1932

Abstract

Plants have evolved sophisticated mechanisms to recycle intracellular constituents, which are essential for developmental and metabolic transitions; for efficient nutrient reuse; and for the proper disposal of proteins, protein complexes, and even entire organelles that become obsolete or dysfunctional. One major route is autophagy, which employs specialized vesicles to encapsulate and deliver cytoplasmic material to the vacuole for breakdown. In the past decade, the mechanics of autophagy and the scores of components involved in autophagic vesicle assembly have been documented. Now emerging is the importance of dedicated receptors that help recruit appropriate cargo, which in many cases exploit ubiquitylation as a signal. Although operating at a low constitutive level in all plant cells, autophagy is upregulated during senescence and various environmental challenges and is essential for proper nutrient allocation. Its importance to plant metabolism and energy balance in particular places autophagy at the nexus of robust crop performance, especially under suboptimal conditions.

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2018-04-29
2024-12-11
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Literature Cited

  1. An H, Haper JW. 1.  2018. Systematic analysis of ribophagy in human cells reveals bystander flux during selective autophagy. Nat. Cell Biol. 20:135–43 [Google Scholar]
  2. Avin-Wittenberg T, Bajdzienko K, Wittenberg G, Alseekh S, Tohge T. 2.  et al. 2015. Global analysis of the role of autophagy in cellular metabolism and energy homeostasis in Arabidopsis seedlings under carbon starvation. Plant Cell 27:306–22 [Google Scholar]
  3. Barros JA, Cavalcanti JHF, Medeiros DB, Nunes-Nesi A, Avin-Wittenberg T. 3.  et al. 2017. Autophagy deficiency compromises alternative pathways of respiration following energy deprivation. Plant Physiol 175:62–76 [Google Scholar]
  4. Bassham DC, MacIntosh GC. 4.  2017. Degradation of cytosolic ribosomes by autophagy-related pathways. Plant Sci 262:169–74 [Google Scholar]
  5. Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC. 5.  2007. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17:1609–14 [Google Scholar]
  6. Book AJ, Gladman NP, Lee SS, Scalf M, Smith LM, Vierstra RD. 6.  2010. Affinity purification of the Arabidopsis 26S proteasome reveals a diverse array of plant proteolytic complexes. J. Biol. Chem. 285:25554–69 [Google Scholar]
  7. Boutrot F, Zipfel C. 7.  2017. Function, discovery and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 55:257–86 [Google Scholar]
  8. Braun P, Carvunis AR, Charloteaux B, Dreze M, Ecker JR. 8.  et al. 2011. Evidence for network evolution in an Arabidopsis interactome map. Science 333:601–7 [Google Scholar]
  9. Carroll AJ.9.  2013. The Arabidopsis cytosolic ribosomal proteome: from form to function. Front. Plant Sci. 4:32 [Google Scholar]
  10. Chanoca A, Kovinich N, Burkel B, Stecha S, Bohorquez-Restrepo A. 10.  et al. 2015. Anthocyanin vacuolar inclusions form by a microautophagy mechanism. Plant Cell 27:2545–59 [Google Scholar]
  11. Chen J, Lalonde S, Obrdlik P, Noorani-Vatani A, Parsa SA. 11.  et al. 2012. Uncovering the Arabidopsis membrane protein interactome enriched in transporters using mating-based split-ubiquitin assays and classification models. Front. Plant Sci. 3:124 [Google Scholar]
  12. Chen L, Su ZZ, Huang L, Xia FN, Qi H. 12.  et al. 2017. The AMP-activated protein kinase KIN10 is involved in the regulation of autophagy in Arabidopsis. Front. Plant Sci 8:1201 [Google Scholar]
  13. Chung T, Phillips AR, Vierstra RD. 13.  2010. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12a and ATG12b loci. Plant J 62:483–93 [Google Scholar]
  14. Chung T, Suttangkakul A, Vierstra RD. 14.  2009. The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-PE adduct are regulated by development and nutrient availability. Plant Physiol 149:220–34 [Google Scholar]
  15. Cohen-Kaplan V, Livneh I, Avni N, Fabre B, Ziv T. 15.  et al. 2016. p62- and ubiquitin-dependent stress-induced autophagy of the mammalian 26S proteasome. PNAS 113:7490–99 [Google Scholar]
  16. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K. 16.  2009. Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6:786–87 [Google Scholar]
  17. Collins GA, Goldberg AL. 17.  2017. The logic of the 26S proteasome. Cell 169:792–806 [Google Scholar]
  18. Contento AL, Kim SJ, Bassham DC. 18.  2004. Transcriptome profiling of the response of Arabidopsis suspension culture cells to sucrose starvation. Plant Physiol 135:2330–47 [Google Scholar]
  19. Contento AL, Xiong Y, Bassham DC. 19.  2005. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J 42:598–608 [Google Scholar]
