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

Florian A. Busch, Jun Tominaga, Masato Muroya, Norihiko Shirakami, Shunichi Takahashi, Wataru Yamori, Takuya Kitaoka, Sara E. Milward, Kohji Nishimura, Erika Matsunami, Yosuke Toda, Chikako Higuchi, Atsuko Muranaka, Tsuneaki Takami, Shunsuke Watanabe, Toshinori Kinoshita, Wataru Sakamoto, Atsushi Sakamoto, Hiroshi Shimada

Research output: Contribution to journalArticle

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.

Original languageEnglish
JournalPlant Journal
DOIs
Publication statusAccepted/In press - Jan 1 2019

Fingerprint

Oxygenases
Photosynthesis
ribulose 1,5-diphosphate
oxygenases
Arabidopsis
photosynthesis
Growth
algae
active sites
assimilation (physiology)
Catalytic Domain
ribulose-1,5 diphosphate
reducing agents
carboxylation
disulfide bonds
Reducing Agents
Oxidants
oxidants
Disulfides
Zea mays

Keywords

  • Arabidopsis thaliana
  • BSD2
  • disulfide bonds
  • oxidative stress
  • protein disulfide reductase
  • redox
  • RuBisCO
  • Zn finger domain

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Busch, F. A., Tominaga, J., Muroya, M., Shirakami, N., Takahashi, S., Yamori, W., ... Shimada, H. (Accepted/In press). Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis. Plant Journal. https://doi.org/10.1111/tpj.14617

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, 01.01.2019.

Research output: Contribution to journalArticle

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 2019, 'Overexpression of BUNDLE SHEATH DEFECTIVE 2 improves the efficiency of photosynthesis and growth in Arabidopsis', Plant Journal. https://doi.org/10.1111/tpj.14617
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. 2019.
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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.",
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AU - Takahashi, Shunichi

AU - Yamori, Wataru

AU - Kitaoka, Takuya

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AU - Nishimura, Kohji

AU - Matsunami, Erika

AU - Toda, Yosuke

AU - Higuchi, Chikako

AU - Muranaka, Atsuko

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