Role of plant autophagy in stress response

Abstract

Autophagy is a conserved pathway for the bulk degradation of cytoplasmic components in all eukaryotes. This process plays a critical role in the adaptation of plants to drastic changing environmental stresses such as starvation, oxidative stress, drought, salt, and pathogen invasion. This paper summarizes the current knowledge about the mechanism and roles of plant autophagy in various plant stress responses.

Keywords

plant autophagy / stress response / drought and salt stress / pathogen

References

[1] Aubert, S., Gout, E., Bligny, R., Marty-Mazars, D., Barrieu, F., Alabouvette, J., Marty, F., and Douce, R. (1996). Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133, 1251-1263 8682862.
[2] Avin-Wittenberg, T., Honig, A., and Galili, G. (2011). Variations on a theme: plant autophagy in comparison to yeast and mammals. Protoplasma 248, 439-446 20830494.
[3] Barth, H., Meiling-Wesse, K., Epple, U.D., and Thumm, M. (2001). Autophagy and the cytoplasm to vacuole targeting pathway both require Aut10p. FEBS Lett 508, 23-28 11707261.
[4] Bassham, D.C., Laporte, M., Marty, F., Moriyasu, Y., Ohsumi, Y., Olsen, L.J., and Yoshimoto, K. (2006). Autophagy in development and stress responses of plants. Autophagy 2, 2-11 16874030.
[5] Chen, Y., Azad, M.B., and Gibson, S.B. (2009). Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 16, 1040-1052 19407826.
[6] 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 18790996.
[7] 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 12114572.
[8] 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 21370973.
[9] He, C., and Levine, B. (2010). The Beclin 1 interactome. Curr Opin Cell Biol 22, 140-149 20097051.
[10] Hofius, D., Schultz-Larsen, T., Joensen, J., Tsitsigiannis, D.I., Petersen, N.H., Mattsson, O., J?rgensen, L.B., Jones, J.D., Mundy, J., and Petersen, M. (2009). Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137, 773-783 19450522.
[11] Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., (2000). A ubiquitin-like system mediates protein lipidation. Nature 408, 488-492 11100732.
[12] 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 18614709.
[13] 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 19619495.
[14] Klionsky, D.J. (2005). The molecular machinery of autophagy: unanswered questions. J Cell Sci 118, 7-18 15615779.
[15] Klionsky, D.J. (2007). Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8, 931-937 17712358.
[16] Klionsky, D.J., Cregg, J.M., Dunn, W.A. Jr, Emr, S.D., Sakai, Y., Sandoval, I.V., Sibirny, A., Subramani, S., Thumm, M., Veenhuis, M., (2003). A unified nomenclature for yeast autophagy-related genes. Dev Cell 5, 539-545 14536056.
[17] Klionsky, D.J., and Ohsumi, Y. (1999). Vacuolar import of proteins and organelles from the cytoplasm. Annu Rev Cell Dev Biol 15, 1-32 10611955.
[18] Kroemer, G., Mari?o, G., and Levine, B. (2010). Autophagy and the integrated stress response. Mol Cell 40, 280-293 20965422.
[19] Kwon, S.I., Cho, H.J., Jung, J.H., Yoshimoto, K., Shirasu, K., and Park, O.K. (2010). The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J 64, 151-164 20659276.
[20] Lai, Z., Wang, F., Zheng, Z., Fan, B., and Chen, Z. (2011). A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66, 953-968 21395886.
[21] Lenz, H.D., Haller, E., Melzer, E., Kober, K., Wurster, K., Stahl, M., Bassham, D.C., Vierstra, R.D., Parker, J.E., Bautor, J., (2011). Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66, 818-830 21332848.
[22] Liu, Y., and Bassham, D.C. (2010). TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 5, e1188320686696.
[23] Liu, Y., Schiff, M., Czymmek, K., Tallóczy, Z., Levine, B., and Dinesh-Kumar, S.P. (2005). Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567-577 15907470.
