AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana

Plant Journal

Volumn 42, Issue 4, 2005, Pages 535-546

  Xiong, Yan ^a   Contento, Anthony L ^a   Bassham, Diane C ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

ATG18; Autophagosome; Autophagy; Senescence; Starvation; Vacuole

Indexed keywords

CELL MEMBRANES; GENES; GROWTH KINETICS; MACROMOLECULES; PLANTS (BOTANY); PROTEINS; RAW MATERIALS;

AUTOPHAGY; EUKARYOTIC CELLS; GROWTH CONDITIONS; SENESCENCE;

CYTOLOGY;

ARABIDOPSIS PROTEIN; ATG18A PROTEIN, ARABIDOPSIS; NITROGEN; SMALL INTERFERING RNA; SUCROSE;

ARABIDOPSIS; ARTICLE; AUTOPHAGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYLOGENY; PHYSIOLOGY; TRANSGENIC PLANT; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOPHAGY; GENE EXPRESSION REGULATION, PLANT; NITROGEN; PHYLOGENY; PLANTS, GENETICALLY MODIFIED; RNA, SMALL INTERFERING; SUCROSE;

CYTOLOGY; GENES; GROWTH RATE; MACROMOLECULES; NUTRIENTS; PLANTS; PROTEINS; RAW MATERIALS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 19444366819     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02397.x     Document Type: Article

References (51)

