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Autophagy in plants

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Abstract

Autophagy is a highly conserved processing mechanism in eukaryotes whereby cytoplasmic components are engulfed in double-membrane vesicles called autophagosomes and are delivered into organelles such as lysosomes (mammal) or vacuoles (yeast/plant) for degradation and recycling of the resulting molecules. Isolation of yeastAUTOPHAGY (ATG) genes has facilitated the identification of correspondingArabidopsis ATG genes based on sequence similarity. Genetic and molecular analyses using knockout and/or knockdown mutants of those genes have unraveled the biological functions of autophagy during plant development, nutrient recycling, and environmental stress responses. Additional roles for autophagy have been suggested in the degradation of oxidized proteins during oxidative stress and the regulation of hypersensitive response (HR)-programmed cell death (PCD) during innate immunity. Our review summarizes knowledge about the structure and function of autophagic pathways andATG components, and the biological roles of autophagy in plants.

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Literature cited

  • Aubert S, Gout E, Bligny R, MartyMazars D, Barrieu F, Alabouvette J, Marty F, 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

    Article  PubMed  CAS  Google Scholar 

  • Baehrecke EH (2005) Autophagy: dual roles in life and death? Nat Rev Mol Cell 6: 505–510

    Article  CAS  Google Scholar 

  • Bassham DC (2007) Plant autophagy-more than a starvation response. Curr Opin Plant Biol 10: 587–593

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2:2–11

    PubMed  CAS  Google Scholar 

  • Bursch W (2001) The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 8: 569–581

    Article  PubMed  CAS  Google Scholar 

  • Chen MH, Liu LF, Chen YR, Wu HK, Yu SM (1994) Expression of áamylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J 6: 625–636

    Article  PubMed  CAS  Google Scholar 

  • Contento AL, Kim SJ, Bassham DC (2004) Transcription profiling of the response ofArabidopsis suspension culture cells to Suc starvation. Plant Physiol 135: 2330–2347

    Article  PubMed  CAS  Google Scholar 

  • Contento AL, XiongY, Bassham DC (2005) Visualization of autophagy inArabidopsis using the fluorescent dye monodansylca-daverine and a GFP-AtATG8e fusion protein. Plant J 42: 598–608

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826–833

    Article  PubMed  CAS  Google Scholar 

  • DoellingJH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence inArabidopsis thaliana. J Biol Chem 277: 33105–33114

    Article  Google Scholar 

  • Ellis C, Turner JG, Devoto A (2002) Protein complexes mediate signaling in plant responses to hormones, light, sucrose, and pathogens. Plant Mol Biol 50: 971–980

    Article  PubMed  CAS  Google Scholar 

  • Fujiki Y, Yoshimoto K, Ohsumi Y (2007) AnArabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol 143: 1132–1139

    Article  PubMed  CAS  Google Scholar 

  • Fujioka Y, Noda NN, Fujii K, Yoshimoto K, Ohsumi Y, Inagaki F (2008) In vitro reconstitution of plant Atg8 and Atg12 conjugation systems essential for autophagy. J Biol Chem 283: 1921–1928

    Article  PubMed  CAS  Google Scholar 

  • Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5: 379–391

    Article  PubMed  CAS  Google Scholar 

  • Gozuacik D, Kimchi A (2007) Autophagy and cell death. Curr Top Dev Biol 78: 217–245

    Article  PubMed  CAS  Google Scholar 

  • Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y, (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282: 37298–37302

    Article  PubMed  CAS  Google Scholar 

  • Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of anArabidopsis autophagy gene. Plant Physiol 129: 1181 -1193

    Article  PubMed  CAS  Google Scholar 

  • Harding TM, Morano KA, Scott SV, Klionsky DJ (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131: 591–602

    Article  PubMed  CAS  Google Scholar 

  • Harding TM, Hefner-Gravink A, Thumm M, Klionsky DJ (1996) Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J Biol Chem 271: 17621–17624

    Article  PubMed  CAS  Google Scholar 

  • Harrison-Lowe NJ, Olsen LJ (2008) Autophagy protein 6 (ATG6) is required for pollen germination inArabidopsis thaliana. Autophagy 4: 339–348

    CAS  Google Scholar 

  • Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408: 488–492

    Article  PubMed  CAS  Google Scholar 

  • Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y (2006) AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy inArabidopsis root tip cells. Plant Cell Physiol 47: 1641–1652

    Article  PubMed  CAS  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323–329

    Article  PubMed  CAS  Google Scholar 

  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720–5728

    Article  PubMed  CAS  Google Scholar 

  • Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150: 1507–1513

    Article  PubMed  CAS  Google Scholar 

  • Kang C, You Y, Avery L (2007) Dual roles of autophagy in the survival ofCaenorhabditis elegans during starvation. Genes Dev 21: 2161–2171

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ (2005) The molecular machinery of autophagy: Unanswered questions. J Cell Sci 118: 7–18

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ (2007) Autophagy; from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931–937

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ etal. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151–175

