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The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis

Suttangkakul, Anongpat, Li, Faqiang, Chung, Taijoon, Vierstra, Richard D.·2011·The Plant Cell
DOI 10.1105/tpc.111.090993
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Abstract

Autophagy is an intracellular recycling route in eukaryotes whereby organelles and cytoplasm are sequestered in vesicles, which are subsequently delivered to the vacuole for breakdown. The process is induced by various nutrient-responsive signaling cascades converging on the Autophagy-Related1 (ATG1)/ATG13 kinase complex. Here, we describe the ATG1/13 complex in Arabidopsis thaliana and show that it is both a regulator and a target of autophagy. Plants missing ATG13 are hypersensitive to nutrient limitations and senesce prematurely similar to mutants lacking other components of the ATG system. Synthesis of the ATG12-ATG5 and ATG8-phosphatidylethanolamine adducts, which are essential for autophagy, still occurs in ATG13-deficient plants, but the biogenesis of ATG8-decorated autophagic bodies does not, indicating that the complex regulates downstream events required for autophagosome enclosure and/or vacuolar delivery. Surprisingly, levels of the ATG1a and ATG13a phosphoproteins drop dramatically during nutrient starvation and rise again upon nutrient addition. This turnover is abrogated by inhibition of the ATG system, indicating that the ATG1/13 complex becomes a target of autophagy. Consistent with this mechanism, ATG1a is delivered to the vacuole with ATG8-decorated autophagic bodies. Given its responsiveness to nutrient demands, the turnover of the ATG1/13 kinase likely provides a dynamic mechanism to tightly connect autophagy to a plant's nutritional status.

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Research works printed but not linked: 60