  20. Courtois-Moreau CL, Pesquet E, Sjödin A, Muñiz L, Bollhöner B. 20.  et al. 2009. A unique program for cell death in xylem fibers of Populus stem. Plant J 58:260–74 [Google Scholar]
  21. Crespo JL, Diaz-Troya S, Florencio FJ. 21.  2005. Inhibition of target of rapamycin signaling in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol 139:1736–49 [Google Scholar]
  22. Cui H, Tsuda K, Parker JE. 22.  2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511 [Google Scholar]
  23. Dagdas YF, Belhaj K, Maqbool A, Chaparro-Garcia A, Pandey P. 23.  et al. 2016. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. eLife 5:e10856Describes the first example of a plant pathogen effector interfering with a host's autophagy machinery. [Google Scholar]
  24. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J. 24.  et al. 2012. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. PNAS 109:15942–46 [Google Scholar]
  25. Devarenne TP.25.  2011. The plant cell death suppressor Adi3 interacts with the autophagic protein Atg8h. Biochem. Biophys. Res. Commun. 412:699–703 [Google Scholar]
  26. Di Berardino J, Marmagne A, Berger A, Yoshimoto K, Cueff G. 26.  et al. 2018. Autophagy controls resource allocations and protein storage accumulation in Arabidopsis seeds. J. Exp. Bot. 69:1403–14 [Google Scholar]
  27. Dikic I.27.  2017. Proteasomal and autophagic degradation systems. Annu. Rev. Biochem. 86:193–224 [Google Scholar]
  28. Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincent M. 28.  et al. 2016. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67:261–85 [Google Scholar]
  29. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD. 29.  2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem 277:33105–14 [Google Scholar]
  30. Dong P, Xiong F, Que Y, Wang K, Yu L. 30.  et al. 2015. Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front. Plant Sci 6:667 [Google Scholar]
  31. Farmer LM, Rinaldi MA, Young PG, Danan CH, Burkhart SE, Bartel B. 31.  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 25:4085–100 [Google Scholar]
  32. Farré JC, Burkenroad A, Burnett SF, Subramani S. 32.  2013. Phosphorylation of mitophagy and pexophagy receptors co-ordinates their interaction with Atg8 and Atg11. EMBO Rep 14:441–49 [Google Scholar]
  33. Farré JC, Subramani S. 33.  2016. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat. Rev. Mol. Cell Biol. 17:537–52 [Google Scholar]
  34. Floyd BE, Morriss SC, MacIntosh GC, Bassham DC. 34.  2015. Evidence for autophagy-dependent pathways of rRNA turnover in Arabidopsis. Autophagy 11:2199–212 [Google Scholar]
  35. Floyd BE, Mugume Y, Morriss SC, MacIntosh GC, Bassham DC. 35.  2017. Localization of RNS2 ribonuclease to the vacuole is required for its role in cellular homeostasis. Planta 245:779–92 [Google Scholar]
  36. Franzmann TM, Jahnel M, Pozniakovsky A, Mahamid J, Holehouse AS. 36.  et al. 2018. Phase separation of a yeast prion protein promotes cellular fitness. Science 359:5654 [Google Scholar]
  37. Fujiki Y, Yoshimoto K, Ohsumi Y. 37.  2007. An Arabidopsis homolog of yeast ATG6 is essential for pollen germination. Plant Physiol 143:1132–39 [Google Scholar]
  38. Fujioka Y, Noda NN, Fujii K, Yoshimoto K, Ohsumi Y, Inagaki F. 38.  2008. In vitro reconstitution of plant ATG8 and ATG12 conjugation systems essential for autophagy. J. Biol. Chem. 283:1921–28 [Google Scholar]
  39. Fujioka Y, Noda NN, Nakatogawa H, Ohsumi Y, Inagaki F. 39.  2010. Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J. Biol. Chem. 285:1508–15 [Google Scholar]
  40. Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM. 40.  et al. 2017. Molecular definitions of autophagy and related processes. EMBO J 36:1811–36 [Google Scholar]
  41. Gao C, Zhuang X, Cui Y, Fu X, He Y. 41.  et al. 2015. Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. PNAS 112:1886–91 [Google Scholar]
  42. Ghiglione HO, Gonzalez FG, Serrago R, Maldonado SB, Chilcott C. 42.  et al. 2008. Autophagy regulated by day length determines the number of fertile florets in wheat. Plant J 55:1010–24 [Google Scholar]
  43. Gladman NP, Marshall RS, Lee KH, Vierstra RD. 43.  2016. The proteasome stress regulon is controlled by a pair of NAC transcription factors in Arabidopsis. Plant Cell 28:1279–96 [Google Scholar]
  44. Goto-Yamada S, Mano S, Nakamori C, Kondo M, Yamawaki R. 44.  et al. 2014. Chaperone and protease functions of LON2 modulate the peroxisomal transition and degradation via autophagy. Plant Cell Physiol 55:482–96 [Google Scholar]
  45. Graf A, Schlereth A, Stitt M, Smith AM. 45.  2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. PNAS 107:9458–63 [Google Scholar]
  46. Grousl T, Ungelenk S, Miller S, Ho CT, Khokhrina M. 46.  et al. 2018. A prion-like domain in Hsp42 drives chaperone-facilitated aggregation of mis-folded proteins. J. Cell Biol. In press. https://doi.org/10.1083/jcb.201708116 [Crossref] [Google Scholar]