[24] Liu, Y., Xiong, Y., and Bassham, D.C. (2009). Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5, 954-963 19587533.
[25] 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 17204848.
[26] Menand, B., Desnos, T., Nussaume, L., Berger, F., Bouchez, D., Meyer, C., and Robaglia, C. (2002). Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci U S A 99, 6422-6427 11983923.
[27] Menzies, F.M., Moreau, K., and Rubinsztein, D.C. (2011). Protein misfolding disorders and macroautophagy. Curr Opin Cell Biol 23, 190-197 21087849.
[28] Nakatogawa, H., Suzuki, K., Kamada, Y., and Ohsumi, Y. (2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10, 458-467 19491929.
[29] Noctor, G., and Foyer, C.H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49, 249-279 15012235.
[30] 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 19619494.
[31] Patel, S., and Dinesh-Kumar, S.P. (2008). Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4, 20-27 17932459.
[32] Rose, T.L., Bonneau, L., Der, C., Marty-Mazars, D., and Marty, F. (2006). Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell 98, 53-67 16354162.
[33] Scherz-Shouval, R., and Elazar, Z. (2011). Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36, 30-38 20728362.
[34] Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., and Elazar, Z. (2007). Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26, 1749-1760 17347651.
[35] Seay, M., Hayward, A.P., Tsao, J., and Dinesh-Kumar, S.P. (2009). Something Old, Something New: Plant Innate Immunity and Autophagy. In: Autophagy in Infection and Immunity . Levine B, Yoshimori T, and Deretic V, eds. Berlin Heidelberg: Springer. 287-306 .
[36] Shin, J.H., Yoshimoto, K., Ohsumi, Y., Jeon, J.S., and An, G. (2009). OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Mol Cells 27, 67-74 19214435.
[37] Slavikova, S., Ufaz, S., Avin-Wittenberg, T., Levanony, H., and Galili, G. (2008). An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot 59, 4029-4043 18836138.
[38] Su, W., Ma, H., Liu, C., Wu, J., and Yang, J. (2006). Identification and characterization of two rice autophagy associated genes, OsAtg8 and OsAtg4. Mol Biol Rep 33, 273-278 17082902.
[39] Thompson, A.R., and Vierstra, R.D. (2005). Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8, 165-173 15752997.
[40] Tsugane, K., Kobayashi, K., Niwa, Y., Ohba, Y., Wada, K., and Kobayashi, H. (1999). A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11, 1195-1206 10402422.
[41] Wang, Y., Nishimura, M.T., Zhao, T., and Tang, D. (2011a). ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J 10.1111/j.1365-1313X.2011.04669.x21645148.
[42] Wang, Y., Wu, Y., and Tang, D. (2011b). The autophagy gene, ATG18a, plays a negative role in powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant Signal Behav 6, 1408-1410 21847024.
[43] Xia, K., Liu, T., Ouyang, J., Wang, R., Fan, T., and Zhang, M. (2011). Genome-Wide Identification, Classification, and Expression Analysis of Autophagy-Associated Gene Homologues in Rice (Oryza sativa L.). DNA Res 10.1093/dnares/dsr102421795261.
[44] Xie, Z., and Klionsky, D.J. (2007). Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9, 1102-1109 17909521.
[45] Xiong, Y., Contento, A.L., and Bassham, D.C. (2007a). Disruption of autophagy results in constitutive oxidative stress in Arabidopsis. Autophagy 3, 257-258 17312382.
[46] Xiong, Y., Contento, A.L., Nguyen, P.Q., and Bassham, D.C. (2007b). Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143, 291-299 17098847.
[47] 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 15494556.
[48] Yoshimoto, K., Jikumaru, Y., Kamiya, Y., Kusano, M., Consonni, C., Panstruga, R., Ohsumi, Y., and 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 19773385.
[49] Zhu, J.K. (2001). Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4, 401-406 11597497.