Origin of the autophagosomal membrane in plants

Frontiers in Plant Science

Volumn 7, Issue November 2016, 2016, Pages

  Zhuang, Xiaohong ^a   Chung, Kin Pan ^a   Jiang, Liwen ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Autophagosome; Autophagy; ER; Membrane contact site; Membrane origin

Indexed keywords

EID: 85007284295     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01655     Document Type: Article

References (76)

1. Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Habermann, A., et al. (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701. doi: 10.1083/jcb.200803137
2. Bockler, S., and Westermann, B. (2014). Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev. Cell 28, 450-458. doi: 10.1016/j.devcel.2014.01.012
3. Chiba, A., Ishida, H., Nishizawa, N. K., Makino, A., and Mae, T. (2003). Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol. 44, 914-921. doi: 10.1093/pcp/pcg118
4. Floyd, B. E., Morriss, S. C., Macintosh, G. C., and Bassham, D. C. (2012). What to eat: evidence for selective autophagy in plants. J. Integr. Plant Biol. 54, 907-920.
5. Gao, C., Luo, M., Zhao, Q., Yang, R., Cui, Y., Zeng, Y., et al. (2014). A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Curr. Biol. 24, 2556-2563.
6. Gao, C., Zhuang, X., Cui, Y., Fu, X., He, Y., Zhao, Q., et al. (2015). Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. Proc. Natl. Acad. Sci. U.S.A. 112, 1886-1891. doi: 10.1073/pnas.1421271112
7. Ge, L., Melville, D., Zhang, M., and Schekman, R. (2013). The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife 2: e00947. doi: 10.7554/eLife. 00947
8. Guiboileau, A., Yoshimoto, K., Soulay, F., Bataille,M. P., Avice, J. C., and Masclaux-Daubresse, C. (2012). Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol. 194, 732-740. doi: 10.1111/j.1469-8137.2012.04084.x
9. Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., et al. (2013). Autophagosomes form at ER-mitochondria contact sites. Nature 495, 389-393. doi: 10.1038/nature11910
10. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., et al. (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129, 1181-1193. doi: 10.1104/pp.011024
11. Hawes, C., Kiviniemi, P., and Kriechbaumer, V. (2015). The endoplasmic reticulum: a dynamic and well-connected organelle. J. Integr. Plant Biol. 57, 50-62. doi: 10.1111/jipb.12297
12. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437. doi: 10.1038/ncb1991
13. Inoue, Y., Suzuki, T., Hattori, M., Yoshimoto, K., Ohsumi, Y., and Moriyasu, Y. (2006). AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol. 47, 1641-1652. doi: 10.1093/pcp/pcl031
14. Ishida, H., Izumi, M., Wada, S., and Makino, A. (2014). Roles of autophagy in chloroplast recycling. Biochim. Biophys. Acta 1837, 512-521. doi: 10.1016/j.bbabio.2013.11.009
15. Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., et al. (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. doi: 10.1104/pp.108.122770
16. Isono, E., Katsiarimpa, A., Muller, I. K., Anzenberger, F., Stierhof, Y. D., Geldner, N., et al. (2010). The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22, 1826-1837. doi: 10.1105/tpc.110.075952
17. Izumi, M., Wada, S., Makino, A., and Ishida, H. (2010). The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol. 154, 1196-1209. doi: 10.1104/pp.110.158519
18. Jaipargas, E. A., Barton, K. A., Mathur, N., and Mathur, J. (2015). Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics. Front. Plant Sci. 6: 783. doi: 10.3389/fpls.2015.00783
19. Karanasios, E., Walker, S. A., Okkenhaug, H., Manifava, M., Hummel, E., Zimmermann, H., et al. (2016). Autophagy initiation by ULK complex assembly on ER tubulovesicular regions marked by ATG9 vesicles. Nat. Commun. 7: 12420. doi: 10.1038/ncomms12420