  47. Grumati P, Morozzi G, Hölper S, Mari M, Harwardt MI. 47.  et al. 2017. Full length RTN3 regulates turnover of tubular endoplasmic reticulum via selective autophagy. eLife 6:e25555 [Google Scholar]
  48. Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M. 48.  et al. 2013. Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol 199:683–94 [Google Scholar]
  49. Guiboileau A, Yoshimoto K, Soulay F, Bataillé MP, Avice JC, Masclaux-Daubresse C. 49.  2012. The autophagy machinery controls nitrogen re-mobilization at the whole plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol 194:732–40 [Google Scholar]
  50. Hachez C, Veljanovski V, Reinhardt H, Guillaumot D, Vanhee C. 50.  et al. 2014. The Arabidopsis abiotic stress–induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation. Plant Cell 26:4974–90 [Google Scholar]
  51. Hafrén A, Macia JL, Love AJ, Milner JJ, Drucker M, Hofius D. 51.  2017. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. PNAS 114:2026–35Together with Reference 58, provides the first evidence for autophagic degradation of specific viral proteins to limit infection. [Google Scholar]
  52. Hafrén A, Üstün S, Hochmuth A, Svenning S, Johansen T, Hofius D. 52.  2018. Turnip mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiol 176:649–62 [Google Scholar]
  53. Han S, Wang Y, Zheng X, Jia Q, Zhao J. 53.  et al. 2015. Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana. Plant Cell 27:1316–31 [Google Scholar]
  54. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H. 54.  et al. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129:1181–93 [Google Scholar]
  55. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S. 55.  et al. 2004. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–58 [Google Scholar]
  56. Havé M, Balliau T, Cottyn-Boitte B, Dérond E, Cueff G. 56.  et al. 2018. Increase of proteasome and papain-like cysteine protease activities in autophagy mutants: back-up compensatory effect or pro-cell death effect. J. Exp. Bot. 69:1369–85 [Google Scholar]
  57. Havé M, Marmagne A, Chardon F, Masclaux-Daubresse C. 57.  2017. Nitrogen re-mobilization during leaf senescence: lessons from Arabidopsis to crops. J. Exp. Bot. 68:2513–29 [Google Scholar]
  58. Haxim Y, Ismayil A, Jia Q, Wang Y, Zheng X. 58.  et al. 2017. Autophagy functions as an anti-viral mechanism against Geminiviruses in plants. eLife 6:e23897 [Google Scholar]
  59. Hillwig MS, Contento AL, Meyer A, Ebany D, Bassham DC, MacIntosh GC. 59.  2011. RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. PNAS 108:1093–98 [Google Scholar]
  60. Hofius D, Li L, Hafrén A, Coll NS. 60.  2017. Autophagy as an emerging arena for plant-pathogen interactions. Curr. Opin. Plant Biol. 38:117–23 [Google Scholar]
  61. Hofius D, Schultz-Larsen T, Jönsen J, Tsitsigiannis DI, Petersen NH. 61.  et al. 2009. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137:773–83 [Google Scholar]
  62. Honig A, Avin-Wittenberg T, Ufaz S, Galili G. 62.  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 [Google Scholar]
  63. Howell SH.63.  2013. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64:477–99 [Google Scholar]
  64. Howell LA, Tomko RJ, Kusmierczyk AR. 64.  2017. Putting it all together: intrinsic and extrinsic mechanisms governing proteasome biogenesis. Front. Biol. 12:19–48 [Google Scholar]
  65. Hua Z, Vierstra RD. 65.  2011. The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 62:299–334 [Google Scholar]
  66. Huber SC, Kaiser WM. 66.  1996. 5-Aminoimidazole-4-carboxamide riboside activates nitrate reductase in darkened spinach and pea leaves. Physiol. Plant. 98:833–37 [Google Scholar]
  67. Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y. 67.  2006. AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol 47:1641–52 [Google Scholar]
  68. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y. 68.  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 148:142–55 [Google Scholar]
  69. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ. 69.  2005. The critical role of Arabidopsis ELECTRON-TRANSFER FLAVOPROTEIN:UBIQUINONE OXIDOREDUCTASE during dark-induced starvation. Plant Cell 17:2587–600 [Google Scholar]
  70. Izumi M, Hidema J, Makino A, Ishida H. 70.  2013. Autophagy contributes to night-time energy availability for growth in Arabidopsis. Plant Physiol 161:1682–93 [Google Scholar]
  71. Izumi M, Hidema J, Wada S, Kondo E, Kurusu T. 71.  et al. 2015. Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation. Plant Physiol 167:1307–20 [Google Scholar]
  72. Izumi M, Ishida H, Nakamura S, Hidema J. 72.  2017. Entire photo-damaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29:377–94 [Google Scholar]
  73. Izumi M, Wada S, Makino A, Ishida H. 73.  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 154:1196–209 [Google Scholar]