  1. Alonso, 2003, Genome-wide insertional mutagenesis of Arabidopsis thaliana, Science, 301, 653, 10.1126/science.1086391 · DOI
  2. Bassham, 2009, Function and regulation of macroautophagy in plants, Biochim. Biophys. Acta, 1793, 1397, 10.1016/j.bbamcr.2009.01.001 · DOI
  3. Chan, 2009, Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism, Mol. Cell. Biol., 29, 157, 10.1128/MCB.01082-08 · DOI · Paper page
  4. Chang, 2009, An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation, Mol. Biol. Cell, 20, 2004, 10.1091/mbc.e08-12-1250 · DOI
  5. Chenna, 2003, Multiple sequence alignment with the Clustal series of programs, Nucleic Acids Res., 31, 3497, 10.1093/nar/gkg500 · DOI
  6. Cheong, 2008, The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae, Mol. Biol. Cell, 19, 668, 10.1091/mbc.e07-08-0826 · DOI · Paper page
  7. Chung, 2010, ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci, Plant J., 62, 483, 10.1111/j.1365-313X.2010.04166.x · DOI · Paper page
  8. Chung, 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, 10.1104/pp.108.126714 · DOI · Paper page
  9. Citovsky, 2006, Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta, J. Mol. Biol., 362, 1120, 10.1016/j.jmb.2006.08.017 · DOI
  10. Contento, 2004, Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation, Plant Physiol., 135, 2330, 10.1104/pp.104.044362 · DOI
  11. Contento, 2005, Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein, Plant J., 42, 598, 10.1111/j.1365-313X.2005.02396.x · DOI
  12. Curtis, 2003, A gateway cloning vector set for high-throughput functional analysis of genes in planta, Plant Physiol., 133, 462, 10.1104/pp.103.027979 · DOI
  13. Deprost, 2007, The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation, EMBO Rep., 8, 864, 10.1038/sj.embor.7401043 · DOI
  14. Doelling, 2002, The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana, J. Biol. Chem., 277, 33105, 10.1074/jbc.M204630200 · DOI
  15. Earley, 2006, Gateway-compatible vectors for plant functional genomics and proteomics, Plant J., 45, 616, 10.1111/j.1365-313X.2005.02617.x · DOI
  16. Fujioka, 2008, In vitro reconstitution of plant Atg8 and Atg12 conjugation systems essential for autophagy, J. Biol. Chem., 283, 1921, 10.1074/jbc.M706214200 · DOI
  17. Funakoshi, 1997, Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae, Gene, 192, 207, 10.1016/S0378-1119(97)00031-0 · DOI
  18. Ganley, 2009, ULK1-ATG13-FIP200 complex mediates mTOR signaling and is essential for autophagy, J. Biol. Chem., 284, 12297, 10.1074/jbc.M900573200 · DOI · Paper page
  19. Gingerich, 2007, Large-scale, lineage-specific expansion of a bric-a-brac/tramtrack/broad complex ubiquitin-ligase gene family in rice, Plant Cell, 19, 2329, 10.1105/tpc.107.051300 · DOI
  20. Hanaoka, 2002, Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene, Plant Physiol., 129, 1181, 10.1104/pp.011024 · DOI
  21. Hanks, 1995, Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification, FASEB J., 9, 576, 10.1096/fasebj.9.8.7768349 · DOI
  22. Hara, 2008, FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells, J. Cell Biol., 181, 497, 10.1083/jcb.200712064 · DOI · Paper page
  23. Hillwig, 2011, RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants, Proc. Natl. Acad. Sci. USA, 108, 1093, 10.1073/pnas.1009809108 · DOI
  24. Hofius, 2009, Autophagic components contribute to hypersensitive cell death in Arabidopsis, Cell, 137, 773, 10.1016/j.cell.2009.02.036 · DOI
  25. Hosokawa, 2009, Atg101, a novel mammalian autophagy protein interacting with Atg13, Autophagy, 5, 973, 10.4161/auto.5.7.9296 · DOI
  26. Ishida, 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, 10.1104/pp.108.122770 · DOI
  27. Johansen, 2011, Selective autophagy mediated by autophagic adapter proteins, Autophagy, 7, 279, 10.4161/auto.7.3.14487 · DOI
  28. Jung, 2009, ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery, Mol. Biol. Cell, 20, 1992, 10.1091/mbc.e08-12-1249 · DOI · Paper page
  29. Kamada, 2000, Tor-mediated induction of autophagy via an Apg1 protein kinase complex, J. Cell Biol., 150, 1507, 10.1083/jcb.150.6.1507 · DOI · Paper page
  30. Lee, 2003, Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum, Plant J., 33, 825, 10.1046/j.1365-313X.2003.01672.x · DOI
  31. Lenz, 2011, Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens, Plant J., 66, 818, 10.1111/j.1365-313X.2011.04546.x · DOI
  32. Liu, 2010, TOR is a negative regulator of autophagy in Arabidopsis thaliana, PLoS ONE, 5, e11883, 10.1371/journal.pone.0011883 · DOI
