OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development

Takamitsu Kurusu, Tomoko Koyano, Shigeru Hanamata, Takahiko Kubo, Yuhei Noguchi, Chikako Yagi, Noriko Nagata, Takashi Yamamoto, Takayuki Ohnishi, Yozo Okazaki, Nobutaka Kitahata, Daichi Ando, Masaya Ishikawa, Shinya Wada, Akio Miyao, Hirohiko Hirochika, Hiroaki Shimada, Amane Makino, Kazuki Saito, Hiroyuki IshidaTetsu Kinoshita, Nori Kurata, Kazuyuki Kuchitsu

Research output: Contribution to journalArticle

69 Citations (Scopus)

Abstract

In flowering plants, the tapetum, the innermost layer of the anther, provides both nutrient and lipid components to developing microspores, pollen grains, and the pollen coat. Though the programmed cell death of the tapetum is one of the most critical and sensitive steps for fertility and is affected by various environmental stresses, its regulatory mechanisms remain mostly unknown. Here we show that autophagy is required for the metabolic regulation and nutrient supply in anthers and that autophagic degradation within tapetum cells is essential for postmeiotic anther development in rice. Autophagosome-like structures and several vacuole-enclosed lipid bodies were observed in postmeiotic tapetum cells specifically at the uninucleate stage during pollen development, which were completely abolished in a retrotransposon-insertional OsATG7 (autophagy-related 7)-knockout mutant defective in autophagy, suggesting that autophagy is induced in tapetum cells. Surprisingly, the mutant showed complete sporophytic male sterility, failed to accumulate lipidic and starch components in pollen grains at the flowering stage, showed reduced pollen germination activity, and had limited anther dehiscence. Lipidomic analyses suggested impairment of editing of phosphatidylcholines and lipid desaturation in the mutant during pollen maturation. These results indicate a critical involvement of autophagy in a reproductive developmental process of rice, and shed light on the novel autophagy-mediated regulation of lipid metabolism in eukaryotic cells.

Original languageEnglish
Pages (from-to)878-888
Number of pages11
JournalAutophagy
Volume10
Issue number5
DOIs
Publication statusPublished - May 2014
Externally publishedYes

Fingerprint

Autophagy
Pollen
Lipid Metabolism
Lipids
Food
Retroelements
Male Infertility
Eukaryotic Cells
Germination
Vacuoles
Phosphatidylcholines
Starch
Fertility
Oryza
Cell Death

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Cell Biology

Cite this

Kurusu, T., Koyano, T., Hanamata, S., Kubo, T., Noguchi, Y., Yagi, C., ... Kuchitsu, K. (2014). OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy, 10(5), 878-888. https://doi.org/10.4161/auto.28279

OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. / Kurusu, Takamitsu; Koyano, Tomoko; Hanamata, Shigeru; Kubo, Takahiko; Noguchi, Yuhei; Yagi, Chikako; Nagata, Noriko; Yamamoto, Takashi; Ohnishi, Takayuki; Okazaki, Yozo; Kitahata, Nobutaka; Ando, Daichi; Ishikawa, Masaya; Wada, Shinya; Miyao, Akio; Hirochika, Hirohiko; Shimada, Hiroaki; Makino, Amane; Saito, Kazuki; Ishida, Hiroyuki; Kinoshita, Tetsu; Kurata, Nori; Kuchitsu, Kazuyuki.

In: Autophagy, Vol. 10, No. 5, 05.2014, p. 878-888.

Research output: Contribution to journalArticle

Kurusu, T, Koyano, T, Hanamata, S, Kubo, T, Noguchi, Y, Yagi, C, Nagata, N, Yamamoto, T, Ohnishi, T, Okazaki, Y, Kitahata, N, Ando, D, Ishikawa, M, Wada, S, Miyao, A, Hirochika, H, Shimada, H, Makino, A, Saito, K, Ishida, H, Kinoshita, T, Kurata, N & Kuchitsu, K 2014, 'OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development', Autophagy, vol. 10, no. 5, pp. 878-888. https://doi.org/10.4161/auto.28279
Kurusu, Takamitsu ; Koyano, Tomoko ; Hanamata, Shigeru ; Kubo, Takahiko ; Noguchi, Yuhei ; Yagi, Chikako ; Nagata, Noriko ; Yamamoto, Takashi ; Ohnishi, Takayuki ; Okazaki, Yozo ; Kitahata, Nobutaka ; Ando, Daichi ; Ishikawa, Masaya ; Wada, Shinya ; Miyao, Akio ; Hirochika, Hirohiko ; Shimada, Hiroaki ; Makino, Amane ; Saito, Kazuki ; Ishida, Hiroyuki ; Kinoshita, Tetsu ; Kurata, Nori ; Kuchitsu, Kazuyuki. / OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. In: Autophagy. 2014 ; Vol. 10, No. 5. pp. 878-888.
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