    PubMed  CAS  Google Scholar 

  • KumaA, Mizushima N, Ishihara N, Ohsumi Y (2002) Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem 277: 18619–18625

    Article  Google Scholar 

  • Lamb E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848–853

    Article  Google Scholar 

  • Levine B, Klionsky DJ (2004) Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 6: 463–477

    Article  PubMed  CAS  Google Scholar 

  • Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132: 27–42

    Article  PubMed  CAS  Google Scholar 

  • Levine B, Yuan J (2005) Autophagy in cell death: An innocent convict? J Clin Invest 115: 2679–2688

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121: 567–577

    Article  PubMed  CAS  Google Scholar 

  • Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8: 741–752

    Article  PubMed  CAS  Google Scholar 

  • Massey AC, Zhang C, Cuervo AM (2006) Chaperone-mediated autophagy in aging and disease. Curr Top Dev Biol 73: 205–235

    Article  PubMed  CAS  Google Scholar 

  • Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of theArabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99: 6422–6427

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498

    Article  PubMed  CAS  Google Scholar 

  • Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873

    Article  PubMed  CAS  Google Scholar 

  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451: 1069–1075

    Article  PubMed  CAS  Google Scholar 

  • Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395: 395–398

    Article  PubMed  CAS  Google Scholar 

  • Moriyasu Y, Hattori M, Jauh GY, Rogers JC (2003) Alpha tonoplast intrinsic protein is specifically associated with vacuole membrane involved in an autophagic process. Plant Cell Physiol 44: 795–802

    Article  PubMed  CAS  Google Scholar 

  • Moriyasu Y, Ohsumi Y (1996) Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiol 111: 1233–1241

    PubMed  CAS  Google Scholar 

  • Mukaiyama H, Oku M, Baba M, Samizo T, Hammond AT, Glick BS, Kato N, Sakai Y (2002) Paz2 and 13 otherPAZ gene products regulate vacuolar engulfment of peroxisomes during micropexophagy. Genes Cells 7: 75–90

    Article  PubMed  CAS  Google Scholar 

  • Nair U, Klionsky DJ (2005) Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast. J Biol Chem 280: 41785–41788

    Article  PubMed  CAS  Google Scholar 

  • Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a Ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130: 165–178

    Article  PubMed  CAS  Google Scholar 

  • Ogawa M, Sasakawa C (2006) Bacterial evasion of the autophagic defense system. Curr Opin Microbiol 9: 62–68

    Article  PubMed  CAS  Google Scholar 

  • Ohsumi Y (2001) Molecular dissection of autophagy: Two ubiquitin-like systems. Nat Rev Mol Cell Biol 2: 211–216

    Article  PubMed  CAS  Google Scholar 

  • Patel S, Caplan J, Dinesh-Kumar SP (2006) Autophagy in the control of programmed cell death. Curr Opin Plant Biol 9: 391–396

    Article  PubMed  CAS  Google Scholar 

  • Patel S, Dinesh-Kumar SP (2008)Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4: 20–27

    PubMed  CAS  Google Scholar 

  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927–939

    Article  PubMed  CAS  Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death. Plant Cell 9: 1157–1168

    Article  PubMed  CAS  Google Scholar 

  • Phillips BA, Suttangkakul A, Vierstra RD (2008) The ATG12 conjugating enzyme ATG10 is essential for autophagic vesicle formation inArabidopsis thaliana. Genetics 178: 1339–1353

    Article  PubMed  CAS  Google Scholar 

  • Qin G, Ma Z, Zhang L, Xing S, Hou X, Deng J, Liu J, Chen Z, Qu LJ, Gu H (2007)Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development. Cell Res 17: 249–263

    PubMed  CAS  Google Scholar 

  • Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F (2006) Starvation-induced expression of autophagy-related genes inArabidopsis. Biol Cell 98: 53–67

    Article  PubMed  CAS  Google Scholar 

  • Sakai Y, Koller A, Rangell LK, Keller GA, Subramani S (1998) Peroxisome degradation by microautophagy inPichia pastoris: identification of specific steps and morphological intermediates. J Cell Biol 141: 625–636

    Article  PubMed  CAS  Google Scholar 

  • Sanmartin M, Ordonez A, Sohn EJ, Robert S, Sanchez-Serrano JJ, Surpin MA, Raikhel NV, Rojo E (2007) Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles inArabidopsis. Proc Natl Acad Sci USA 104: 3645–3650

    Article  PubMed  CAS  Google Scholar 

  • Scherz-Shouval R, Elazar Z (2007) ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 17: 422–427

    Article  PubMed  CAS  Google Scholar 

  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749–1760

    Article  PubMed  CAS  Google Scholar 

  • Schmelzle T, Hall MN (2000) TOR, a central controller of cell growth. Cell 103: 253–262

    Article  PubMed  CAS  Google Scholar 

  • Scott RC, Juhasz G, Neufeld TP (2007) Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 17: 1–11