  74. Jacoby RP, Li L, Huang S, Lee CP, Millar AH, Taylor NL. 74.  2012. Mitochondrial composition, function and stress response in plants. J. Integr. Plant Biol. 54:887–906 [Google Scholar]
  75. Jarvis P, López-Juez E. 75.  2013. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14:787–802 [Google Scholar]
  76. Jo EK, Yuk JM, Shin DM, Sasakawa C. 76.  2013. Roles of autophagy in elimination of intracellular bacterial pathogens. Front. Immunol. 4:97 [Google Scholar]
  77. Jung JY, Kim YW, Kwak JM, Hwang JU, Young J. 77.  et al. 2002. Phosphatidylinositol-3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–412 [Google Scholar]
  78. Kabbage M, Williams B, Dickman MB. 78.  2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLOS Pathog 9:e1003287 [Google Scholar]
  79. Kalinowska K, Isono E. 79.  2018. All roads lead to the vacuole: autophagic transport as part of the endomembrane trafficking network. J. Exp. Bot. 69:1313–24 [Google Scholar]
  80. Kalvari I, Tsompanis S, Mulakkal NC, Osgood R, Johansen T. 80.  et al. 2014. iLIR: a web resource for prediction of Atg8-family interacting proteins. Autophagy 10:913–25 [Google Scholar]
  81. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. 81.  2009. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17:98–109 [Google Scholar]
  82. Katsiarimpa A, Kalinowska K, Anzenberger F, Weis C, Ostertag M. 82.  et al. 2013. The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25:2236–52 [Google Scholar]
  83. Keech O, Pesquet E, Ahad A, Askne A, Nordvall D. 83.  et al. 2007. The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant Cell Environ 30:1523–34 [Google Scholar]
  84. Kellner R, de la Concepcion JC, Maqbool A, Kamoun S, Dagdas YF. 84.  2017. ATG8 expansion: a driver of selective autophagy diversification. Trends Plant Sci 22:204–14 [Google Scholar]
  85. Ketelaar T, Voss C, Dimmock SA, Thumm M, Hussey PJ. 85.  2004. Arabidopsis homologs of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett 567:302–6 [Google Scholar]
  86. Khaminets A, Heinrich T, Mari M, Grumati P, Hübner AK. 86.  et al. 2015. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 522:354–58 [Google Scholar]
  87. Kim DY, Scalf M, Smith LM, Vierstra RD. 87.  2013. Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell 25:1523–40 [Google Scholar]
  88. Kim J, Lee H, Lee HN, Kim SH, Shin KD, Chung T. 88.  2013. Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell 25:4956–66 [Google Scholar]
  89. Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL. 89.  et al. 2009. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33:505–16 [Google Scholar]
  90. Klopffleisch K, Phan N, Augustin K, Bayne RS, Booker KS. 90.  et al. 2011. The Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis. Mol. Syst. Biol. 7:532 [Google Scholar]
  91. Kraft C, Deplazes A, Sohrmann M, Peter M. 91.  2008. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10:602–10 [Google Scholar]
  92. Kraft C, Kijanska M, Kalie E, Siergiejuk E, Lee SS. 92.  et al. 2012. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J 31:3691–703 [Google Scholar]
  93. Kraft C, Peter M. 93.  2008. Is the Rsp5 ubiquitin ligase involved in the regulation of ribophagy?. Autophagy 4:838–40 [Google Scholar]
  94. Krinke O, Rülland E, Valentova O, Vergnolle C, Renou JP. 94.  et al. 2007. Phosphatidylinositol-4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol 144:1347–59 [Google Scholar]
  95. Kulich I, Pečenková T, Sekereš J, Smetana O, Fendrych M. 95.  et al. 2013. An Arabidopsis exocyst sub-complex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14:1155–65 [Google Scholar]
  96. Kurusu T, Koyano T, Hanamata S, Kubo T, Noguchi Y. 96.  et al. 2014. OsATG7 is required for autophagy-dependent lipid metabolism in rice post-meiotic anther development. Autophagy 10:878–88 [Google Scholar]
  97. Kwon SI, Cho HJ, Jung JH, Yoshimoto K, Shirasu K, Park OK. 97.  2010. The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J 64:151–64 [Google Scholar]
  98. Lai Z, Wang F, Zheng Z, Fan B, Chen Z. 98.  2011. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66:953–68 [Google Scholar]
  99. Le Bars R, Marion J, Le Borgne R, Satiat-Jeunemaitre B, Bianchi MW. 99.  2014. ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat. Commun. 5:4121Reports that ATG5 defines a phagophore subdomain that is closely connected to the cortical ER. [Google Scholar]
  100. Lee HN, Zarza X, Kim JH, Yoon MJ, Kim SH. 100.  et al. 2018. Arabidopsis VPS38 is required for vacuolar trafficking but is dispensable for autophagy. Plant Physiol 176:1559–72 [Google Scholar]
  101. Lee Y, Bak G, Choi Y, Chuang WI, Cho HT, Lee Y. 101.  2008. Roles of phosphatidylinositol-3-kinase in root hair growth. Plant Physiol 147:624–35 [Google Scholar]
