The ATG12-conjugating Enzyme ATG10 Is Essential for Autophagic Vesicle Formation in Arabidopsis Thaliana

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2008 Feb 5

PMID 18245858

Citations 144

Authors

Allison R Phillips

Anongpat Suttangkakul

Richard D Vierstra

Affiliations

Soon will be listed here.

Abstract

Autophagy is an important intracellular recycling system in eukaryotes that utilizes small vesicles to traffic cytosolic proteins and organelles to the vacuole for breakdown. Vesicle formation requires the conjugation of the two ubiquitin-fold polypeptides ATG8 and ATG12 to phosphatidylethanolamine and the ATG5 protein, respectively. Using Arabidopsis thaliana mutants affecting the ATG5 target or the ATG7 E1 required to initiate ligation of both ATG8 and ATG12, we previously showed that the ATG8/12 conjugation pathways together are important when plants encounter nutrient stress and during senescence. To characterize the ATG12 conjugation pathway specifically, we characterized a null mutant eliminating the E2-conjugating enzyme ATG10 that, similar to plants missing ATG5 or ATG7, cannot form the ATG12-ATG5 conjugate. atg10-1 plants are hypersensitive to nitrogen and carbon starvation and initiate senescence and programmed cell death (PCD) more quickly than wild type, as indicated by elevated levels of senescence- and PCD-related mRNAs and proteins during carbon starvation. As detected with a GFP-ATG8a reporter, atg10-1 and atg5-1 mutant plants fail to accumulate autophagic bodies inside the vacuole. These results indicate that ATG10 is essential for ATG12 conjugation and that the ATG12-ATG5 conjugate is necessary to form autophagic vesicles and for the timely progression of senescence and PCD in plants.

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References

Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D . Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 2002; 129(3):1181-93. PMC: 166512. DOI: 10.1104/pp.011024. View

Balk J, Leaver C . The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell. 2001; 13(8):1803-18. PMC: 139137. DOI: 10.1105/tpc.010116. View

Drose S, Bindseil K, Bowman E, Siebers A, Zeeck A, Altendorf K . Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry. 1993; 32(15):3902-6. DOI: 10.1021/bi00066a008. View

van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge U, Kunze R . Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 2006; 141(2):776-92. PMC: 1475451. DOI: 10.1104/pp.106.079293. View

Ohsumi Y . Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001; 2(3):211-6. DOI: 10.1038/35056522. View

Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M . A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science. 2004; 305(5685):855-8. DOI: 10.1126/science.1099859. View

Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H . Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 2007; 144(3):1429-41. PMC: 1914121. DOI: 10.1104/pp.107.100172. View

Tsukada M, Ohsumi Y . Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993; 333(1-2):169-74. DOI: 10.1016/0014-5793(93)80398-e. View

Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T . Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol. 1999; 147(2):435-46. PMC: 2174223. DOI: 10.1083/jcb.147.2.435. View

10.

Doelling J, Walker J, Friedman E, Thompson A, Vierstra R . The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem. 2002; 277(36):33105-14. DOI: 10.1074/jbc.M204630200. View

11.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

12.

Swidzinski J, Sweetlove L, Leaver C . A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J. 2002; 30(4):431-46. DOI: 10.1046/j.1365-313x.2002.01301.x. View

13.

Bassham D . Plant autophagy--more than a starvation response. Curr Opin Plant Biol. 2007; 10(6):587-93. DOI: 10.1016/j.pbi.2007.06.006. View

14.

Brown D, Sun X, Cohen G . Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J Biol Chem. 1993; 268(5):3037-9. View

15.

Xiong Y, Contento A, Bassham D . AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J. 2005; 42(4):535-46. DOI: 10.1111/j.1365-313X.2005.02397.x. View

16.

Suzuki K, Kubota Y, Sekito T, Ohsumi Y . Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells. 2007; 12(2):209-18. DOI: 10.1111/j.1365-2443.2007.01050.x. View

17.

Osuna D, Usadel B, Morcuende R, Gibon Y, Blasing O, Hohne M . Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J. 2007; 49(3):463-91. DOI: 10.1111/j.1365-313X.2006.02979.x. View

18.

Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N . A ubiquitin-like system mediates protein lipidation. Nature. 2000; 408(6811):488-92. DOI: 10.1038/35044114. View

19.

Oh S, Lee S, Chung I, Lee C, Nam H . A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol. 1996; 30(4):739-54. DOI: 10.1007/BF00019008. View

20.

Smalle J, Vierstra R . The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol. 2004; 55:555-90. DOI: 10.1146/annurev.arplant.55.031903.141801. View