To deliver or to degrade – an interplay of the ubiquitin–proteasome system, autophagy and vesicular transport in plants

FEBS Journal

Volumn , Issue , 2016, Pages 3534-3555

  Zientara Rytter, Katarzyna ^a   Sirko, Agnieszka ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

autophagy; proteasome; selective autophagy; ubiquitin; vesicular trafficking

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ANTHOCYANIN; ATG7 PROTEIN; ATG8 PROTEIN; AUTOPHAGY PROTEIN 5; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; AUTOPHAGOSOME; AUTOPHAGY; CHLOROPHAGY; ENDOPLASMIC RETICULUM STRESS; EXOCYTOSIS; HUMAN; INTRACELLULAR TRANSPORT; MICROTUBULE; MITOPHAGY; NONHUMAN; PEXOPHAGY; PLANT GROWTH; PLASTID; PRIORITY JOURNAL; RETICULOPHAGY; REVIEW; SELECTIVE AUTOPHAGY; UBIQUITIN PROTEASOME SYSTEM; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; VESICULAR TRANSPORT;

EID: 84990205354     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13712     Document Type: Review

References (195)

1. Lilienbaum A (2013) Relationship between the proteasomal system and autophagy. Int J Biochem Mol Biol 4, 1–26.
2. Hatfield PM, Gosink MM, Carpenter TB & Vierstra RD (1997) The ubiquitin-activating enzyme (E1) gene family in Arabidopsis thaliana. Plant J 11, 213–226.
3. Vierstra RD (1996) Proteolysis in plants: mechanisms and functions. Plant Mol Biol 32, 275–302.
4. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10, 385–397.
5. Mazzucotelli E, Belloni S, Marone D, De Leonardis A, Guerra D, Di Fonzo N, Cattivelli L & Mastrangelo A (2006) The e3 ubiquitin ligase gene family in plants: regulation by degradation. Curr Genomics 7, 509–522.
6. Moon J, Parry G & Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16, 3181–3195.
7. Kurepa J, Wang S, Li Y & Smalle J (2009) Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav 4, 924–927.
8. Wojcik C & DeMartino GN (2003) Intracellular localization of proteasomes. Int J Biochem Cell Biol 35, 579–589.
9. Yorimitsu T & Klionsky DJ (2005) Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol Biol Cell 16, 1593–1605.
10. Liu Y & Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63, 215–237.
11. Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53, 1355–1365.
12. Tooze SA & Yoshimori T (2010) The origin of the autophagosomal membrane. Nat Cell Biol 12, 831–835.
13. van Doorn WG & Papini A (2013) Ultrastructure of autophagy in plant cells: a review. Autophagy 9, 1922–1936.
14. Wang CW & Klionsky DJ (2003) The molecular mechanism of autophagy. Mol Med 9, 65–76.
15. Hiratsuka R & Terasaka O (2011) Pollen tube reuses intracellular components of nucellar cells undergoing programmed cell death in Pinus densiflora. Protoplasma 248, 339–351.
16. Gaffal KP, Friedrichs GJ & El-Gammal S (2007) Ultrastructural evidence for a dual function of the phloem and programmed cell death in the floral nectary of Digitalis purpurea. Ann Bot 99, 593–607.
17. Li F & Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17, 526–537.
18. Klionsky DJ (2005) Autophagy. Curr Biol 15, R282–R283.
19. 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.
20. 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 an Arabidopsis autophagy gene. Plant Physiol 129, 1181–1193.
21. Doelling JH, Walker JM, Friedman EM, Thompson AR & Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 277, 33105–33114.
22. Thompson AR, Doelling JH, Suttangkakul A & Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138, 2097–2110.
23. Seay M, Patel S & Dinesh-Kumar SP (2006) Autophagy and plant innate immunity. Cell Microbiol 8, 899–906.
24. 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.
25. Rose TL, Bonneau L, Der C, Marty-Mazars D & Marty F (2006) Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell 98, 53–67.
26. Niwa Y, Kato T, Tabata S, Seki M, Kobayashi M, Shinozaki K & Moriyasu Y (2004) Disposal of chloroplasts with abnormal function into the vacuole in Arabidopsis thaliana cotyledon cells. Protoplasma 223, 229–232.