  102. Lee Y, Kim ES, Choi Y, Hwang I, Staiger CJ. 102.  et al. 2008. The Arabidopsis phosphatidylinositol-3-kinase is important for pollen development. Plant Physiol 147:1886–97 [Google Scholar]
  103. Lenz HD, Haller E, Melzer E, Kober K, Wurster K. 103.  et al. 2011. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66:818–30 [Google Scholar]
  104. Levanony H, Rubin R, Altschuler Y, Galili G. 104.  1992. Evidence for a novel route of wheat storage proteins to vacuoles. J. Cell Biol. 119:1117–28 [Google Scholar]
  105. Li F, Chung T, Pennington JG, Federico ML, Kaeppler HF. 105.  et al. 2015. Autophagic recycling plays a central role in maize nitrogen re-mobilization. Plant Cell 27:1389–408Reports the first example of autophagy deficiency in maize and its role in nutrient remobilization to developing seeds. [Google Scholar]
  106. Li F, Chung T, Vierstra RD. 106.  2014. AUTOPHAGY-RELATED11 plays a critical role in general autophagy and senescence-induced mitophagy in Arabidopsis. Plant Cell 26:788–807 [Google Scholar]
  107. Li F, Vierstra RD. 107.  2012. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–37 [Google Scholar]
  108. Li W, Chen M, Wang E, Hu L, Hawkesford MJ. 108.  et al. 2016. Genome-wide analysis of autophagy-associated genes in foxtail millet (Setaria italica L.) and characterization of the function of SiATG8a in conferring tolerance to nitrogen starvation in rice. BMC Genom 17:797 [Google Scholar]
  109. Ling Q, Huang W, Baldwin A, Jarvis P. 109.  2012. Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338:655–59 [Google Scholar]
  110. Lingard MJ, Monroe-Augustus M, Bartel B. 110.  2009. Peroxisome-associated matrix protein degradation in Arabidopsis. PNAS 106:4561–66 [Google Scholar]
  111. Liu Y, Bassham DC. 111.  2010. TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLOS ONE 5:e11883 [Google Scholar]
  112. Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP. 112.  2005. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567–77 [Google Scholar]
  113. Liu Y, Soto-Burgos J, Deng Y, Srivastava R, Howell SH, Bassham DC. 113.  2012. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24:4635–51 [Google Scholar]
  114. Lu K, Psakhye I, Jentsch S. 114.  2014. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell 158:549–63 [Google Scholar]
  115. Maqbool A, Hughes RK, Dagdas YF, Tregidgo N, Zess E. 115.  et al. 2016. Structural basis of host AUTOPHAGY-RELATED8 (ATG8) binding by the Irish potato famine pathogen effector protein PexRD54. J. Biol. Chem. 291:20270–82 [Google Scholar]
  116. Marshall RS, Li F, Gemperline DC, Book AJ, Vierstra RD. 116.  2015. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 58:1053–66Provides the first report of proteasomes being degraded by autophagy, via the Ub-binding RPN10 receptor. [Google Scholar]
  117. Marshall RS, McLoughlin F, Vierstra RD. 117.  2016. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep 16:1717–32 [Google Scholar]
  118. Marshall RS, Vierstra RD. 118.  2015. Eat or be eaten: the autophagic plight of inactive 26S proteasomes. Autophagy 11:1927–28 [Google Scholar]
  119. Masclaux-Daubresse C, Chen Q, Havé M. 119.  2017. Regulation of nutrient recycling via autophagy. Curr. Opin. Plant Biol. 39:8–17 [Google Scholar]
  120. Masclaux-Daubresse C, Clément G, Anne P, Routaboul JM, Guiboileau A. 120.  et al. 2014. Stitching together the multiple dimensions of autophagy using metabolomics and transcriptomics reveals impacts on metabolism, development, and plant responses to the environment in Arabidopsis. Plant Cell 26:1857–77Provides the first comprehensive view on the importance of autophagy to plant metabolism. [Google Scholar]
  121. Matsuoka K, Bassham DC, Raikhel NV, Nakamura K. 121.  1995. Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J. Cell Biol. 130:1307–18 [Google Scholar]
  122. Matsuoka K, Higuchi T, Maeshima M, Nakamura K. 122.  1997. A vacuolar-type H+-ATPase in a non-vacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells. Plant Cell 9:533–46 [Google Scholar]
  123. Merkolova EA, Guiboileau A, Naya L, Masclaux-Daubresse C, Yoshimoto K. 123.  2014. Assessment and optimization of autophagy monitoring methods in Arabidopsis roots indicate direct fusion of autophagosomes with vacuoles. Plant Cell Physiol 55:715–26 [Google Scholar]
  124. Michaeli S, Honig A, Levanony H, Peled-Zehavi H, Galili G. 124.  2014. Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26:4084–101 [Google Scholar]
  125. Minina EA, Moschou PN, Vetukuri RR, Sanches-Vera V, Cardoso C. 125.  et al. 2018. Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness. J. Exp. Bot. 69:1415–32 [Google Scholar]
  126. Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H. 126.  et al. 2015. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 522:359–62 [Google Scholar]