20. Kolb, C., Nagel, M. K., Kalinowska, K., Hagmann, J., Ichikawa, M., Anzenberger, F., et al. (2015). FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis. Plant Physiol. 167, 1361-1373. doi: 10.1104/pp.114.253377
21. Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., Weissman, J. S., et al. (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481. doi: 10.1126/science.1175088
22. Kwon, S. I., Cho, H. J., Kim, S. R., and Park, O. K. (2013). The Rab GTPase RabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis. Plant Physiol. 161, 1722-1736. doi: 10.1104/pp.112.208108
23. Lamb, C. A., Yoshimori, T., and Tooze, S. A. (2013). The autophagosome: origins unknown, biogenesis complex. Nat. Rev. Mol. Cell Biol. 14, 759-774. doi: 10.1038/nrm3696
24. Le Bars, R., Marion, J., Le Borgne, R., Satiat-Jeunemaitre, B., and Bianchi, M. W. (2014). ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat. Commun. 5: 4121. doi: 10.1038/ncomms5121
25. Lee, T. A., Vande Wetering, S. W., and Brusslan, J. A. (2013). Stromal protein degradation is incomplete in Arabidopsis thaliana autophagy mutants undergoing natural senescence. BMC Res. Notes 6: 17. doi: 10.1186/1756-0500-6-17
26. Li, F., Chung, T., and Vierstra, R. D. (2014). AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 26, 788-807. doi: 10.1105/tpc.113.120014
27. Li, F., and Vierstra, R. D. (2012). Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci. 17, 526-537. doi: 10.1016/j.tplants.2012.05.006
28. Lin, Y., Ding, Y., Wang, J., Shen, J., Kung, C. H., Zhuang, X., et al. (2015). Exocystpositive organelles and autophagosomes are distinct organelles in plants. Plant Physiol. 169, 1917-1932.
29. Liu, Y., and Bassham, D. C. (2012). Autophagy: pathways for self-eating in plant cells. Annu. Rev. Plant Biol. 63, 215-237. doi: 10.1146/annurev-arplant-042811-105441
30. 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. doi: 10.1105/tpc.112.101535
31. 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. doi: 10.1016/j.devcel.2013.05.024
32. Mari, M., Griffith, J., Rieter, E., Krishnappa, L., Klionsky, D. J., and Reggiori, F. (2010). An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J. Cell Biol. 190, 1005-1022. doi: 10.1083/jcb.200912089
33. Martinez, D. E., Costa, M. L., Gomez, F. M., Otegui, M. S., and Guiamet, J. J. (2008). ‘Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves. Plant J. 56, 196-206. doi: 10.1111/j.1365-313X.2008.03585.x
34. Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N. T., Izumi, T., et al. (2010). Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190, 511-521. doi: 10.1083/jcb.200911141
35. Michaeli, S., and Galili, G. (2014). Degradation of organelles or specific organelle components via selective autophagy in plant cells. Int. J. Mol. Sci. 15, 7624-7638.
36. Michaeli, S., Honig, A., Levanony, H., Peled-Zehavi, H., and Galili, G. (2014). Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagydependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26, 4084-4101. doi: 10.1105/tpc.114.129999
37. Minamikawa, T., Toyooka, K., Okamoto, T., Hara-Nishimura, I., and Nishimura, M. (2001). Degradation of ribulose-bisphosphate carboxylase by vacuolar enzymes of senescing French bean leaves: immunocytochemical and ultrastructural observations. Protoplasma 218, 144-153. doi: 10.1007/BF01306604
38. Mitsuhashi, N., Shimada, T., Mano, S., Nishimura, M., and Hara-Nishimura, I. (2000). Characterization of organelles in the vacuolar-sorting pathway by visualization with GFP in tobacco BY-2 cells. Plant Cell Physiol. 41, 993-1001. doi: 10.1093/pcp/pcd040