27. Aubert S, Gout E, Bligny R, Marty-Mazars 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.
28. Xiong Y, Contento AL & Bassham DC (2007) Disruption of autophagy results in constitutive oxidative stress in Arabidopsis. Autophagy 3, 257–258.
29. Xiong Y, Contento AL, Nguyen PQ & Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143, 291–299.
30. Reumann S, Voitsekhovskaja O & Lillo C (2010) From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247, 233–256.
31. Diaz-Troya S, Perez-Perez ME, Florencio FJ & Crespo JL (2008) The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4, 851–865.
32. Yoshimoto K, Takano Y & Sakai Y (2010) Autophagy in plants and phytopathogens. FEBS Lett 584, 1350–1358.
33. Xiong Y, Contento AL & Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42, 535–546.
34. Ketelaar T, Voss C, Dimmock SA, Thumm M & Hussey PJ (2004) Arabidopsis homologues of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett 567, 302–306.
35. Kirkin V, Lamark T, Johansen T & Dikic I (2009) NBR1 cooperates with p62 in selective autophagy of ubiquitinated targets. Autophagy 5, 732–733.
36. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149–1163.
37. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G & Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282, 24131–24145.
38. Khaminets A, Behl C & Dikic I (2015) Ubiquitin-dependent and independent signals in selective autophagy. Trends Cell Biol 26, 6–16.
39. Svenning S, Lamark T, Krause K & 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.
40. Zientara-Rytter K, Lukomska J, Moniuszko G, Gwozdecki R, Surowiecki P, Lewandowska M, Liszewska F, Wawrzynska A & Sirko A (2011) Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7, 1145–1158.
41. Ohsumi Y (2014) Historical landmarks of autophagy research. Cell Res 24, 9–23.
42. Rabinowitz JD & White E (2010) Autophagy and metabolism. Science 330, 1344–1348.
43. Nakatogawa H, Suzuki K, Kamada Y & Ohsumi Y (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10, 458–467.
44. Deprost D, Truong HN, Robaglia C & Meyer C (2005) An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem Biophys Res Commun 326, 844–850.
45. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C & Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99, 6422–6427.
46. Kamada Y, Yoshino K, Kondo C, Kawamata T, Oshiro N, Yonezawa K & Ohsumi Y (2010) Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 30, 1049–1058.
47. Kamada Y (2010) Prime-numbered Atg proteins act at the primary step in autophagy: unphosphorylatable Atg13 can induce autophagy without TOR inactivation. Autophagy 6, 415–416.
48. Suttangkakul A, Li F, Chung T & Vierstra RD (2011) The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23, 3761–3779.
49. Chen Y & Klionsky DJ (2011) The regulation of autophagy – unanswered questions. J Cell Sci 124, 161–170.
50. Ahn CS, Han JA, Lee HS, Lee S & Pai HS (2011) The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23, 185–209.
51. Anderson GH, Veit B & Hanson MR (2005) The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol 3, 12.
52. Mahfouz MM, Kim S, Delauney AJ & Verma DP (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18, 477–490.
53. Moreau M, Azzopardi M, Clement G, Dobrenel T, Marchive C, Renne C, Martin-Magniette ML, Taconnat L, Renou JP, Robaglia C et al. (2012) Mutations in the Arabidopsis homolog of LST8/GbetaL, a partner of the target of Rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24, 463–481.
54. Xiong Y & Sheen J (2014) The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol 164, 499–512.
55. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C & Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8, 864–870.
56. Anderson GH & Hanson MR (2005) The Arabidopsis Mei2 homologue AML1 binds AtRaptor1B, the plant homologue of a major regulator of eukaryotic cell growth. BMC Plant Biol 5, 2.
57. Liu Y & Bassham DC (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 5, e11883.
58. Perez-Perez ME, Florencio FJ & Crespo JL (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152, 1874–1888.
59. Roach PJ (2011) AMPK -> ULK1 -> autophagy. Mol Cell Biol 31, 3082–3084.
60. Baena-Gonzalez E, Rolland F, Thevelein JM & Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942.
61. 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.