  127. Montané MH, Menand B. 127.  2013. ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells without changing developmental patterning. J. Exp. Bot. 64:4361–74 [Google Scholar]
  128. Moriyasu Y, Inoue Y. 128.  2008. Use of protease inhibitors for detecting autophagy in plants. Methods Enzymol 451:557–80 [Google Scholar]
  129. Moriyasu Y, Ohsumi Y. 129.  1996. Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant. Physiol. 111:1233–41 [Google Scholar]
  130. Müller M, Kötter P, Behrendt C, Walter E, Scheckhuber CQ. 130.  et al. 2015. Synthetic quantitative array technology identifies the Ubp3-Bre5 deubiquitinase complex as a negative regulator of mitophagy. Cell Rep 10:1215–25 [Google Scholar]
  131. Nakahara KS, Masuta C, Yamada S, Shimura H, Kashihara Y. 131.  et al. 2012. A tobacco calmodulin-like protein provides secondary defence by binding to and directing degradation of virus RNA silencing suppressors. PNAS 109:10113–18 [Google Scholar]
  132. Nemec AA, Howell LA, Peterson AK, Murray MA, Tomko RJ. 132.  2017. Autophagic clearance of proteasomes in yeast requires the conserved sorting nexin Snx4. J. Biol. Chem. 292:21466–80 [Google Scholar]
  133. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T. 133.  et al. 2009. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461:654–58 [Google Scholar]
  134. Noda NN, Ohsumi Y, Inagaki F. 134.  2010. An Atg8-interacting motif crucial for selective autophagy. FEBS Lett 584:1379–85 [Google Scholar]
  135. Nolan TM, Brennan B, Yang M, Chen J, Zhang M. 135.  et al. 2017. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41:33–46Demonstrates a role for receptor phosphorylation in regulating selective autophagic degradation of BES1 by DSK2. [Google Scholar]
  136. Nziengui H, Bouhidel K, Pillon D, Der C, Marty F, Schöefs B. 136.  2007. Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Lett 581:3356–62 [Google Scholar]
  137. Ohsumi Y.137.  2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2:211–16 [Google Scholar]
  138. Okamoto K, Kondo-Okamoto N, Ohsumi Y. 138.  2009. The mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17:87–97 [Google Scholar]
  139. Ossareh-Nazari B, Niño CA, Bengtson MH, Lee JW, Joazeiro CA, Dargemont C. 139.  2014. Ubiquitylation by the Ltn1 E3 ligase protects 60S ribosomes from starvation-induced selective autophagy. J. Cell Biol. 204:909–17 [Google Scholar]
  140. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA. 140.  et al. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282:24131–45 [Google Scholar]
  141. Paul AL, Sehnke PC, Ferl RJ. 141.  2005. Isoform-specific subcellular localization among 14-3-3 proteins in Arabidopsis seems to be driven by client interactions. Mol. Biol. Cell 16:1735–43 [Google Scholar]
  142. Pecenková T, Markovic V, Sabol P, Kulich I, Žárský V. 142.  2017. Exocyst- and autophagy-related membrane trafficking in plants. J. Exp. Bot. 69:47–57 [Google Scholar]
  143. Pérez-Pérez ME, Florencio FJ, Crespo JL. 143.  2010. Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152:1874–88 [Google Scholar]
  144. Phillips AR, Suttangkakul A, Vierstra RD. 144.  2008. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178:1339–53 [Google Scholar]
  145. Popa C, Li L, Gil S, Tatjer L, Hashii K. 145.  et al. 2016. The effector AWR5 from the plant pathogen Ralstonia solanacearum is an inhibitor of the TOR signalling pathway. Sci. Rep. 6:27058 [Google Scholar]
  146. Pourcel L, Irani NG, Lu Y, Riedl K, Schwartz S, Grotewold E. 146.  2010. The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol. Plant 3:78–90 [Google Scholar]
  147. Pu Y, Luo X, Bassham DC. 147.  2017. TOR-dependent and -independent pathways regulate autophagy in Arabidopsis thaliana. Front. Plant Sci 8:1204 [Google Scholar]
  148. Qi H, Xia FN, Xie LJ, Yu LJ, Chen QF. 148.  et al. 2017. TRAF family proteins regulate autophagy dynamics by modulating AUTOPHAGY-RELATED6 stability in Arabidopsis. Plant Cell 29:890–911 [Google Scholar]
  149. Reyes FC, Chung T, Holding D, Jung R, Vierstra RD, Otegui MS. 149.  2011. Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell 23:769–84 [Google Scholar]
  150. Roberts P, Moshitch-Moshkovitz S, Kvam E, O'Toole E, Winey M, Goldfarb DS. 150.  2003. Piecemeal microautophagy of the nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell 14:129–41 [Google Scholar]
  151. Robinson DG, Oliviusson P, Hinz G. 151.  2005. Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 6:615–25 [Google Scholar]
  152. Rojo E, Zouhar J, Carter C, Kovaleva V, Raikhel NV. 152.  2003. A unique mechanism for protein processing and degradation in Arabidopsis thaliana. PNAS 100:7389–94 [Google Scholar]
  153. Sargent G, van Zutphen T, Shatseva T, Zhang L, Di Giovanni V. 153.  et al. 2016. PEX2 is the E3 ubiquitin ligase required for pexophagy during starvation. J. Cell Biol. 214:677–90 [Google Scholar]