39. Mizushima, N., and Komatsu, M. (2011). Autophagy: renovation of cells and tissues. Cell 147, 728-741. doi: 10.1016/j.cell.2011.10.026
40. Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011). The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132. doi: 10.1146/annurev-cellbio-092910-154005
41. Mueller, S. J., and Reski, R. (2015). Mitochondrial dynamics and the ER: the plant perspective. Front. Cell Dev. Biol. 3: 78. doi: 10.3389/fcell.2015.00078
42. Munch, D., Teh, O. K.,Malinovsky, F. G., Liu, Q., Vetukuri, R. R., El Kasmi, F., et al. (2015). Retromer contributes to immunity-associated cell death in Arabidopsis. Plant Cell 27, 463-479. doi: 10.1105/tpc.114.132043
43. Oliviusson, P., Heinzerling, O., Hillmer, S., Hinz, G., Tse, Y. C., Jiang, L., et al. (2006). Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18, 1239-1252. doi: 10.1105/tpc.105.035907
44. Orsi, A., Razi, M., Dooley, H. C., Robinson, D., Weston, A. E., Collinson, L. M., et al. (2012). Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23, 1860-1873. doi: 10.1091/mbc.E11-09-0746
45. Otegui, M. S., Noh, Y. S., Martinez, D. E., Vila Petroff, M. G., Staehelin, L. A., Amasino, R. M., et al. (2005). Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41, 831-844. doi: 10.1111/j.1365-313X.2005.02346.x
46. Perez-Sancho, J., Tilsner, J., Samuels, A. L., Botella, M. A., Bayer, E. M., and Rosado, A. (2016). Stitching organelles: organization and function of specialized membrane contact sites in plants. Trends Cell Biol. 26, 705-717. doi: 10.1016/j.tcb.2016.05.007
47. Phillips, M. J., and Voeltz, G. K. (2016). Structure and function of ER membrane contact sites with other organelles. Nat. Rev. Mol. Cell Biol. 17, 69-82. doi: 10.1038/nrm.2015.8
48. Popovic, D., and Dikic, I. (2014). TBC1D5 and the AP2 complex regulate ATG9 trafficking and initiation of autophagy. EMBO Rep. 15, 392-401. doi: 10.1002/embr.201337995
49. Puri, C., Renna, M., Bento, C. F., Moreau, K., and Rubinsztein, D. C. (2013). Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154, 1285-1299. doi: 10.1016/j.cell.2013.08.044
50. Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C., and Rubinsztein, D. C. (2010). Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12, 747-757. doi: 10.1038/ncb1010-1021c
51. Razi, M., Chan, E. Y., and Tooze, S. A. (2009). Early endosomes and endosomal coatomer are required for autophagy. J. Cell Biol. 185, 305-321. doi: 10.1083/jcb.200810098
52. Sakuraba, Y., Lee, S. H., Kim, Y. S., Park, O. K., Hortensteiner, S., and Paek, N. C. (2014). Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. J. Exp. Bot. 65, 3915-3925. doi: 10.1093/jxb/eru008
53. Schattat, M., Barton, K., Baudisch, B., Klosgen, R. B., and Mathur, J. (2011). Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol. 155, 1667-1677. doi: 10.1104/pp.110.170480
54. Shin, K. D., Lee, H. N., and Chung, T. (2014). A revised assay for monitoring autophagic flux in Arabidopsis thaliana reveals involvement of AUTOPHAGY-RELATED9 in autophagy. Mol. Cells 37, 399-405. doi: 10.14348/molcells.2014.0042
55. Spitzer, C., Li, F., Buono, R., Roschzttardtz, H., Chung, T., Zhang, M., et al. (2015). The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 27, 391-402. doi: 10.1105/tpc.114.135939
56. Surpin, M., Zheng, H., Morita, M. T., Saito, C., Avila, E., Blakeslee, J. J., 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. doi: 10.1105/tpc.016121
57. Veljanovski, V., and Batoko, H. (2014). Selective autophagy of non-ubiquitylated targets in plants: looking for cognate receptor/adaptor proteins. Front. Plant Sci. 5: 308. doi: 10.3389/fpls.2014.00308