62. Hayward AP & Dinesh-Kumar SP (2011) What can plant autophagy do for an innate immune response? Annu Rev Phytopathol 49, 557–576.
63. 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.
64. 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.
65. Fujiki Y, Yoshimoto K & Ohsumi Y (2007) An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol 143, 1132–1139.
66. Patel S & Dinesh-Kumar SP (2008) Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4, 20–27.
67. Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, Bjorkoy G & 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.
68. Reggiori F, Shintani T, Nair U & Klionsky DJ (2005) Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1, 101–109.
69. Monastyrska I, He C, Geng J, Hoppe AD, Li Z & Klionsky DJ (2008) Arp2 links autophagic machinery with the actin cytoskeleton. Mol Biol Cell 19, 1962–1975.
70. He C, Song H, Yorimitsu T, Monastyrska I, Yen WL, Legakis JE & Klionsky DJ (2006) Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J Cell Biol 175, 925–935.
71. Boldogh IR, Yang HC, Nowakowski WD, Karmon SL, Hays LG, Yates JR III & Pon LA (2001) Arp2/3 complex and actin dynamics are required for actin-based mitochondrial motility in yeast. Proc Natl Acad Sci USA 98, 3162–3167.
72. Gouin E, Welch MD & Cossart P (2005) Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8, 35–45.
73. 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 in Arabidopsis root tip cells. Plant Cell Physiol 47, 1641–1652.
74. Nakatogawa H (2013) Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy. Essays Biochem 55, 39–50.
75. 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.
76. Woo J, Park E & Dinesh-Kumar SP (2014) Differential processing of Arabidopsis ubiquitin-like Atg8 autophagy proteins by Atg4 cysteine proteases. Proc Natl Acad Sci USA 111, 863–868.
77. Hanada T, Satomi Y, Takao T & Ohsumi Y (2009) The amino-terminal region of Atg3 is essential for association with phosphatidylethanolamine in Atg8 lipidation. FEBS Lett 583, 1078–1083.
78. Chung T, Suttangkakul A & Vierstra RD (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.
79. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M et al. (2000) A ubiquitin-like system mediates protein lipidation. Nature 408, 488–492.
80. Chung T, Phillips AR & Vierstra RD (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.
81. 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.
82. Kramer H (2013) Route to destruction: autophagosomes SNARE lysosomes. J Cell Biol 201, 495–497.
83. 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.
84. Phillips AR, Suttangkakul A & Vierstra RD (2008) The ATG12-conjugating enzyme ATG10 Is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178, 1339–1353.
85. Menzies FM, Moreau K & Rubinsztein DC (2011) Protein misfolding disorders and macroautophagy. Curr Opin Cell Biol 23, 190–197.
86. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, Brown SD & Rubinsztein DC (2005) Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37, 771–776.
87. Jahreiss L, Menzies FM & Rubinsztein DC (2008) The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9, 574–587.
88. Kouno T, Mizuguchi M, Tanida I, Ueno T, Kanematsu T, Mori Y, Shinoda H, Hirata M, Kominami E & Kawano K (2005) Solution structure of microtubule-associated protein light chain 3 and identification of its functional subdomains. J Biol Chem 280, 24610–24617.
89. Mann SS & Hammarback JA (1994) Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B. J Biol Chem 269, 11492–11497.
90. Fu MM, Nirschl JJ & Holzbaur EL (2014) LC3 binding to the scaffolding protein JIP1 regulates processive dynein-driven transport of autophagosomes. Dev Cell 29, 577–590.
91. Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH & Thumm M (1998) Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J 17, 3597–3607.
92. 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.
93. Pankiv S & Johansen T (2010) FYCO1: linking autophagosomes to microtubule plus end-directing molecular motors. Autophagy 6, 550–552.
94. Wywial E & Singh SM (2010) Identification and structural characterization of FYVE domain-containing proteins of Arabidopsis thaliana. BMC Plant Biol 10, 157.
95. Marchbank K, Waters S, Roberts RG, Solomon E & Whitehouse CA (2012) MAP1B interaction with the FW domain of the autophagic receptor Nbr1 facilitates its association to the microtubule network. Int J Cell Biol 2012, 208014.
