Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis

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Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis. / Busch, Florian A; Tominaga, Jun; Muroya, Masato; Shirakami, Norihiko; Takahashi, Shunichi; Yamori, Wataru; Kitaoka, Takuya; Milward, Sara E; Nishimura, Kohji; Matsunami, Erika; Toda, Yosuke; Higuchi, Chikako; Muranaka, Atsuko; Takami, Tsuneaki; Watanabe, Shunsuke; Kinoshita, Toshinori; Sakamoto, Wataru; Sakamoto, Atsushi; Shimada, Hiroshi.

In: Plant Journal, Vol. 102, No. 1, 04.2020, p. 129-137.

Research output: Contribution to journalArticlepeer-review

Harvard

Busch, FA, Tominaga, J, Muroya, M, Shirakami, N, Takahashi, S, Yamori, W, Kitaoka, T, Milward, SE, Nishimura, K, Matsunami, E, Toda, Y, Higuchi, C, Muranaka, A, Takami, T, Watanabe, S, Kinoshita, T, Sakamoto, W, Sakamoto, A & Shimada, H 2020, 'Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis', Plant Journal, vol. 102, no. 1, pp. 129-137. https://doi.org/10.1111/tpj.14617

APA

Busch, F. A., Tominaga, J., Muroya, M., Shirakami, N., Takahashi, S., Yamori, W., Kitaoka, T., Milward, S. E., Nishimura, K., Matsunami, E., Toda, Y., Higuchi, C., Muranaka, A., Takami, T., Watanabe, S., Kinoshita, T., Sakamoto, W., Sakamoto, A., & Shimada, H. (2020). Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis. Plant Journal, 102(1), 129-137. https://doi.org/10.1111/tpj.14617

Vancouver

Author

Busch, Florian A ; Tominaga, Jun ; Muroya, Masato ; Shirakami, Norihiko ; Takahashi, Shunichi ; Yamori, Wataru ; Kitaoka, Takuya ; Milward, Sara E ; Nishimura, Kohji ; Matsunami, Erika ; Toda, Yosuke ; Higuchi, Chikako ; Muranaka, Atsuko ; Takami, Tsuneaki ; Watanabe, Shunsuke ; Kinoshita, Toshinori ; Sakamoto, Wataru ; Sakamoto, Atsushi ; Shimada, Hiroshi. / Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis. In: Plant Journal. 2020 ; Vol. 102, No. 1. pp. 129-137.

