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 language | English |
|---|---|
| Pages (from-to) | 878-888 |
| Number of pages | 11 |
| Journal | Autophagy |
| Volume | 10 |
| Issue number | 5 |
| DOIs | |
| Publication status | Published - May 2014 |
| Externally published | Yes |
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All Science Journal Classification (ASJC) codes
- Molecular Biology
- Cell Biology
Cite this
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 journal › Article
}
TY - JOUR
T1 - OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development
AU - Kurusu, Takamitsu
AU - Koyano, Tomoko
AU - Hanamata, Shigeru
AU - Kubo, Takahiko
AU - Noguchi, Yuhei
AU - Yagi, Chikako
AU - Nagata, Noriko
AU - Yamamoto, Takashi
AU - Ohnishi, Takayuki
AU - Okazaki, Yozo
AU - Kitahata, Nobutaka
AU - Ando, Daichi
AU - Ishikawa, Masaya
AU - Wada, Shinya
AU - Miyao, Akio
AU - Hirochika, Hirohiko
AU - Shimada, Hiroaki
AU - Makino, Amane
AU - Saito, Kazuki
AU - Ishida, Hiroyuki
AU - Kinoshita, Tetsu
AU - Kurata, Nori
AU - Kuchitsu, Kazuyuki
PY - 2014/5
Y1 - 2014/5
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=84899751909&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84899751909&partnerID=8YFLogxK
U2 - 10.4161/auto.28279
DO - 10.4161/auto.28279
M3 - Article
C2 - 24674921
AN - SCOPUS:84899751909
VL - 10
SP - 878
EP - 888
JO - Autophagy
JF - Autophagy
SN - 1554-8627
IS - 5
ER -