    Article  PubMed  CAS  Google Scholar 

  • Seay MD, Dinesh-Kumar SP (2005) Life after death: are autophagy genes involved in cell death and survival during plant innate immune responses? Autophagy 1: 185–186

    PubMed  Google Scholar 

  • Seay MD, Patel S, Dinesh-Kumar SP (2006) Autophagy and plant innate immunity. Cellular Microbiology 8: 899–906

    Article  PubMed  CAS  Google Scholar 

  • Slavikova S, Shy G, Yao YL, Giozman R, Levanony H, Pietrokovski S, Elazar Z, Galili G (2005) The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses inArabidopsis plants. J Exp Bot 56: 2839–2849

    Article  PubMed  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55: 555–590

    Article  PubMed  CAS  Google Scholar 

  • Su W, Ma H, Liu C, Wu J, Yang J (2006) Identification and characterization of two rice autophagy associated genes, OsAtg8 and OsAtg4. Mol Biol Rep 33: 273–278

    Article  PubMed  CAS  Google Scholar 

  • Surpin M, Zheng H, Moria MT, Saito C, Avila E, Blakeslee JJ, Bandyopadhyay A, Kovaleva V, Carter D, Murphy A, Tasaka M, Raikhel N (2003) The VTI family of SNARE proteins is nessary for plant viability and mediates different protein transport pathways. Plant Cell 15: 2885–2899

    Article  PubMed  CAS  Google Scholar 

  • Suzuki NN, Yoshimoto K, Fujioka Y, Ohsumi Y, Inagaki F (2005) The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy 1: 119–126

    PubMed  CAS  Google Scholar 

  • Takatsuka C, Inoue Y, Matsuoka K, Moriyasu Y (2004) 3-Methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions. Plant Cell Physiol 45: 265–274

    Article  PubMed  CAS  Google Scholar 

  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling inArabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138: 2097–2110

    Article  PubMed  CAS  Google Scholar 

  • Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8: 165–173

    Article  PubMed  CAS  Google Scholar 

  • Thumm M, Egner R, Koch M, Schlumpberger M, Straub M, Veenhuis M, Wolf DH (1994) Isolation of autophagocytosis mutants ofSaccharomyces cerevisiae. FEBS Lett 349: 275–280

    Article  PubMed  CAS  Google Scholar 

  • Titorenko VI, Keizer I, Harder W, Veenhuis M (1995) Isolation and characterization of mutants impaired in the selective degradation of peroxisomes in the yeastHansenula polymorpha. J Bacteriol 177: 357–363

    PubMed  CAS  Google Scholar 

  • Toyooka K, Moriyasu Y, Goto Y, Takeuchi M, Fukuda H, Matsuoka K (2006) Protein aggregates are transported to vacuoles by a macroautophagic mechanism in nutrient-starved plant cells. Autophagy 2: 96–106

    PubMed  CAS  Google Scholar 

  • Toyooka K, Okamoto T, Minamikawa T (2001) Cotyledon cells ofVigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components. J Cell Biol 154: 973–982

    Article  PubMed  CAS  Google Scholar 

  • Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants ofSaccharomyces cerevisiae. FEBS Lett 333: 169–174

    Article  PubMed  CAS  Google Scholar 

  • Van der Wilden W, Herman EM, Chrispeels MJ (1980) Protein bodies of mung bean cotyledons as autophagic organelles. Proc Natl Acad Sci USA 77: 428–432

    Article  PubMed  Google Scholar 

  • Van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trends Plant Sci 10: 117–122

    PubMed  Google Scholar 

  • Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8: 135–142

    Article  PubMed  CAS  Google Scholar 

  • Wang CW, Kim J, Huang WP, Abeliovich H, Stromhaug PE, Dunn WA, Klionsky DJ (2001) Apg2 is a novel protein required for the cytoplasm to vacuole targeting, autophagy, and pexophagy. J Biol Chem 276: 30442–30451

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence inArabidopsis thaliana. Plant J 42: 535–546

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Contento AL, Bassham DC (2007a) Disruption of autophagy results in constitutive oxidative stress in Arabidopsis. Autophagy 3: 257–258

    PubMed  CAS  Google Scholar 

  • Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007b) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143: 291–299

    Article  PubMed  CAS  Google Scholar 

  • Yano K, Suzuki T, Moriyasu Y (2007) Constitutive autophagy in plant root cells. Autophagy 3: 360–362

    PubMed  CAS  Google Scholar 

  • Yoshimori T (2007) Autophagy: Paying Charon’s toll. Cell 128: 833–836

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yuan W, Tuttle DL, Shi YJ, Ralph GS, Dunn Jr. WA (1997) Glucose-induced microautophagy inPichia pastoris requires the α-sub- unit of phosphofructokinase. J Cell Sci 110: 1935–1945

    PubMed  CAS  Google Scholar 

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Correspondence to Ohkmae K. Park.

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Kwon, S.I., Park, O.K. Autophagy in plants. J. Plant Biol. 51, 313–320 (2008). https://doi.org/10.1007/BF03036132

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