96. Wang H & Olsen RW (2000) Binding of the GABA(A) receptor-associated protein (GABARAP) to microtubules and microfilaments suggests involvement of the cytoskeleton in GABARAPGABA(A) receptor interaction. J Neurochem 75, 644–655.
97. Kast DJ & Dominguez R (2015) WHAMM links actin assembly via the Arp2/3 complex to autophagy. Autophagy 11, 1702–1704.
98. Kast DJ, Zajac AL, Holzbaur EL, Ostap EM & Dominguez R (2015) WHAMM directs the Arp2/3 complex to the ER for autophagosome biogenesis through an actin comet tail mechanism. Curr Biol 25, 1791–1797.
99. Wang CW, Stromhaug PE, Shima J & Klionsky DJ (2002) The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J Biol Chem 277, 47917–47927.
100. Darsow T, Rieder SE & Emr SD (1997) A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J Cell Biol 138, 517–529.
101. Fischer von Mollard G & Stevens TH (1999) The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Mol Biol Cell 10, 1719–1732.
102. Sato TK, Darsow T & Emr SD (1998) Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking. Mol Cell Biol 18, 5308–5319.
103. Surpin M, Zheng H, Morita MT, Saito C, Avila E, Blakeslee JJ, Bandyopadhyay A, Kovaleva V, Carter D, Murphy A 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.
104. Birgisdottir AB, Lamark T & Johansen T (2013) The LIR motif - crucial for selective autophagy. J Cell Sci 126, 3237–3247.
105. Alemu EA, Lamark T, Torgersen KM, Birgisdottir AB, Larsen KB, Jain A, Olsvik H, Overvatn A, Kirkin V & 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.
106. Kraft C, Kijanska M, Kalie E, Siergiejuk E, Lee SS, Semplicio G, Stoffel I, Brezovich A, Verma M, Hansmann I et al. (2012) Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J 31, 3691–3703.
107. Nakatogawa H, Ohbayashi S, Sakoh-Nakatogawa M, Kakuta S, Suzuki SW, Kirisako H, Kondo-Kakuta C, Noda NN, Yamamoto H & 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.
108. Noda NN, Ohsumi Y & Inagaki F (2010) Atg8-family interacting motif crucial for selective autophagy. FEBS Lett 584, 1379–1385.
109. Kumeta H, Watanabe M, Nakatogawa H, Yamaguchi M, Ogura K, Adachi W, Fujioka Y, Noda NN, Ohsumi Y & Inagaki F (2010) The NMR structure of the autophagy-related protein Atg8. J Biomol NMR 47, 237–241.
110. Johansen T & Lamark T (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7, 279–296.
111. Noda NN, Kumeta H, Nakatogawa H, Satoo K, Adachi W, Ishii J, Fujioka Y, Ohsumi Y & Inagaki F (2008) Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 13, 1211–1218.
112. Ichimura Y, Kominami E, Tanaka K & Komatsu M (2008) Selective turnover of p62/A170/SQSTM1 by autophagy. Autophagy 4, 1063–1066.
113. Kalvari I, Tsompanis S, Mulakkal NC, Osgood R, Johansen T, Nezis IP & Promponas VJ (2014) iLIR: A web resource for prediction of Atg8-family interacting proteins. Autophagy 10, 913–925.
114. Floyd BE, Morriss SC, Macintosh GC & Bassham DC (2012) What to eat: evidence for selective autophagy in plants. J Integr Plant Biol 54, 907–920.
115. Lamark T, Kirkin V, Dikic I & Johansen T (2009) NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 8, 1986–1990.
116. Cha-Molstad H, Sung KS, Hwang J, Kim KA, Yu JE, Yoo YD, Jang JM, Han DH, Molstad M, Kim JG et al. (2015) Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through p62 binding. Nat Cell Biol 17, 917–929.
117. Zientara-Rytter K & Sirko A (2014) Significant role of PB1 and UBA domains in multimerization of Joka2, a selective autophagy cargo receptor from tobacco. Front Plant Sci 5, 13.
118. Vanhee C, Zapotoczny G, Masquelier D, Ghislain M & 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.
119. Vanhee C & Batoko H (2011) Arabidopsis TSPO and porphyrins metabolism: a transient signaling connection? Plant Signal Behav 6, 1383–1385.
