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
- Aubert S., Gout E., Bligny R., Marty-Mazars D., Barrieu F., Alabouvette J., Marty F., Douce R. 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. 1996;133:1251–1263. doi: 10.1083/jcb.133.6.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Avin-Wittenberg T., Honig A., Galili G. Variations on a theme: plant autophagy in comparison to yeast and mammals. Protoplasma. 2011;248:439–446. doi: 10.1007/s00709-010-0205-x. [DOI] [PubMed] [Google Scholar]
- Barth H., Meiling-Wesse K., Epple U.D., Thumm M. Autophagy and the cytoplasm to vacuole targeting pathway both require Aut10p. FEBS Lett. 2001;508:23–28. doi: 10.1016/S0014-5793(01)03016-2. [DOI] [PubMed] [Google Scholar]
- Bassham D.C., Laporte M., Marty F., Moriyasu Y., Ohsumi Y., Olsen L.J., Yoshimoto K. Autophagy in development and stress responses of plants. Autophagy. 2006;2:2–11. doi: 10.4161/auto.2092. [DOI] [PubMed] [Google Scholar]
- Chen Y., Azad M.B., Gibson S.B. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ. 2009;16:1040–1052. doi: 10.1038/cdd.2009.49. [DOI] [PubMed] [Google Scholar]
- Chung T., Suttangkakul A., Vierstra R.D. 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. 2009;149:220–234. doi: 10.1104/pp.108.126714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanaoka H., Noda T., Shirano Y., Kato T., Hayashi H., Shibata D., Tabata S., Ohsumi Y. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 2002;129:1181–1193. doi: 10.1104/pp.011024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hayward A.P., Dinesh-Kumar S.P. What can plant autophagy do for an innate immune response? Annu Rev Phytopathol. 2011;49:557–576. doi: 10.1146/annurev-phyto-072910-095333. [DOI] [PubMed] [Google Scholar]
- He C., Levine B. The Beclin 1 interactome. Curr Opin Cell Biol. 2010;22:140–149. doi: 10.1016/j.ceb.2010.01.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hofius D., Schultz-Larsen T., Joensen J., Tsitsigiannis D.I., Petersen N.H., Mattsson O., Jørgensen L.B., Jones J.D., Mundy J., Petersen M. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell. 2009;137:773–783. doi: 10.1016/j.cell.2009.02.036. [DOI] [PubMed] [Google Scholar]
- Ichimura Y., Kirisako T., Takao T., Satomi Y., Shimonishi Y., Ishihara N., Mizushima N., Tanida I., Kominami E., Ohsumi M., et al. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408:488–492. doi: 10.1038/35044114. [DOI] [PubMed] [Google Scholar]
- Ishida H., Yoshimoto K., Izumi M., Reisen D., Yano Y., Makino A., Ohsumi Y., Hanson M.R., Mae T. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 2008;148:142–155. doi: 10.1104/pp.108.122770. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell. 2009;17:98–109. doi: 10.1016/j.devcel.2009.06.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klionsky D.J. The molecular machinery of autophagy: unanswered questions. J Cell Sci. 2005;118:7–18. doi: 10.1242/jcs.01620. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8:931–937. doi: 10.1038/nrm2245. [DOI] [PubMed] [Google Scholar]
- 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., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell. 2003;5:539–545. doi: 10.1016/S1534-5807(03)00296-X. [DOI] [PubMed] [Google Scholar]
- Klionsky D.J., Ohsumi Y. Vacuolar import of proteins and organelles from the cytoplasm. Annu Rev Cell Dev Biol. 1999;15:1–32. doi: 10.1146/annurev.cellbio.15.1.1. [DOI] [PubMed] [Google Scholar]
- Kroemer G., Mariño G., Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–293. doi: 10.1016/j.molcel.2010.09.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kwon S.I., Cho H.J., Jung J.H., Yoshimoto K., Shirasu K., Park O.K. The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J. 2010;64:151–164. doi: 10.1111/j.1365-313X.2010.04315.x. [DOI] [PubMed] [Google Scholar]
- Lai Z., Wang F., Zheng Z., Fan B., Chen Z. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J. 2011;66:953–968. doi: 10.1111/j.1365-313X.2011.04553.x. [DOI] [PubMed] [Google Scholar]
- Lenz H.D., Haller E., Melzer E., Kober K., Wurster K., Stahl M., Bassham D.C., Vierstra R.D., Parker J.E., Bautor J., et al. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 2011;66:818–830. doi: 10.1111/j.1365-313X.2011.04546.x. [DOI] [PubMed] [Google Scholar]
- Liu Y., Bassham D.C. TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One. 2010;5:e11883. doi: 10.1371/journal.pone.0011883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu Y., Schiff M., Czymmek K., Tallóczy Z., Levine B., Dinesh-Kumar S.P. Autophagy regulates programmed cell death during the plant innate immune response. Cell. 2005;121:567–577. doi: 10.1016/j.cell.2005.03.007. [DOI] [PubMed] [Google Scholar]