Bibtex

@article{4551653feaf64d3ba6bec87e5004b6f2,
title = "Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis",
abstract = "Bundle Sheath Defective 2, BSD2, is a stroma-targeted protein initially identified as a factor required for the biogenesis of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) in maize. Plants and algae universally have a homologous gene for BSD2 and its deficiency causes a RuBisCO-less phenotype. As RuBisCO can be the rate-limiting step in CO2 assimilation, the overexpression of BSD2 might improve photosynthesis and productivity through the accumulation of RuBisCO. To examine this hypothesis, we produced BSD2 overexpression lines in Arabidopsis. Compared with wild type, the BSD2 overexpression lines BSD2ox-2 and BSD2ox-3 expressed 4.8-fold and 8.8-fold higher BSD2 mRNA, respectively, whereas the empty-vector (EV) harbouring plants had a comparable expression level. The overexpression lines showed a significantly higher CO2 assimilation rate per available CO2 and productivity than EV plants. The maximum carboxylation rate per total catalytic site was accelerated in the overexpression lines, while the number of total catalytic sites and RuBisCO content were unaffected. We then isolated recombinant BSD2 (rBSD2) from E. coli and found that rBSD2 reduces disulfide bonds using reductants present in vivo, for example glutathione, and that rBSD2 has the ability to reactivate RuBisCO that has been inactivated by oxidants. Furthermore, 15% of RuBisCO freshly isolated from leaves of EV was oxidatively inactivated, as compared with 0% in BSD2-overexpression lines, suggesting that the overexpression of BSD2 maintains RuBisCO to be in the reduced active form in vivo. Our results demonstrated that the overexpression of BSD2 improves photosynthetic efficiency in Arabidopsis and we conclude that it is involved in mediating RuBisCO activation.",
keywords = "Arabidopsis thaliana, BSD2, RuBisCO, Zn finger domain, disulfide bonds, oxidative stress, protein disulfide reductase, redox",
author = "Busch, {Florian A} and Jun Tominaga and Masato Muroya and Norihiko Shirakami and Shunichi Takahashi and Wataru Yamori and Takuya Kitaoka and Milward, {Sara E} and Kohji Nishimura and Erika Matsunami and Yosuke Toda and Chikako Higuchi and Atsuko Muranaka and Tsuneaki Takami and Shunsuke Watanabe and Toshinori Kinoshita and Wataru Sakamoto and Atsushi Sakamoto and Hiroshi Shimada",
note = "Funding Information: We are grateful to Spencer M. Whitney, Susanne von Caemmerer (both at The Australian National University) and Yoshiko Tateishi (Hiroshima University) for a gift of anti‐BSD2 antibody and their advice and technical assistance with the in vitro RuBisCO activity assays. This work was supported in part by a JSPS KAKENHI Grant Number 26450081 (HS), 16H06552 (WY), A‐STEP from the Japan Science and Technology Agency (HS), the Ministry of Education, Culture, Sports, Science and Technology (MEXT) as part of Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University in Japan (HS), grants from the Advanced Low Carbon Technology Research and Development Program from the Japan Science and Technology Agency (ST, TK, and HS), and the Join Usage/Research Center, Institute of Plant Science and Resources, Okayama University (HS), and the Japan Society for the Promotion of Science under the Japan‐UK Research Cooperative Program from the Ministry of Education, Culture, Sports, Science and Technology of Japan (TK). JT is supported by Research Fellowships for Young Scientists from JSPS, and FAB is supported by the Australian Government through the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE1401000015). Publisher Copyright: {\textcopyright} 2019 The Authors The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",
year = "2020",
month = apr,
doi = "10.1111/tpj.14617",
language = "English",
volume = "102",
pages = "129--137",
journal = "The Plant journal : for cell and molecular biology",
issn = "0960-7412",
publisher = "Wiley",
number = "1",

}

RIS

TY - JOUR

T1 - Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis

AU - Busch, Florian A

AU - Tominaga, Jun

AU - Muroya, Masato

AU - Shirakami, Norihiko

AU - Takahashi, Shunichi

AU - Yamori, Wataru

AU - Kitaoka, Takuya

AU - Milward, Sara E

AU - Nishimura, Kohji

AU - Matsunami, Erika

AU - Toda, Yosuke

AU - Higuchi, Chikako

AU - Muranaka, Atsuko

AU - Takami, Tsuneaki

AU - Watanabe, Shunsuke

AU - Kinoshita, Toshinori

AU - Sakamoto, Wataru

AU - Sakamoto, Atsushi

AU - Shimada, Hiroshi

N1 - Funding Information: We are grateful to Spencer M. Whitney, Susanne von Caemmerer (both at The Australian National University) and Yoshiko Tateishi (Hiroshima University) for a gift of anti‐BSD2 antibody and their advice and technical assistance with the in vitro RuBisCO activity assays. This work was supported in part by a JSPS KAKENHI Grant Number 26450081 (HS), 16H06552 (WY), A‐STEP from the Japan Science and Technology Agency (HS), the Ministry of Education, Culture, Sports, Science and Technology (MEXT) as part of Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University in Japan (HS), grants from the Advanced Low Carbon Technology Research and Development Program from the Japan Science and Technology Agency (ST, TK, and HS), and the Join Usage/Research Center, Institute of Plant Science and Resources, Okayama University (HS), and the Japan Society for the Promotion of Science under the Japan‐UK Research Cooperative Program from the Ministry of Education, Culture, Sports, Science and Technology of Japan (TK). JT is supported by Research Fellowships for Young Scientists from JSPS, and FAB is supported by the Australian Government through the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE1401000015). Publisher Copyright: © 2019 The Authors The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/4