120. Devarenne TP (2011) The plant cell death suppressor Adi3 interacts with the autophagic protein Atg8 h. Biochem Biophys Res Commun 412, 699–703.
121. Ek-Ramos MJ, Avila J, Cheng C, Martin GB & Devarenne TP (2010) The T-loop extension of the tomato protein kinase AvrPto-dependent Pto-interacting protein 3 (Adi3) directs nuclear localization for suppression of plant cell death. J Biol Chem 285, 17584–17594.
122. Bogdanove AJ & Martin GB (2000) AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc Natl Acad Sci USA 97, 8836–8840.
123. Avin-Wittenberg T, Michaeli S, Honig A & Galili G (2012) ATI1, a newly identified atg8-interacting protein, binds two different Atg8 homologs. Plant Signal Behav 7, 685–687.
124. Honig A, Avin-Wittenberg T, Ufaz S & Galili G (2012) A new type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 24, 288–303.
125. Gould KS (2004) Nature's Swiss Army Knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 2004, 314–320.
126. Pourcel L, Irani NG, Lu Y, Riedl K, Schwartz S & Grotewold E (2010) The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol Plant 3, 78–90.
127. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57, 761–780.
128. Conn S, Zhang W & Franco C (2003) Anthocyanic vacuolar inclusions (AVIs) selectively bind acylated anthocyanins in Vitis vinifera L. (grapevine) suspension culture. Biotechnol Lett 25, 835–839.
129. Marrs KA, Alfenito MR, Lloyd AM & Walbot V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375, 397–400.
130. Verweij W, Spelt C, Di Sansebastiano GP, Vermeer J, Reale L, Ferranti F, Koes R & Quattrocchio F (2008) An H+ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat Cell Biol 10, 1456–1462.
131. Chen S, Zhou L, Zhang Y, Leng Y, Pei XY, Lin H, Jones R, Orlowski RZ, Dai Y & Grant S (2014) Targeting SQSTM1/p62 induces cargo-loading failure and converts autophagy to apoptosis via NBK/Bik. Mol Cell Biol 34, 3435–3449.
132. Zhang X, Lu H, Ai H, Peng R, Yang Y, Li A, Hong H, Peng J & Liu K (2014) Distribution, cleavage and lipidation of Atg8 fusion proteins in Spodoptera litura Sl-HP cells. PLoS One 9, e96059.
133. Li F, Chung T & Vierstra RD (2014) AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 26, 788–807.
134. Ishida H, Izumi M, Wada S & Makino A (2014) Roles of autophagy in chloroplast recycling. Biochim Biophys Acta 1837, 512–521.
135. Dong J & Chen W (2013) The role of autophagy in chloroplast degradation and chlorophagy in immune defenses during Pst DC3000 (AvrRps4) infection. PLoS One 8, e73091.
136. Hayward AP, Tsao J & Dinesh-Kumar SP (2009) Autophagy and plant innate immunity: defense through degradation. Semin Cell Dev Biol 20, 1041–1047.
137. Lee TA, Vande Wetering SW & Brusslan JA (2013) Stromal protein degradation is incomplete in Arabidopsis thaliana autophagy mutants undergoing natural senescence. BMC Res Notes 6, 17.
138. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T & Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149, 885–893.
139. Izumi M, Wada S, Makino A & 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.
140. Michaeli S, Honig A, Levanony H, Peled-Zehavi H & Galili G (2014) Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26, 4084–4101.
141. Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, Huang L, Du Y, Hong Y, Tang D et al. (2013) Autophagy contributes to leaf starch degradation. Plant Cell 25, 1383–1399.
142. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR & 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.
143. Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM & Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41, 831–844.
144. Prins A, van Heerden PD, Olmos E, Kunert KJ & Foyer CH (2008) Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: a model for dynamic interactions with ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. J Exp Bot 59, 1935–1950.
145. Chiba A, Ishida H, Nishizawa NK, Makino A & 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.
146. Ishida H & Yoshimoto K (2008) Chloroplasts are partially mobilized to the vacuole by autophagy. Autophagy 4, 961–962.
