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Plant Physiol, July 2002, Vol. 129, pp. 1181-1193

Leaf Senescence and Starvation-Induced Chlorosis Are Accelerated by the Disruption of an Arabidopsis Autophagy Gene1

Hideki Hanaoka, Takeshi Noda, Yumiko Shirano,2 Tomohiko Kato, Hiroaki Hayashi, Daisuke Shibata,3 Satoshi Tabata, and Yoshinori Ohsumi*

Department of Cell Biology, National Institute for Basic Biology, Nishigonaka 38, Myodaiji-cho, Okazaki 444-8585 Japan (H. Hanaoka, T.N., Y.O.); Department of Molecular Biomechanics, School of Life Science, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan (H. Hanaoka, T.N., Y.O.); Mitsui Plant Biotechnology Research Institute (disbanded in March 1999), Tsukuba, Ibaraki 305-0047, Japan (Y.S., D.S.); Kazusa DNA Research Institute, Yana 1532-3, Kisarazu, Chiba 292-0812, Japan (T.K., S.T.); and Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan (H. Hayashi)

Autophagy is an intracellular process for vacuolar bulk degradation of cytoplasmic components. The molecular machinery responsible for yeast and mammalian autophagy has recently begun to be elucidated at the cellular level, but the role that autophagy plays at the organismal level has yet to be determined. In this study, a genome-wide search revealed significant conservation between yeast and plant autophagy genes. Twenty-five plant genes that are homologous to 12 yeast genes essential for autophagy were discovered. We identified an Arabidopsis mutant carrying a T-DNA insertion within AtAPG9, which is the only ortholog of yeast Apg9 in Arabidopsis (atapg9-1). AtAPG9 is transcribed in every wild-type organ tested but not in the atapg9-1 mutant. Under nitrogen or carbon-starvation conditions, chlorosis was observed earlier in atapg9-1 cotyledons and rosette leaves compared with wild-type plants. Furthermore, atapg9-1 exhibited a reduction in seed set when nitrogen starved. Even under nutrient growth conditions, bolting and natural leaf senescence were accelerated in atapg9-1 plants. Senescence-associated genes SEN1 and YSL4 were up-regulated in atapg9-1 before induction of senescence, unlike in wild type. All of these phenotypes were complemented by the expression of wild-type AtAPG9 in atapg9-1 plants. These results imply that autophagy is required for maintenance of the cellular viability under nutrient-limited conditions and for efficient nutrient use as a whole plant.

1 This work was supported in part by the Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan.

2 Present address: Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853.

3 Present address: Kazusa DNA Research Institute, Yana 1532-3, Kisarazu, Chiba 292-0812, Japan.

* Corresponding author; e-mail yohsumi{at}nibb.ac.jp; fax 81-564-55-7516.

© 2002 American Society of Plant Physiologists


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