  33. Liu, 2005, Autophagy regulates programmed cell death during the plant innate immune response, Cell, 121, 567, 10.1016/j.cell.2005.03.007 · DOI
  34. Ma, 2005, Organ-specific expression of Arabidopsis genome during development, Plant Physiol., 138, 80, 10.1104/pp.104.054783 · DOI
  35. Meiling-Wesse, 2002, Ccz1p/Aut11p/Cvt16p is essential for autophagy and the CVT pathway, FEBS Lett., 526, 71, 10.1016/S0014-5793(02)03119-8 · DOI
  36. Menand, 2002, Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene, Proc. Natl. Acad. Sci. USA, 99, 6422, 10.1073/pnas.092141899 · DOI
  37. Mercer, 2009, A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy, Autophagy, 5, 649, 10.4161/auto.5.5.8249 · DOI
  38. Nelson, 2007, A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants, Plant J., 51, 1126, 10.1111/j.1365-313X.2007.03212.x · DOI
  39. Noda, 2008, Structural basis of target recognition by Atg8/LC3 during selective autophagy, Genes Cells, 13, 1211, 10.1111/j.1365-2443.2008.01238.x · DOI
  40. Page, 1996, TreeView: An application to display phylogenetic trees on personal computers, Comput. Appl. Biosci., 12, 357
  41. Phillips, 2008, The ATG12-conjugating enzyme ATG10 Is essential for autophagic vesicle formation in Arabidopsis thaliana, Genetics, 178, 1339, 10.1534/genetics.107.086199 · DOI
  42. Reyes, 2011, Delivery of prolamins to the protein storage vacuole in maize aleurone cells, Plant Cell, 23, 769, 10.1105/tpc.110.082156 · DOI
  43. Ronquist, 2003, MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 19, 1572, 10.1093/bioinformatics/btg180 · DOI
  44. Rosso, 2003, An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics, Plant Mol. Biol., 53, 247, 10.1023/B:PLAN.0000009297.37235.4a · DOI
  45. Sláviková, 2005, The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants, J. Exp. Bot., 56, 2839, 10.1093/jxb/eri276 · DOI
  46. Smalle, 2002, Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12, Plant Cell, 14, 17, 10.1105/tpc.010381 · DOI
  47. Suzuki, 2001, The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation, EMBO J., 20, 5971, 10.1093/emboj/20.21.5971 · DOI
  48. Suzuki, 2007, Hierarchy of Atg proteins in pre-autophagosomal structure organization, Genes Cells, 12, 209, 10.1111/j.1365-2443.2007.01050.x · DOI
  49. Suzuki, 2010, Current knowledge of the pre-autophagosomal structure (PAS), FEBS Lett., 584, 1280, 10.1016/j.febslet.2010.02.001 · DOI
  50. Thompson, 2005, Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways, Plant Physiol., 138, 2097, 10.1104/pp.105.060673 · DOI · Paper page
  51. Thompson, 2005, Autophagic recycling: Lessons from yeast help define the process in plants, Curr. Opin. Plant Biol., 8, 165, 10.1016/j.pbi.2005.01.013 · DOI
  52. Ulijasz, 2009, Cyanochromes are blue/green light photoreversible photoreceptors defined by a stable double cysteine linkage to a phycoviolobilin-type chromophore, J. Biol. Chem., 284, 29757, 10.1074/jbc.M109.038513 · DOI
  53. Vanhee, 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, 10.1105/tpc.110.081570 · DOI
  54. Vierstra, 2009, The ubiquitin-26S proteasome system at the nexus of plant biology, Nat. Rev. Mol. Cell Biol., 10, 385, 10.1038/nrm2688 · DOI
  55. Wada, 2009, Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves, Plant Physiol., 149, 885, 10.1104/pp.108.130013 · DOI
  56. Xie, 2007, Autophagosome formation: Core machinery and adaptations, Nat. Cell Biol., 9, 1102, 10.1038/ncb1007-1102 · DOI
  57. Xiong, 2005, AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana, Plant J., 42, 535, 10.1111/j.1365-313X.2005.02397.x · DOI
  58. Yoshimoto, 2004, Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy, Plant Cell, 16, 2967, 10.1105/tpc.104.025395 · DOI · Paper page
  59. Yoshimoto, 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, 10.1105/tpc.109.068635 · DOI
  60. Zheng, 2011, AUXIN UP-REGULATED F-BOX PROTEIN1 regulates the cross talk between auxin transport and cytokinin signaling during plant root growth, Plant Physiol., 156, 1878, 10.1104/pp.111.179812 · DOI

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Metadata

Authors
Suttangkakul, A., Li, F., Chung, T., & Vierstra, R. D.
Affiliations
Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706
Venue
The Plant Cell
Publisher
Oxford University Press (OUP)
Published
2011-10-01
Volume
23
Issue
10
Pages
3761-3779
ISSN
  • 1532-298X
  • 1040-4651
DOI
10.1105/tpc.111.090993
Cited by
311
References
8
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)

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