147. Honig A, Avin-Wittenberg T & Galili G (2012) Selective autophagy in the aid of plant germination and response to nutrient starvation. Autophagy 8, 838–839.
148. Liu Y, Burgos JS, Deng Y, Srivastava R, Howell SH & Bassham DC (2012) Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24, 4635–4651.
149. Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S, Yamada K, Hayashi M, Sakamoto W, Ohsumi Y & Nishimura M (2013) Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 25, 4967–4983.
150. Kim J, Lee H, Lee HN, Kim SH, Shin KD & Chung T (2013) Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell 25, 4956–4966.
151. Farmer LM, Rinaldi MA, Young PG, Danan CH, Burkhart SE & 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.
152. Bartel B, Farmer LM, Rinaldi MA, Young PG, Danan CH & Burkhart SE (2014) Mutation of the Arabidopsis LON2 peroxisomal protease enhances pexophagy. Autophagy 10, 518–519.
153. Ostersetzer O, Kato Y, Adam Z & Sakamoto W (2007) Multiple intracellular locations of Lon protease in Arabidopsis: evidence for the localization of AtLon4 to chloroplasts. Plant Cell Physiol 48, 881–885.
154. Lingard MJ & Bartel B (2009) Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import. Plant Physiol 151, 1354–1365.
155. Burnett SF, Farre JC, Nazarko TY & Subramani S (2015) Peroxisomal Pex3 activates selective autophagy of peroxisomes via interaction with the pexophagy receptor Atg30. J Biol Chem 290, 8623–8631.
156. Farre JC, Manjithaya R, Mathewson RD & Subramani S (2008) PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell 14, 365–376.
157. Nazarko TY, Ozeki K, Till A, Ramakrishnan G, Lotfi P, Yan M & Subramani S (2014) Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J Cell Biol 204, 541–557.
158. Motley AM, Nuttall JM & Hettema EH (2012) Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J 31, 2852–2868.
159. Motley AM, Nuttall JM & Hettema EH (2012) Atg36: the Saccharomyces cerevisiae receptor for pexophagy. Autophagy 8, 1680–1681.
160. Nordgren M, Francisco T, Lismont C, Hennebel L, Brees C, Wang B, Van Veldhoven PP, Azevedo JE & Fransen M (2015) Export-deficient monoubiquitinated PEX5 triggers peroxisome removal in SV40 large T antigen-transformed mouse embryonic fibroblasts. Autophagy 11, 1326–1340.
161. Subramani S (2015) A mammalian pexophagy target. Nat Cell Biol 17, 1371–1373.
162. Zhang J, Tripathi DN, Jing J, Alexander A, Kim J, Powell RT, Dere R, Tait-Mulder J, Lee JH, Paull TT et al. (2015) ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat Cell Biol 17, 1259–1269.
163. Kim HP, Wang X, Chen ZH, Lee SJ, Huang MH, Wang Y, Ryter SW & Choi AM (2008) Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 4, 887–895.
164. Young PG & Bartel B (2015) Pexophagy and peroxisomal protein turnover in plants. Biochim Biophys Acta 1863, 999–1005.
165. Reyes FC, Chung T, Holding D, Jung R, Vierstra R & Otegui MS (2011) Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell 23, 769–784.
166. Levanony H, Rubin R, Altschuler Y & Galili G (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119, 1117–1128.
167. Spitzer C, Li F, Buono R, Roschzttardtz H, Chung T, Zhang M, Osteryoung KW, Vierstra RD & Otegui MS (2015) The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 27, 391–402.
168. Synek L, Sekeres J & Zarsky V (2014) The exocyst at the interface between cytoskeleton and membranes in eukaryotic cells. Front Plant Sci 4, 543.
169. Bodemann BO, Orvedahl A, Cheng T, Ram RR, Ou YH, Formstecher E, Maiti M, Hazelett CC, Wauson EM, Balakireva M et al. (2011) RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144, 253–267.
170. Chien Y, Kim S, Bumeister R, Loo YM, Kwon SW, Johnson CL, Balakireva MG, Romeo Y, Kopelovich L, Gale M Jr et al. (2006) RalB GTPase-mediated activation of the IkappaB family kinase TBK1 couples innate immune signaling to tumor cell survival. Cell 127, 157–170.
