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

• Published in: The Plant journal : for cell and molecular biology Vol. 102; no. 1; pp. 129 - 137
• Main Authors: 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
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.04.2020; John Wiley and Sons Inc
• Subjects: Active sites; Algae; Arabidopsis; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis Proteins - physiology; Arabidopsis thaliana; Assimilation; BSD2; Carbon dioxide; Carboxylation; Disulfide bonds; E coli; Escherichia coli; Gene Expression Regulation, Plant; Glutathione; Homology; mRNA; Original; Oxidants; oxidative stress; Oxidizing agents; Oxygenase; Phenotypes; Photosynthesis; Photosynthesis - genetics; Productivity; protein disulfide reductase; Recombinant Proteins; redox; Ribulose-bisphosphate carboxylase; Ribulose-Bisphosphate Carboxylase - metabolism; RuBisCO; Sheaths; Stroma; Zn finger domain; Arabidopsis thaliana; BSD2; protein disulfide reductase; disulfide bonds; Zn finger domain; RuBisCO; oxidative stress; redox
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14617

Summary 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. Significance Statement Catalytic properties of RuBisCO are susceptible to oxidation of its thiols, but the underlying process resulting in a change in RuBisCO activation has been largely elusive. Here we identify BSD2, known as a chaperone for RuBisCO assembly, as a protein that takes an essential role in the redox homeostasis of mature RuBisCO. We show that overexpression of BSD2 improves RuBisCO carboxylation efficiency through manipulating the redox potential.