Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A plastidial sodium-dependent pyruvate transporter

A Corrigendum to this article was published on 28 September 2011

This article has been updated


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: The novel C 4 -associated transcripts encoding plastid-targeted membrane proteins.
Figure 2: BASS2 protein levels.
Figure 3: Pyruvate uptake activity.
Figure 4: BASS2 function in A. thaliana.

Accession codes

Primary accessions


Data deposits

cDNA sequences for F. trinervia BASS2, F. trinervia BASS4 and F. bidentis NHD1 have been deposited in the DNA Data Bank of Japan, with respective accession numbers AB522102, AB522103 and AB642169.

Change history

  • 17 October 2011

    Parts of the Supplementary Information were inadvertently not uploaded and the file was also corrupted; this has been corrected.


  1. 1

    Schwender, J., Ohlrogge, J. & Shachar-Hill, Y. Understanding flux in plant metabolic networks. Curr. Opin. Plant Biol. 7, 309–317 (2004)

    CAS  Article  Google Scholar 

  2. 2

    Hemmerlin, A. et al. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco Bright Yellow-2 cells. J. Biol. Chem. 278, 26666–26676 (2003)

    CAS  Article  Google Scholar 

  3. 3

    Schulze-Siebert, D., Heineke, D., Scharf, H. & Schultz, G. Pyruvate-derived amino acids in spinach chloroplasts: synthesis and regulation during photosynthetic carbon metabolism. Plant Physiol. 76, 465–471 (1984)

    CAS  Article  Google Scholar 

  4. 4

    Proudlove, M. O. & Thurman, D. A. The uptake of 2-oxoglutarate and pyruvate by isolated pea chloroplasts. New Phytol. 88, 255–264 (1981)

    CAS  Article  Google Scholar 

  5. 5

    Bräutigam, A., Hoffmann-Benning, S. & Weber, A. P. M. Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol. 148, 568–579 (2008)

    Article  Google Scholar 

  6. 6

    Huber, S. C. & Edwards, G. E. Transport in C4 mesophyll chloroplasts. Characterization of the pyruvate carrier. Biochim. Biophys. Acta 462, 583–602 (1977)

    CAS  Article  Google Scholar 

  7. 7

    Flügge, U. I., Stitt, M. & Heldt, H. W. Light-driven uptake of pyruvate into mesophyll chloroplasts from maize. FEBS Lett. 183, 335–339 (1985)

    Article  Google Scholar 

  8. 8

    Ohnishi, J. & Kanai, R. Pyruvate uptake induced by a pH jump in mesophyll chloroplasts of maize and sorghum, NADP-malic enzyme type C4 species. FEBS Lett. 269, 122–124 (1990)

    CAS  Article  Google Scholar 

  9. 9

    Ohnishi, J. & Kanai, R. Na+-induced uptake of pyruvate into mesophyll chloroplasts of a C4 plant, Panicum miliaceum . FEBS Lett. 219, 347–350 (1987)

    CAS  Article  Google Scholar 

  10. 10

    Aoki, N., Ohnishi, J. & Kanai, R. Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants — a comparative study. Plant Cell Physiol. 33, 805–809 (1992)

    CAS  Google Scholar 

  11. 11

    Weber, A. P. M. & von Caemmerer, S. Plastid transport and metabolism of C3 and C4 plants — comparative analysis and possible biotechnological exploitation. Curr. Opin. Plant Biol. 13, 1–9 (2010)

    Article  Google Scholar 

  12. 12

    McKown, A. D., Moncalvo, J.-M. & Dengler, N. G. Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am. J. Bot. 92, 1911–1928 (2005)

    CAS  Article  Google Scholar 

  13. 13

    Sawada, Y. et al. Arabidopsis bile acid:sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol. 50, 1579–1586 (2009)

    CAS  Article  Google Scholar 

  14. 14

    Gigolashvili, T. et al. The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana . Plant Cell 21, 1813–1829 (2009)

    CAS  Article  Google Scholar 

  15. 15

    Cellier, F. et al. Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. Plant J. 39, 834–846 (2004)

    CAS  Article  Google Scholar 

  16. 16

    Bräutigam, A. et al. An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiol. 155, 142–156 (2011)

    Article  Google Scholar 

  17. 17

    Majeran, W. et al. Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol. Cell. Proteomics 7, 1609–1638 (2008)

