title: Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice.
abstract: Much of the nitrogen in leaves is distributed to chloroplasts, mainly in photosynthetic proteins. During leaf senescence, chloroplastic proteins, including Rubisco, are rapidly degraded, and the released nitrogen is remobilized and reused in newly developing tissues. Autophagy facilitates the degradation of intracellular components for nutrient recycling in all eukaryotes, and recent studies have revealed critical roles for autophagy in Rubisco degradation and nitrogen remobilization into seeds in Arabidopsis (Arabidopsis thaliana). Here, we examined the function of autophagy in vegetative growth and nitrogen usage in a cereal plant, rice (Oryza sativa). An autophagy-disrupted rice mutant, Osatg7-1, showed reduced biomass production and nitrogen use efficiency compared with the wild type. While Osatg7-1 showed early visible leaf senescence, the nitrogen concentration remained high in the senescent leaves. (15)N pulse chase analysis revealed suppression of nitrogen remobilization during leaf senescence in Osatg7-1. Accordingly, the reduction of nitrogen available for newly developing tissues in Osatg7-1 likely led its reduced leaf area and tillers. The limited leaf growth in Osatg7-1 decreased the photosynthetic capacity of the plant. Much of the nitrogen remaining in senescent leaves of Osatg7-1 was in soluble proteins, and the Rubisco concentration in senescing leaves of Osatg7-1 was about 2.5 times higher than in the wild type. Transmission electron micrographs showed a cytosolic fraction rich with organelles in senescent leaves of Osatg7-1. Our results suggest that autophagy contributes to efficient nitrogen remobilization at the whole-plant level by facilitating protein degradation for nitrogen recycling in senescent leaves.
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Shinya
authors: http://orcid.org/0000-0002-7932-159X
authors: S
authors: Wada
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Yasukzu
authors: Y
authors: Hayashida
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Masanori
authors: http://orcid.org/0000-0001-5222-9163
authors: M
authors: Izumi
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Takamitsu
authors: T
authors: Kurusu
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Shigeru
authors: http://orcid.org/0000-0002-5979-0436
authors: S
authors: Hanamata
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Keiichi
authors: http://orcid.org/0000-0002-3759-7643
authors: K
authors: Kanno
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Soichi
authors: S
authors: Kojima
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Tomoyuki
authors: http://orcid.org/0000-0002-3875-0216
authors: T
authors: Yamaya
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Kazuyuki
authors: http://orcid.org/0000-0001-8854-0375
authors: K
authors: Kuchitsu
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.).
authors: Amane
authors: A
authors: Makino
authors: Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan (S.W, Y.H., K.Ka., S.K., T.Y., A.M., H.I.); Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan (M.I.);Frontier Research Institute for Interdisciplinary Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai 980-8578, Japan (M.I.); School of Bioscience and Biotechnology, Tokyo University of Technology, Hachioji, Tokyo 192-0982, Japan (T.K.);Department of Applied Biological Science (T.K., S.H., K.Ku.), and Research Institute for Science and Technology (T.K., K.Ku.), Tokyo University of Science, Noda, Chiba 278-8510, Japan; andCREST, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan (A.M.) hiroyuki@biochem.tohoku.ac.jp.
authors: Hiroyuki
authors: http://orcid.org/0000-0002-8682-4566
authors: H
authors: Ishida
mesh_terms: D001343:Autophagy / Q000235:genetics; D018533:Biomass; D017343:Genes, Plant; D058503:Mesophyll Cells / Q000378:metabolism / Q000648:ultrastructure; D009154:Mutation / Q000235:genetics; D009584:Nitrogen / Q000378:metabolism*; D012275:Oryza / Q000033:anatomy & histology / Q000166:cytology* / Q000254:growth & development / Q000378:metabolism*; D010788:Photosynthesis; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism
chemical_list: D010940:Plant Proteins; D012273:Ribulose-Bisphosphate Carboxylase; D009584:Nitrogen