171. Cvrckova F & Zarsky V (2013) Old AIMs of the exocyst: evidence for an ancestral association of exocyst subunits with autophagy-associated Atg8 proteins. Plant Signal Behav 8, e27099.
172. Kulich I, Pecenkova T, Sekeres J, Smetana O, Fendrych M, Foissner I, Hoftberger M & Zarsky V (2013) Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14, 1155–1165.
173. Wang J, Ding Y, Wang J, Hillmer S, Miao Y, Lo SW, Wang X, Robinson DG & Jiang L (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.
174. Ding Y, Wang J, Chun Lai JH, Ling Chan VH, Wang X, Cai Y, Tan X, Bao Y, Xia J, Robinson DG et al. (2014) Exo70E2 is essential for exocyst subunit recruitment and EXPO formation in both plants and animals. Mol Biol Cell 25, 412–426.
175. Baboshina OV & Haas AL (1996) Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5. J Biol Chem 271, 2823–2831.
176. Tan JM, Wong ES, Kirkpatrick DS, Pletnikova O, Ko HS, Tay SP, Ho MW, Troncoso J, Gygi SP, Lee MK et al. (2008) Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet 17, 431–439.
177. Ikeda F, Crosetto N & Dikic I (2010) What determines the specificity and outcomes of ubiquitin signaling? Cell 143, 677–681.
178. Marshall RS, Li F, Gemperline DC, Book AJ & Vierstra RD (2015) Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell 58, 1053–1066.
179. Korolchuk VI, Menzies FM & Rubinsztein DC (2010) Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 584, 1393–1398.
180. Lamark T & Johansen T (2010) Autophagy: links with the proteasome. Curr Opin Cell Biol 22, 192–198.
181. Babu JR, Geetha T & Wooten MW (2005) Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem 94, 192–203.
182. Geetha T, Seibenhener ML, Chen L, Madura K & Wooten MW (2008) p62 serves as a shuttling factor for TrkA interaction with the proteasome. Biochem Biophys Res Commun 374, 33–37.
183. Gal J, Strom AL, Kwinter DM, Kilty R, Zhang J, Shi P, Fu W, Wooten MW & Zhu H (2009) Sequestosome 1/p62 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism. J Neurochem 111, 1062–1073.
184. Ulbricht A, Arndt V & Hohfeld J (2013) Chaperone-assisted proteostasis is essential for mechanotransduction in mammalian cells. Commun Integr Biol 6, e24925.
185. McClellan AJ, Tam S, Kaganovich D & Frydman J (2005) Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 7, 736–741.
186. Dai Q, Qian SB, Li HH, McDonough H, Borchers C, Huang D, Takayama S, Younger JM, Ren HY, Cyr DM et al. (2005) Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J Biol Chem 280, 38673–38681.
187. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU & Behl C (2009) Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 28, 889–901.
188. Sroka K, Voigt A, Deeg S, Reed JC, Schulz JB, Bahr M & Kermer P (2009) BAG1 modulates huntingtin toxicity, aggregation, degradation, and subcellular distribution. J Neurochem 111, 801–807.
189. Shin Y, Klucken J, Patterson C, Hyman BT & McLean PJ (2005) The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem 280, 23727–23734.
190. Gamerdinger M, Carra S & Behl C (2011) Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J Mol Med (Berl) 89, 1175–1182.
191. Carra S, Seguin SJ & Landry J (2008) HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 4, 237–239.
192. Fang S, Li L, Cui B, Men S, Shen Y & Yang X (2013) Structural insight into plant programmed cell death mediated by BAG proteins in Arabidopsis thaliana. Acta Crystallogr D Biol Crystallogr 69, 934–945.
193. Kabbage M & Dickman MB (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65, 1390–1402.
194. Liu Y & Bassham DC (2013) Degradation of the endoplasmic reticulum by autophagy in plants. Autophagy 9, 622–623.
195. Xu J, Ji J & Yan XH (2012) Cross-talk between AMPK and mTOR in regulating energy balance. Crit Rev Food Sci Nutr 52, 373–381.