.
46. Noda, N.N., Ohsumi, Y., and Inagaki, F. (2010). Atg8 family interacting motif crucial for selective autophagy. FEBS Lett. 584: 1379-1385.
47. Novak, I., et al. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11: 45-51.
48. Okamoto, K., Kondo-Okamoto, N., and Ohsumi, Y. (2009). Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17: 87-97.
49. Pankiv, S., Alemu, E.A., Brech, A., Bruun, J.A., Lamark, T., Overvatn, A., Bjørkøy, G., and Johansen, T. (2010). FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol. 188: 253-269.
50. Phillips, A.R., Suttangkakul, A., and Vierstra, R.D. (2008). The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178: 1339-1353.
51. Ragusa, M.J., Stanley, R.E., and Hurley, J.H. (2012). Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151: 1501-1512.
52. Reggiori, F., and Klionsky, D.J. (2013). Autophagic processes in yeast: Mechanism, machinery and regulation. Genetics 194: 341-361.
53. Reyes, F.C., Chung, T., Holding, D., Jung, R., Vierstra, R., and Otegui, M.S. (2011). Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell 23: 769-784.
54. Scott, I., and Logan, D.C. (2010). Mitochondrial dynamics. In Plant Mitochondria, F. Kempken, ed (Berlin: Springer), pp. 31-63.
55. Shibata, M., Oikawa, K., Yoshimoto, K., Kondo, M., Mano, S., Yamada, K., Hayashi, M., Sakamoto, W., Ohsumi, Y., and Nishimura, M. (2013). Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 25: 4967-4983.
56. Shintani, T., and Klionsky, D.J. (2004). Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 279: 29889-29894.
57. Smalle, J., Kurepa, J., Yang, P., Babiychuk, E., Kushnir, S., Durski, A., and Vierstra, R.D. (2002). Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12. Plant Cell 14: 17-32.
58. Suttangkakul, A., Li, F., Chung, T., and Vierstra, R.D. (2011). The ATG1/ ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23: 3761-3779.
59. Suzuki, K., Kubota, Y., Sekito, T., and Ohsumi, Y. (2007). Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12: 209-218.
60. Svenning, S., Lamark, T., Krause, K., and Johansen, T. (2011). Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7: 993-1010.
61. Thompson, A.R., Doelling, J.H., Suttangkakul, A., and Vierstra, R.D. (2005). Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138: 2097-2110.
62. Vanhee, C., Zapotoczny, G., Masquelier, D., Ghislain, M., and Batoko, H. (2011). The Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy-dependent degradation mechanism. Plant Cell 23: 785-805.
63. Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., and Makino, A. (2009). Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 149: 885-893.
64. Weaver, L.M., and Amasino, R.M. (2001). Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol. 127: 876-886.
65. Wong, P.M., Puente, C., Ganley, I.G., and Jiang, X. (2013). The ULK1 complex: Sensing nutrient signals for autophagy activation. Autophagy 9: 124-137.
66. Xiong, Y., Contento, A.L., and Bassham, D.C. (2005). AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J. 42: 535-546.
67. Xiong, Y., McCormack, M., Li, L., Hall, Q., Xiang, C., and Sheen, J. (2013). Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496: 181-186.
68. Yorimitsu, T., and Klionsky, D.J. (2005). Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol. Biol. Cell 16: 1593-1605.
69. Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T., and Ohsumi, Y. (2004). Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16: 2967-2983.
70. Zhang, X., and Hu, J. (2009). Two small protein families, DYNAMINRELATED PROTEIN3 and FISSION1, are required for peroxisome fission in Arabidopsis. Plant J. 57: 146-159.
71. Zhou, J., Wang, J., Cheng, Y., Chi, Y.J., Fan, B., Yu, J.Q., and Chen, Z. (2013). NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet. 9: e1003196.