  154. Schepetilnikov M, Dimitrova M, Mancera-Martinez E, Geldreich A, Keller M, Ryabova LA. 154.  2013. TOR and S6K1 promote translation re-initiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J 32:1087–102 [Google Scholar]
  155. Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S. 155.  et al. 2013. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 25:4967–83 [Google Scholar]
  156. Sláviková S, Shy G, Yao Y, Glozman R, Levanony H. 156.  et al. 2005. The autophagy-associated Atg8 gene family operates during both favourable growth conditions and starvation stress in Arabidopsis. J. Exp. Bot 56:2839–49 [Google Scholar]
  157. Sontag EM, Samant RS, Frydman J. 157.  2017. Mechanisms and functions of spatial protein quality control. Annu. Rev. Biochem. 86:97–122 [Google Scholar]
  158. Soto-Burgos J, Bassham DC. 158.  2017. SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana. PLOS ONE 12:e0182591 [Google Scholar]
  159. Spitzer C, Li F, Buono R, Roschzttardtz H, Chung T. 159.  et al. 2015. The endosomal protein CHARGED MULTI-VESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 27:391–402 [Google Scholar]
  160. Surpin M, Zheng H, Morita MT, Saito C, Avila E. 160.  et al. 2003. The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15:2885–99 [Google Scholar]
  161. Sutipatanasomboon A, Herberth S, Alwood EG, Häweker H, Müller B. 161.  et al. 2017. Disruption of the plant-specific CFS1 gene impairs autophagosome turnover and triggers EDS1-dependent cell death. Sci. Rep. 7:8677 [Google Scholar]
  162. Suttangkakul A, Li F, Chung T, Vierstra RD. 162.  2011. The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23:3761–79 [Google Scholar]
  163. Svenning S, Lamark T, Krause K, Johansen T. 163.  2011. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7:993–1010Together with Reference 200, this paper describes the identification of NBR1/Joka2, the first selective autophagy receptor reported in plants. [Google Scholar]
  164. Takáč T, Pechan T, Šamajová O, Šamaj J. 164.  2013. Vesicular trafficking and stress response coupled to PI3K inhibition by LY294002 as revealed by proteomic and cell biological analysis. J. Proteome Res. 12:4435–48 [Google Scholar]
  165. Takatsuka C, Inoue Y, Matsuoka K, Moriyasu Y. 165.  2004. 3-Methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions. Plant Cell Physiol 45:265–74 [Google Scholar]
  166. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. 166.  2005. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138:2097–110 [Google Scholar]
  167. Thompson AR, Vierstra RD. 167.  2005. Autophagic recycling: Lessons from yeast help define the process in plants. Curr. Opin. Plant Biol. 8:165–73 [Google Scholar]
  168. Tolley N, Sparkes IA, Hunter PR, Craddock CP, Nuttall J. 168.  et al. 2008. Over-expression of a plant reticulon re-models the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 9:94–102 [Google Scholar]
  169. Üstün S, Hafrén A, Liu Q, Marshall RS, Minina EA. 169.  et al. 2018. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell In press. https://doi.org/10.1105/tpc.17.00815 [Google Scholar]
  170. van Doorn WG, Papini A. 170.  2013. The ultra-structure of autophagy in plant cells: a review. Autophagy 9:1922–36 [Google Scholar]
  171. Vanhee C, Zapotoczny G, Masquelier D, Ghislain M, Batoko H. 171.  2011. The Arabidopsis multi-stress 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 [Google Scholar]
  172. Vierstra RD.172.  2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10:385–97 [Google Scholar]
  173. Voitsekhovskaja OV, Schiermeyer A, Reumann S. 173.  2014. Plant peroxisomes are degraded by starvation-induced and constitutive autophagy in tobacco BY-2 suspension–cultured cells. Front. Plant Sci. 5:629 [Google Scholar]
  174. Wada S, Hayashida Y, Izumi M, Kurusu T, Hanamata S. 174.  et al. 2015. Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiol 168:60–73 [Google Scholar]
  175. Waite KA, De La Mota-Peynado A, Vontz G, Roelofs J. 175.  2016. Starvation induces proteasome autophagy with different pathways for core and regulatory particles. J. Biol. Chem. 291:3239–53 [Google Scholar]
  176. Wang P, Mugume Y, Bassham DC. 176.  2018. New advances in autophagy in plants: regulation, selectivity and function. Semin. Cell Dev. Biol. In press. https://doi.org/10.1016/j.semcdb.2017.07.018 [Crossref] [Google Scholar]
  177. Wang P, Richardson C, Hawes C, Hussey PJ. 177.  2016. Arabidopsis NAP1 regulates the formation of autophagosomes. Curr. Biol. 26:2060–69 [Google Scholar]
  178. Wang Y, Nishimura MT, Zhao T, Tang D. 178.  2011. ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J 68:74–87 [Google Scholar]
