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

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‐l...

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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
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Summary:	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.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work.
ISSN:	0960-7412 1365-313X
DOI:	10.1111/tpj.14617