1. Abeliovich, H., Dunn, W.A., Jr, Kim, J. and Klionsky, D.J. (2000) Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol. 151, 1025-1033.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Aubert, S., Gout, E., Bligny, R., Marty-Mazars, D., Barrieu, F., Alabouvette, J., Marty, F. and 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.
4. Barth, H., Meiling-Wesse, K., Epple, U.D. and Thumm, M. (2001) Autophagy and the cytoplasm to vacuole targeting pathway both require Aut10p. FEBS Lett. 508, 23-28.
5. Barth, H., Meiling-Wesse, K., Epple, U.D. and Thumm, M. (2002) Mai1p is essential for maturation of proaminopeptidase I but not for autophagy. FEBS Lett. 512, 173-179.
6. Bateman, A., Coin, L., Durbin, R. et al. (2004) The Pfam protein families database. Nucleic Acids Res. 32, 138-141.
7. Bruno, W.J., Socci, N.D. and Halpern, A.L. (2000) Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol. 17, 189-197.
8. Chapman, D.J. (1988) Qualitative analysis of pigments. In Experimental Phycology: A Laboratory Manual (Lobban, C.S., Chapman, D.J. and Kremer, B.P., eds). New York: Cambridge University Press, pp. 93-103.
9. Chen, M.H., Liu, L.F., Chen, Y.R., Wu, H.K. and Yu, S.M. (1994) Expression of α-amylases, carbohydrate metabolism and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J. 6, 625-636.
10. Chuang, C.F. and Meyerowitz, E.M. (2000) Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 97, 4985-4990.
11. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
12. Contento, A.L., Kim, S.J. and Bassham, D.C. (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to sue starvation. Plant Physiol. 135, 2330-2347.
13. Contento, A.L., Xiong, Y. and Bassham, D.C. (2005) Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J. in press.
14. Duelling, J.H., Walker, J.M., Friedman, E.M., Thompson, A.R. and Vierstra, R.D. (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277, 33105-33114.
15. Dove, S.K., Piper, R.C., McEwen, R.K. et al. (2004) Svplp defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J. 23, 1922-1933.
16. Felsenstein, J. (2002) PHYLIP (Phytogeny Inference Package), Version 3.6.2. Seattle: University of Washington.
17. Georgakopoulos, T., Koutroubas, G., Vakonakis, I., Tzermia, M., Prokova, V., Voutsina, A. and Alexandraki, D. (2001) Functional analysis of the Saccharomyces cerevisiae YFR021w/YGR223c/YPL100w ORF family suggests relations to mitochondrial/peroxisomal functions and amino acid signalling pathways. Yeast, 18, 1155-1171.
18. Guan, J., Stromhaug, P.E., George, M.D., Habibzadegah-Tari, P., Bevan, A., Dunn, W.A. and Klionsky, D.J. (2001) Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol. Biol. Cell, 12, 3821-3838.
19. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S. and Ohsumi, Y. (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129, 1181-1193.
20. Harding, T.M., Morano, K.A., Scott, S.V. and Klionsky, D.J. (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131, 591-602.
21. Ishihara, N., Hamasaki, M., Yokota, S., Suzuki, K., Kamada, Y., Kihara, A., Yoshimori, T., Noda, T. and Ohsumi, Y. (2001) Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell, 12, 3690-3702.
22. Kelley, LA., MacCallum, R.M. and Sternberg, M.J.E. (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 499-520.
23. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T. and Ohsumi, Y. (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446.
24. Klionsky, D.J. (ed.) (2004) Autophagy: an overview. In Autophagy. Georgetown, TX: Landes Bioscience, pp. 1-10.
25. Klionsky, D.J. and Ohsumi, Y. (1999) Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 1-32.
26. Lang, T., Reiche, S., Straub, M., Bredschneider, M. and Thumm, M. (2000) Autophagy and the cvt pathway both depend on AUT9. J. Bacteriol. 182, 2125-2133.
27. Levanony, H., Rubin, R., Altschuler, Y. and Galili, G. (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J. Cell Biol. 119, 1117-1128.
28. Matile, P. (1997) The vacuole and cell senescence. Adv. Bot. Res. 25, 87-111.
29. Meiling-Wesse, K., Barth, H., Voss, C., Eskelinen, E.L., Epple, U.D. and Thumm, M. (2004) Atg21 is required for effective recruitment of Atg8 to the preautophagosomal structure during the Cvt pathway. J. Biol. Chem. 279, 37741-37750.
30. Mersereau, M., Pazour, G.J. and Das, A. (1990) Efficient transformation of Agrobacterium tumefaciens by electroporation. Gene, 90, 149-151.
31. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M. and Ohsumi, Y. (1998) A protein conjugation system essential for autophagy. Nature, 395, 395-398.
32. Moriyasu, Y. and Ohsumi, Y. (1996) Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiol. 111, 1233-1241.
33. Munafo, D.B. and Colombo, M.I. (2001) A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J. Cell Sci. 114, 3619-3629.
34. Noda, T., Kim, J., Huang, W.P., Baba, M., Tokunaga, C., Ohsumi, Y. and Klionsky, D.J. (2000) Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J. Cell Biol. 148, 465-480.
35. Reggiori, F., Tucker, K.A., Stromhaug, P.E. and Klionsky, D.J. (2004) The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell, 6, 79-90.
36. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. and Mittler, R. (2004) When defense pathways collide. The response of Arabidopsisto a combination of drought and heat stress. Plant Physiol. 134, 1683-1696.
37. Rojo, E., Gillmor, C.S., Kovaleva, V., Somerville, C.R. and Raikhel, N.V. (2001) VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell, 1, 303-310.
38. Sanderfoot, A.A., Pilgrim, M., Adam, L. and Raikhel, N.V. (2001) Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell, 13, 659-666.
39. Scott, S.V., Hefner-Gravink, A., Morano, K.A., Noda, T., Ohsumi, Y. and Klionsky, D.J. (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl Acad. Sci. USA, 93, 12304-12308.
40. Scott, S.V., Nice, D.C., Nau, J.J., Weisman, L.S., Kamada, Y., Keizer-Gunnink, I., Funakoshi, T., Veenhuis, M., Ohsumi, Y. and Klionsky, D.J. (2000) Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J. Biol. Chem. 275, 25840-25849.
41. Sheen, J. (2002) A transient expression assay using Arabidopsis mesophyll protoplasts. http://genetics.mgh.harvard.edu/sheen-web/
42. Shimodaira, H. and Hasegawa, M. (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics, 17, 1246-1247.
43. Strimmer, K. and von Haeseler, A. (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964-969.
44. Stromhaug, P.E., Reggiori, F., Guan, J., Wang, C.W. and Klionsky, D.J. (2004) Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol. Biol. Cell, 15, 3553-3566.
45. Surpin, M., Zheng, H., Morita, M.T. 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.
46. Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T. and Ohsumi, Y. (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971-5981.
47. Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. and Wolf, D.H. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349, 275-280.
48. Tsukada, M. and Ohsumi, Y. (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174.
49. Weaver, L.M., Gan, S., Quirino, B. and Amasino, R.M. (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37, 455-469.
50. Yang, Z. (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
51. Yoshimori, T. and Mizushima, N. (2004) Mammalian homologues of yeast autophagy proteins. In Autophagy (Klionsky, D.J., ed.). Georgetown, TX: Landes Bioscience, pp. 202-207.