  179. Woodson JD, Joens MS, Sinson AB, Gilkerson J, Salomé PA. 179.  et al. 2015. Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts. Science 350:450–54 [Google Scholar]
  180. Wurzer B, Zaffagnini G, Fracchiolla D, Turco E, Abert C. 180.  et al. 2015. Oligomerization of p62 allows for selection of ubiquitylated cargo and isolation membrane during selective autophagy. eLife 4:e08941 [Google Scholar]
  181. Xia K, Liu T, Ouyang J, Wang R, Fan T, Zhang M. 181.  2011. Genome-wide identification, classification and expression analysis of autophagy-associated gene homologs in rice (Oryza sativa L.). DNA Res 18:363–77 [Google Scholar]
  182. Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang NN. 182.  2012. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLOS ONE 7:e37217 [Google Scholar]
  183. Xie Q, Tzfadia O, Levy M, Weithorn E, Peled-Zehavi H. 183.  et al. 2016. hfAIM: a reliable bioinformatics approach for in silico genome-wide identification of autophagy-associated Atg8-interacting motifs in various organisms. Autophagy 12:876–87 [Google Scholar]
  184. Xiong Y, Contento AL, Bassham DC. 184.  2005. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42:535–46 [Google Scholar]
  185. Xiong Y, Sheen J. 185.  2012. Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J. Biol. Chem. 287:2836–42 [Google Scholar]
  186. Xu N, Gao XQ, Zhao XY, Zhu DZ, Zhou LZ, Zhang XS. 186.  2011. Arabidopsis VPS15 is essential for pollen development and germination through modulating phosphatidylinositol-3-phosphate formation. Plant Mol. Biol. 77:251–60 [Google Scholar]
  187. Yamaguchi M, Matoba K, Sawada R, Fujioka Y, Nakatogawa H. 187.  et al. 2012. Non-canonical recognition and UBL loading of distinct E2s by autophagy-essential Atg7. Nat. Struct. Mol. Biol. 19:1250–56 [Google Scholar]
  188. Yamano K, Matsuda N, Tanaka K. 188.  2016. The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep 17:300–16 [Google Scholar]
  189. Yang X, Srivastava R, Howell SH, Bassham DC. 189.  2016. Activation of autophagy by unfolded proteins during endoplasmic reticulum stress. Plant J 85:83–95 [Google Scholar]
  190. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S. 190.  et al. 2004. Processing of the ubiquitin-like ATG8 proteins by ATG4 is essential for plant autophagy. Plant Cell 16:2967–83 [Google Scholar]
  191. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C. 191.  et al. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–27 [Google Scholar]
  192. Young PG, Bartel B. 192.  2016. Pexophagy and peroxisomal protein turnover in plants. Biochim. Biophys. Acta 1863:999–1005 [Google Scholar]
  193. Zhang J, Tripathi DN, Jing J, Alexander A, Kim J. 193.  et al. 2015. ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat. Cell Biol. 17:1259–69 [Google Scholar]
  194. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA. 194.  et al. 2009. Inhibition of SNF1-related protein kinase 1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–71 [Google Scholar]
  195. Zhou J, Wang J, Cheng Y, Chi YJ, Fan B. 195.  et al. 2013. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLOS Genet 9:e1003196 [Google Scholar]
  196. Zhou J, Wang J, Yu JQ, Chen Z. 196.  2014. Role and regulation of autophagy in heat stress responses of tomato plants. Front. Plant Sci. 5:174 [Google Scholar]
  197. Zhou XM, Zhao P, Wang W, Zou J, Cheng TH. 197.  et al. 2015. A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues. DNA Res 22:245–57 [Google Scholar]
  198. Zhuang X, Chung KP, Cui Y, Lin W, Gao C. 198.  et al. 2017. ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. PNAS 114:426–35Reports that the phagophore emerges from the endoplasmic reticulum and that this process requires ATG9. [Google Scholar]
  199. Zhuang X, Wang H, Lam SK, Gao C, Wang X. 199.  et al. 2013. A BAR-domain protein SH3P2, which binds to phosphatidylinositol-3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25:4596–615Provides an early example of an ATG8-interacting protein regulating autophagosome formation rather than cargo recruitment. [Google Scholar]
  200. Zientara-Rytter K, Lukomska J, Moniuszko G, Gwozdecki R, Surowiecki P. 200.  et al. 2011. Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7:1145–58 [Google Scholar]
  201. Zvereva AS, Golyaev V, Turco S, Gubaeva EG, Rajeswaran R. 201.  et al. 2016. A viral protein suppresses oxidative burst– and salicylic acid–dependent autophagy and facilitates bacterial growth on virus-infected plants. New Phytol 211:1020–34 [Google Scholar]
  202. Marshall RS, Vierstra RD. 202.  2018. Proteasome storage granules protect proteasomes from autophagic degradation upon carbon starvation. eLife In press Describes a novel route to protect substrates from autophagy by aggregating them into a membrane-less cytoplasmic compartment. [Google Scholar]
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