- Liu Y., Xiong Y., Bassham D.C. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy. 2009;5:954–963. doi: 10.4161/auto.5.7.9290. [DOI] [PubMed] [Google Scholar]
- Meijer W.H., van der Klei I.J., Veenhuis M., Kiel J.A. 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. 2007;3:106–116. doi: 10.4161/auto.3595. [DOI] [PubMed] [Google Scholar]
- Menand B., Desnos T., Nussaume L., Berger F., Bouchez D., Meyer C., Robaglia C. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci U S A. 2002;99:6422–6427. doi: 10.1073/pnas.092141899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menzies F.M., Moreau K., Rubinsztein D.C. Protein misfolding disorders and macroautophagy. Curr Opin Cell Biol. 2011;23:190–197. doi: 10.1016/j.ceb.2010.10.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakatogawa H., Suzuki K., Kamada Y., Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467. doi: 10.1038/nrm2708. [DOI] [PubMed] [Google Scholar]
- Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:249–279. doi: 10.1146/annurev.arplant.49.1.249. [DOI] [PubMed] [Google Scholar]
- Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell. 2009;17:87–97. doi: 10.1016/j.devcel.2009.06.013. [DOI] [PubMed] [Google Scholar]
- Patel S., Dinesh-Kumar S.P. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy. 2008;4:20–27. doi: 10.4161/auto.5056. [DOI] [PubMed] [Google Scholar]
- Rose T.L., Bonneau L., Der C., Marty-Mazars D., Marty F. Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell. 2006;98:53–67. doi: 10.1042/BC20040516. [DOI] [PubMed] [Google Scholar]
- Scherz-Shouval R., Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36:30–38. doi: 10.1016/j.tibs.2010.07.007. [DOI] [PubMed] [Google Scholar]
- Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007;26:1749–1760. doi: 10.1038/sj.emboj.7601623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seay M., Hayward A.P., Tsao J., Dinesh-Kumar S.P. Something Old, Something New: Plant Innate Immunity and Autophagy. In: Levine B., Yoshimori T., Deretic V., editors. Autophagy in Infection and Immunity. Berlin Heidelberg: Springer; 2009. pp. 287–306. [Google Scholar]
- Shin J.H., Yoshimoto K., Ohsumi Y., Jeon J.S., An G. OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Mol Cells. 2009;27:67–74. doi: 10.1007/s10059-009-0006-2. [DOI] [PubMed] [Google Scholar]
- Slavikova S., Ufaz S., Avin-Wittenberg T., Levanony H., Galili G. An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot. 2008;59:4029–4043. doi: 10.1093/jxb/ern244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su W., Ma H., Liu C., Wu J., Yang J. Identification and characterization of two rice autophagy associated genes, OsAtg8 and OsAtg4. Mol Biol Rep. 2006;33:273–278. doi: 10.1007/s11033-006-9011-0. [DOI] [PubMed] [Google Scholar]
- Thompson A.R., Vierstra R.D. Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol. 2005;8:165–173. doi: 10.1016/j.pbi.2005.01.013. [DOI] [PubMed] [Google Scholar]
- Tsugane K., Kobayashi K., Niwa Y., Ohba Y., Wada K., Kobayashi H. A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell. 1999;11:1195–1206. doi: 10.1105/tpc.11.7.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. [DOI] [PubMed]
- Wang Y., Wu Y., Tang D. The autophagy gene, ATG18a, plays a negative role in powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant Signal Behav. 2011;6:1408–1410. doi: 10.4161/psb.6.9.16967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. [DOI] [PMC free article] [PubMed]
- Xie Z., Klionsky D.J. Autophagosome formation: core machinery and adaptations. Nat Cell Biol. 2007;9:1102–1109. doi: 10.1038/ncb1007-1102. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Contento A.L., Bassham D.C. Disruption of autophagy results in constitutive oxidative stress in Arabidopsis. Autophagy. 2007;3:257–258. doi: 10.4161/auto.3847. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Contento A.L., Nguyen P.Q., Bassham D.C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 2007;143:291–299. doi: 10.1104/pp.106.092106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshimoto K., Hanaoka H., Sato S., Kato T., Tabata S., Noda T., Ohsumi Y. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell. 2004;16:2967–2983. doi: 10.1105/tpc.104.025395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshimoto K., Jikumaru Y., Kamiya Y., Kusano M., Consonni C., Panstruga R., Ohsumi Y., Shirasu K. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009;21:2914–2927. doi: 10.1105/tpc.109.068635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu J.K. Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol. 2001;4:401–406. doi: 10.1016/S1369-5266(00)00192-8. [DOI] [PubMed] [Google Scholar]