Y1 - 2020/4

N2 - Bundle Sheath Defective 2, BSD2, is a stroma-targeted protein initially identified as a factor required for the biogenesis of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) in maize. Plants and algae universally have a homologous gene for BSD2 and its deficiency causes a RuBisCO-less phenotype. As RuBisCO can be the rate-limiting step in CO2 assimilation, the overexpression of BSD2 might improve photosynthesis and productivity through the accumulation of RuBisCO. To examine this hypothesis, we produced BSD2 overexpression lines in Arabidopsis. Compared with wild type, the BSD2 overexpression lines BSD2ox-2 and BSD2ox-3 expressed 4.8-fold and 8.8-fold higher BSD2 mRNA, respectively, whereas the empty-vector (EV) harbouring plants had a comparable expression level. The overexpression lines showed a significantly higher CO2 assimilation rate per available CO2 and productivity than EV plants. The maximum carboxylation rate per total catalytic site was accelerated in the overexpression lines, while the number of total catalytic sites and RuBisCO content were unaffected. We then isolated recombinant BSD2 (rBSD2) from E. coli and found that rBSD2 reduces disulfide bonds using reductants present in vivo, for example glutathione, and that rBSD2 has the ability to reactivate RuBisCO that has been inactivated by oxidants. Furthermore, 15% of RuBisCO freshly isolated from leaves of EV was oxidatively inactivated, as compared with 0% in BSD2-overexpression lines, suggesting that the overexpression of BSD2 maintains RuBisCO to be in the reduced active form in vivo. Our results demonstrated that the overexpression of BSD2 improves photosynthetic efficiency in Arabidopsis and we conclude that it is involved in mediating RuBisCO activation.

AB - Bundle Sheath Defective 2, BSD2, is a stroma-targeted protein initially identified as a factor required for the biogenesis of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) in maize. Plants and algae universally have a homologous gene for BSD2 and its deficiency causes a RuBisCO-less phenotype. As RuBisCO can be the rate-limiting step in CO2 assimilation, the overexpression of BSD2 might improve photosynthesis and productivity through the accumulation of RuBisCO. To examine this hypothesis, we produced BSD2 overexpression lines in Arabidopsis. Compared with wild type, the BSD2 overexpression lines BSD2ox-2 and BSD2ox-3 expressed 4.8-fold and 8.8-fold higher BSD2 mRNA, respectively, whereas the empty-vector (EV) harbouring plants had a comparable expression level. The overexpression lines showed a significantly higher CO2 assimilation rate per available CO2 and productivity than EV plants. The maximum carboxylation rate per total catalytic site was accelerated in the overexpression lines, while the number of total catalytic sites and RuBisCO content were unaffected. We then isolated recombinant BSD2 (rBSD2) from E. coli and found that rBSD2 reduces disulfide bonds using reductants present in vivo, for example glutathione, and that rBSD2 has the ability to reactivate RuBisCO that has been inactivated by oxidants. Furthermore, 15% of RuBisCO freshly isolated from leaves of EV was oxidatively inactivated, as compared with 0% in BSD2-overexpression lines, suggesting that the overexpression of BSD2 maintains RuBisCO to be in the reduced active form in vivo. Our results demonstrated that the overexpression of BSD2 improves photosynthetic efficiency in Arabidopsis and we conclude that it is involved in mediating RuBisCO activation.

KW - Arabidopsis thaliana

KW - BSD2

KW - RuBisCO

KW - Zn finger domain

KW - disulfide bonds

KW - oxidative stress

KW - protein disulfide reductase

KW - redox

UR - http://www.scopus.com/inward/record.url?scp=85077160652&partnerID=8YFLogxK

U2 - 10.1111/tpj.14617

DO - 10.1111/tpj.14617

M3 - Article

C2 - 31755157

VL - 102

SP - 129

EP - 137

JO - The Plant journal : for cell and molecular biology

JF - The Plant journal : for cell and molecular biology

SN - 0960-7412

IS - 1

ER -