Pyruvate serves as a metabolic precursor for many plastid-localized biosynthetic pathways, such as those for fatty acids1, terpenoids2 and branched-chain amino acids3. In spite of the importance of pyruvate uptake into plastids (organelles within cells of plants and algae), the molecular mechanisms of this uptake have not yet been explored. This is mainly because pyruvate is a relatively small compound that is able to passively permeate lipid bilayers4, which precludes accurate measurement of pyruvate transport activity in reconstituted liposomes. Using differential transcriptome analyses of C3 and C4 plants of the genera Flaveria and Cleome, here we have identified a novel gene that is abundant in C4 species, named BASS2 (BILE ACID:SODIUM SYMPORTER FAMILY PROTEIN 2). The BASS2 protein is localized at the chloroplast envelope membrane, and is highly abundant in C4 plants that have the sodium-dependent pyruvate transporter. Recombinant BASS2 shows sodium-dependent pyruvate uptake activity. Sodium influx is balanced by a sodium:proton antiporter (NHD1), which was mimicked in recombinant Escherichia coli cells expressing both BASS2 and NHD1. Arabidopsis thaliana bass2 mutants lack pyruvate uptake into chloroplasts, which affects plastid-localized isopentenyl diphosphate synthesis, as evidenced by increased sensitivity of such mutants to mevastatin, an inhibitor of cytosolic isopentenyl diphosphate biosynthesis. We thus provide molecular evidence for a sodium-coupled metabolite transporter in plastid envelopes. Orthologues of BASS2 can be detected in all the genomes of land plants that have been characterized so far, thus indicating the widespread importance of sodium-coupled pyruvate import into plastids.
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We thank G. Schönknecht, S. Yamaguchi and Y. Kamiya for discussions; N. Das, S. von Caemmerer and R. T. Furbank for critical reading of the manuscript; R. F. Sage, T. Endo, M. Munekage, J. Hibberd and M. Ku for gifts of seeds; T. Kinoshita for technical advice on the BASS2 immunoblot analysis; N. Aoki and S. Koreeda for technical advice on the pyruvate-uptake measurements; A. Izumida for preparation of the F. trinervia cDNA library; and Y. Takahashi for suggesting the dual expression system. This work was supported in part by the Ministry of Education, Science and Culture of Japan (Grants-in-Aid for Scientific Research to T.F. and K.I.), by a Sasakawa Scientific Research Grant from the Japan Science Society to T.F., and by the German Research Foundation (CRC-TR1 and IRTG 1525/1 to A.P.M.W., and CRC 590 to P.W.).
The authors declare no competing financial interests.
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Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y. et al. A plastidial sodium-dependent pyruvate transporter. Nature 476, 472–475 (2011). https://doi.org/10.1038/nature10250
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