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2.A.16 The Tellurite-resistance/Dicarboxylate Transporter (TDT) Family


The TDT family includes members from the bacterial (E. coli and Haemophilus influenzae), archaeal (Methanococcus jannaschii) and eukaryotic (Schizosaccharomyces pombe) kingdoms and therefore occurs ubiquitously. Only three members of the family have been functionally characterized. One is the TehA protein of E. coli which functions as a tellurite-resistance uptake permease; the second is the Mae1 protein of S. pombe which functions in the uptake of malate and other dicarboxylates by a proton symport mechanism, the third is the sulfite efflux pump of Saccharomyces cerevisiae (Park and Bakalinsky, 2000). These proteins are 320-460 aas, but some are larger. The homologues contain an internal repeat. They exhibit 10 putative transmembrane α-helical spanners (TMSs). The phylogenetic tree for the TDT family exhibits three major branches, one for the bacterial proteins, one for the archaeal proteins and one for the yeast protein. (Saier et al., 1999).

Stomatal pores, formed by two surrounding guard cells in the epidermis of plant leaves, allow influx of atmospheric carbon dioxide in exchange for transpirational water loss. Stomata also restrict the entry of ozone - an important air pollutant that has an increasingly negative impact on crop yields, and thus global carbon fixation and climate change. The aperture of stomatal pores is regulated by the transport of osmotically active ions and metabolites across guard cell membranes.

Guard cell anion channels function as important regulators of stomatal closure and are essential in mediating stomatal responses to physiological and stress stimuli. Vahisalu et al. (2008) and Negi et al. (2008) have identified an ozone-sensitive Arabidopsis thaliana mutant, slac1. They found that SLAC1 (SLOW ANION CHANNEL-ASSOCIATED 1) is preferentially expressed in guard cells and encodes a distant homologue of the Tellurite-resistance/Dicarboxylate transporter family with closest resemblance to TehA (2.A.16.1.1; 20% identity, 38% similarity, e-11). The plasma membrane protein SLAC1 is essential for stomatal closure in response to CO2, abscisic acid, ozone, light/dark transitions, humidity change, calcium ions, hydrogen peroxide and nitric oxide. Mutations in SLAC1 impair slow (S-type) anion channel currents that are activated by cytosolic Ca2+ and abscisic acid, but do not affect rapid (R-type) anion channel currents or Ca2+ channel function.


The transport reaction catalyzed by the TehA protein of E. coli is:


Tellurite (out) + nH+ (out) → Tellurite (in) + nH+ (in).


The transport reaction catalyzed by the Mae1 protein of S. pombe is:


C4-Dicarboxylate (out) + nH+ (out) C4-Dicarboxylate (in) + nH+ (in).


The transport reaction catalyzed by the Ssu1 protein is:

sulfite (in)→sulfite (out)

References associated with 2.A.16 family:

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Chen, Y.H., L. Hu, M. Punta, R. Bruni, B. Hillerich, B. Kloss, B. Rost, J. Love, S.A. Siegelbaum, and W.A. Hendrickson. (2010). Homologue structure of the SLAC1 anion channel for closing stomata in leaves. Nature 467: 1074-1080. 20981093
Dreyer, I., J.L. Gomez-Porras, D.M. Riaño-Pachón, R. Hedrich, and D. Geiger. (2012). Molecular Evolution of Slow and Quick Anion Channels (SLACs and QUACs/ALMTs). Front Plant Sci 3: 263. 23226151
Geiger, D., T. Maierhofer, K.A. Al-Rasheid, S. Scherzer, P. Mumm, A. Liese, P. Ache, C. Wellmann, I. Marten, E. Grill, T. Romeis, and R. Hedrich. (2011). Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4: ra32. 21586729
Grobler, J., F. Bauer, R.E. Subden, and H.J. Van Vuuren. (1995). The mae1 gene of Schizosaccharomyces pombe encodes a permease for malate and other C4 dicarboxylic acids. Yeast 11: 1485-1491. 8750236
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Negi, J., O. Matsuda, T. Nagasawa, Y. Oba, H. Takahashi, M. Kawai-Yamada, H. Uchimiya, M. Hashimoto, and K. Iba. (2008). CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature. 452: 483-486. 18305482
Park, H., and A.T. Bakalinsky. (2000). SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. Yeast 16: 881-888. 10870099
Saier, M.H., Jr., B.H. Eng, S. Fard, J. Garg, D.A. Haggerty, W.J. Hutchinson, D.L. Jack, E.C. Lai, H.J. Liu, D.P. Nusinew, A.M. Omar, S.S. Pao, I.T. Paulsen, J.A. Quan, M. Sliwinski, T.-T. Tseng, S. Wachi and G.B. Young (1999). Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochem. Biophys. Acta 1422: 1-56. 10082980
Taylor, D.E., Y. Hou, R.J. Turner, and J.H. Weiner (1994). Location of a potassium tellurite resistance operon (tehA tehB) within the terminus of Escherichia coli K-12. J. Bacteriol. 176: 2740—2742. 8169225
Vahisalu, T., H. Kollist, Y.F. Wang, N. Nishimura, W.Y. Chan, G. Valerio, A. Lamminmäki, M. Brosché, H. Moldau, R. Desikan, J.I. Schroeder, and J. Kangasjärvi. (2008). SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature. 452: 487-491. 18305484
Walter, E.G., J.H. Weiner, and D.E. Taylor (1990). Nucleotide sequence and overexpression of the tellurite-resistance determinant from the IncHII plasmid pHH1508a. Gene 101: 1—7. 2060788
Yamamoto, Y., J. Negi, C. Wang, Y. Isogai, J.I. Schroeder, and K. Iba. (2016). The Transmembrane Region of Guard Cell SLAC1 Channels Perceives CO2 Signals via an ABA-Independent Pathway in Arabidopsis. Plant Cell. [Epub: Ahead of Print] 26764376
Zhang, W. (2011). Roles of heterotrimeric G proteins in guard cell ion channel regulation. Plant Signal Behav 6: 986-990. 21617376