58. Voss, C., Lahiri, S., Young, B. P., Loewen, C. J., and Prinz, W. A. (2012). ERshaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae. J. Cell Sci. 125, 4791-4799. doi: 10.1242/jcs.105635
59. Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., et al. (2009). Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 149, 885-893. doi: 10.1104/pp.108.130013
60. Wang, J., Ding, Y., Wang, J., Hillmer, S., Miao, Y., Lo, S. W., et al. (2010). EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22, 4009-4030. doi: 10.1105/tpc.110.080697
61. Wang, P., Richardson, C., Hawkins, T. J., Sparkes, I., Hawes, C., and Hussey, P. J. (2016). Plant VAP27 proteins: domain characterization, intracellular localization and role in plant development. New Phytol. 210, 1311-1326. doi: 10.1111/nph.13857
62. Wang, S., and Blumwald, E. (2014). Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell 26, 4875-4888. doi: 10.1105/tpc.114.133116
63. Wang, Y., Yu, B. J., Zhao, J. P., Guo, J. B., Li, Y., Han, S. J., et al. (2013). Autophagy contributes to leaf starch degradation. Plant Cell 25, 1383-1399. doi: 10.1105/tpc.112.108993
64. Wang, Z., Xu, C., and Benning, C. (2012). TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 70, 614-623. doi: 10.1111/j.1365-313X.2012.04900.x
65. Wittenbach, V. A., Lin, W., and Hebert, R. R. (1982). Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiol. 69, 98-102. doi: 10.1104/pp.69.1.98
66. Wu, W. X., Lin, C. X., Wu, K., Jiang, L., Wang, X. J., Li, W., et al. (2016). FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. EMBO J. 35, 1368-1384. doi: 10.15252/embj.201593102
67. Xie, Q. J., Michaeli, S., Peled-Zehavi, N., and Galili, G. (2015). Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci. 20, 264-265. doi: 10.1016/j.tplants.2015.03.013
68. Yamamoto, H., Kakuta, S., Watanabe, T. M., Kitamura, A., Sekito, T., Kondo-Kakuta, C., et al. (2012). Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J. Cell Biol. 198, 219-233. doi: 10.1083/jcb.201202061
69. Yang, J. Y., and Yang, W. Y. (2013). Bit-by-bit autophagic removal of parkinlabelled mitochondria. Nat. Commun. 4: 2428. doi: 10.1038/ncomms3428
70. Yang, X., Srivastava, R., Howell, S. H., and Bassham, D. C. (2016). Activation of autophagy by unfolded proteins during endoplasmic reticulum stress. Plant J. 85, 83-95. doi: 10.1111/tpj.13091
71. Zavodszky, E., Seaman, M. N., Moreau, K., Jimenez-Sanchez, M., Breusegem, S. Y., Harbour, M. E., et al. (2014). Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat. Commun. 5: 3828. doi: 10.1038/ncomms4828
72. Zeng, Y., Chung, K. P., Li, B., Lai, C. M., Lam, S. K., Wang, X., et al. (2015). Unique COPII component AtSar1a/AtSec23a pair is required for the distinct function of protein ER export in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 112, 14360-14365. doi: 10.1073/pnas.1519333112
73. Zheng, W., Zhou, J., He, Y., Xie, Q., Chen, A., Zheng, H., et al. (2015). Retromer is essential for autophagy-dependent plant infection by the rice blast fungus. PLoS Genet. 11: e1005704. doi: 10.1371/journal.pgen.1005704
74. Zhuang, X., Cui, Y., Gao, C., and Jiang, L. (2015). Endocytic and autophagic pathways crosstalk in plants. Curr. Opin. Plant Biol. 28, 39-47. doi: 10.1016/j.pbi.2015.08.010
75. Zhuang, X., and Jiang, L. (2014). Autophagosome biogenesis in plants: roles of SH3P2. Autophagy 10, 704-705. doi: 10.4161/auto.28060
76. Zhuang, X., Wang, H., Lam, S. K., Gao, C., Wang, X., Cai, Y., et al. (2013). A BARdomain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25, 4596-4615. doi: 10.1105/tpc.113.118307