    CAS  Article  Google Scholar 

  18. 18

    Weber, A. P. M., Schwacke, R. & Flügge, U. I. Solute transporters of the plastid envelope membrane. Annu. Rev. Plant Biol. 56, 133–164 (2005)

    Article  Google Scholar 

  19. 19

    Suzuki, M. et al. Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels. Plant J. 37, 750–761 (2004)

    CAS  Article  Google Scholar 

  20. 20

    Aoki, N. & Kanai, R. Reappraisal of the role of sodium in the light-dependent active transport of pyruvate into mesophyll chloroplasts of C4 plants. Plant Cell Physiol. 38, 1217–1225 (1997)

    CAS  Article  Google Scholar 

  21. 21

    Sugden, M. C. & Holness, M. J. Trials, tribulations and finally, a transporter: the identification of the mitochondrial pyruvate transporter. Biochem. J. 374, e1–e2 (2003)

    CAS  Article  Google Scholar 

  22. 22

    Furumoto, T., Hata, S. & Izui, K. cDNA cloning and characterization of maize phosphoenolpyruvate carboxykinase, a bundle sheath cell-specific enzyme. Plant Mol. Biol. 41, 301–311 (1999)

    CAS  Article  Google Scholar 

  23. 23

    Furumoto, T. et al. Vascular-tissue abundant expression of plant TAF10, an orthologous gene for TATA box-binding protein-associated factor 10, in Flaveria trinervia and abnormal morphology of Arabidopsis thaliana transformants on its over-expression. Plant Cell Physiol. 46, 108–117 (2005)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Weber, A. P. M., Weber, K. L., Carr, K., Wilkerson, C. & Ohlrogge, J. B. Sampling the Arabidopsis transcriptome with massively parallel pyrosequencing. Plant Physiol. 144, 32–42 (2007)

    CAS  Article  Google Scholar 

  25. 25

    Furumoto, T., Izui, K., Quinn, V., Furbank, R. T. & von Caemmerer, S. Phosphorylation of phosphoenolpyruvate carboxylase is not essential for high photosynthetic rates in the C4 species Flaveria bidentis . Plant Physiol. 144, 1936–1945 (2007)

    CAS  Article  Google Scholar 

  26. 26

    Padan, E., Maisler, N., Taglicht, D., Karpel, R. & Schuldiner, S. Deletion of ant in Escherichia coli reveals its function in adaptation to high salinity and an alternative Na+/H+ antiporter system(s). J. Biol. Chem. 264, 20297–20302 (1989)

    CAS  PubMed  Google Scholar 

  27. 27

    Pavón, L. R. et al. Arabidopsis ANTR1 is a thylakoid Na-dependent phosphate transporter. J. Biol. Chem. 283, 13520–13527 (2008)

    Article  Google Scholar 

  28. 28

    Tsuchiya, T., Hasan, S. M. & Raven, J. Glutamate transport driven by an electrochemical gradient of sodium ions in Escherichia coli . J. Bacteriol. 131, 848–853 (1977)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Tamada, Y. et al. Temporary expression of the TAF10 gene and its requirement for normal development of Arabidopsis thaliana . Plant Cell Physiol. 48, 134–146 (2007)

    CAS  Article  Google Scholar 

Download references


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.).

Author information




T.Y. performed the differential screening and isolated the BASS2 gene. M.N. and Y.O.-I. analysed C4-abundant genes. Y.O.-I. prepared the bass2 mutants and revealed BASS2 expression. M.S. performed the confocal laser micro-scanning and the analyses of immunohistochemistry. J.O. and T.F. performed the pyruvate-uptake measurements on isolated chloroplasts, and A.B., A.P.M.W. and T.F. performed the E. coli whole-cell uptake measurements. U.G., P.W., A.B. and A.P.M.W. performed Flaveria and Cleome transcriptome analyses and the phylogenic analysis. S.H. was involved in designing the study, T.F. and K.I. designed the study, and T.F. and A.P.M.W. wrote the paper.

Corresponding author

Correspondence to Tsuyoshi Furumoto.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Text, Supplementary References and Supplementary Figures 1-12 with legends. This file was replaced on 17 October 2011 as the Supplementary Text and Supplementary References were omitted from the original file posted on line. (PDF 4233 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y. et al. A plastidial sodium-dependent pyruvate transporter. Nature 476, 472–475 (2011).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing