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 a few 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)



This family belongs to the .

 

References:

Cabrera, E., R. González-Montelongo, T. Giraldez, D. Alvarez de la Rosa, and J.M. Siverio. (2014). Molecular components of nitrate and nitrite efflux in yeast. Eukaryot. Cell. 13: 267-278.

Camarasa, C., F. Bidard, M. Bony, P. Barre, and S. Dequin. (2001). Characterization of Schizosaccharomyces pombe malate permease by expression in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 67: 4144-4151.

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.

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.

Duan, X., Y. Yu, H. Duanmu, C. Chen, X. Sun, L. Cao, Q. Li, X. Ding, B. Liu, and Y. Zhu. (2017). GsSLAH3, a Glycine soja slow type anion channel homologue, positively modulates plant bicarbonate stress tolerance. Physiol Plant. [Epub: Ahead of Print]

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.

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.

Kollist, H., M. Jossier, K. Laanemets, and S. Thomine. (2011). Anion channels in plant cells. FEBS J. 278: 4277-4292.

Léchenne, B., U. Reichard, C. Zaugg, M. Fratti, J. Kunert, O. Boulat, and M. Monod. (2007). Sulphite efflux pumps in Aspergillus fumigatus and dermatophytes. Microbiology 153: 905-913.

Liu, J., Z. Xie, H.D. Shin, J. Li, G. Du, J. Chen, and L. Liu. (2017). Rewiring the reductive tricarboxylic acid pathway and L-malate transport pathway of Aspergillus oryzae for overproduction of L-malate. J Biotechnol 253: 1-9.

Moraes, T.F. and R.A. Reithmeier. (2012). Membrane transport metabolons. Biochim. Biophys. Acta. 1818: 2687-2706.

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.

Osawa, H. and H. Matsumoto. (2006). Cytotoxic thio-malate is transported by both an aluminum-responsive malate efflux pathway in wheat and the MAE1 malate permease in Schizosaccharomyces pombe. Planta 224: 462-471.

Park, H., and A.T. Bakalinsky. (2000). SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. Yeast 16: 881-888.

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.

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.

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.

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.

Wang, C., J. Zhang, and J.I. Schroeder. (2017). Two-electrode Voltage-clamp Recordings in Xenopus laevis Oocytes: Reconstitution of Abscisic Acid Activation of SLAC1 Anion Channel via PYL9 ABA Receptor. Bio Protoc 7:.

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]

Zhang, A., H.M. Ren, Y.Q. Tan, G.N. Qi, F.Y. Yao, G.L. Wu, L.W. Yang, J. Hussain, S.J. Sun, and Y.F. Wang. (2016). S-type Anion Channels SLAC1 and SLAH3 Function as Essential Negative Regulators of Inward K+ Channels and Stomatal Opening in Arabidopsis. Plant Cell. [Epub: Ahead of Print]

Zhang, W. (2011). Roles of heterotrimeric G proteins in guard cell ion channel regulation. Plant Signal Behav 6: 986-990.

Examples:

TC#NameOrganismal TypeExample
2.A.16.1.1

Tellurite resistance protein, TehA.  Encoded in an operon with the gene for a tellurite S-adenosylmethionine-dependent methyl transferase.  Together they confer tellurite resistance (Moraes and Reithmeier 2012).

Bacteria

TehA of E. coli

 
2.A.16.1.2

Tellurite resistance protein TehA homologue. An anion channel involved in tellurite resistance.  A quasi-symmetrical homotrimer in which each subunit has 10 TMSs and forms a channel.  The crystal structure is known at 1.2 A resolution (Chen et al. 2010).  The helices are arranged from helical hairpin pairs to form a central 5-helix transmembrane pore that is gated by a conserved phenylalanine residue.  Gating is controlled by kinase activation.  Selectivity for various anions may be a function of the energetic cost of ion dehydration (Chen et al. 2010).

Bacteria

Tellurite resistance protein tehA homologue of Haemophilus influenzae

 
Examples:

TC#NameOrganismal TypeExample
2.A.16.2.1

Mae1 malate:proton symport protein.  May also transport other dicarboxylates such as oxaloacetate, malonate, succinate and fumarate (Camarasa et al. 2001). May also transport thio-malate (Osawa and Matsumoto 2006).

Yeast

Mae1 of Schizosaccharomyces pombe

 
2.A.16.2.2The ATP-dependent subtelomeric helicase, RecQ (2100 aas with a 5 TMS N-terminal domain (residues 43-210). 94% identical to 2.A.16.2.1 (malate transporter) of the same species. YeastRecQ of Schizosaccharomyces pombe (Q5EAK4)
 
2.A.16.2.3

C4-dicarboxylate transporter/malic acid transport protein, Mae1 of 395 aas and 10 TMSs.  It has been overexpressed for the production of L-malate (Liu et al. 2017).

Mae1 of Emericella nidulans (Aspergillus nidulans)

 
Examples:

TC#NameOrganismal TypeExample
2.A.16.3.1

The sulfite efflux (sulfite sensitivity) protein, SSU1. Expression is controlled by the FZF1-4 transcriptional activator; only free sulfite (not complexed sulfite) is exported (Park and Bakalinsky, 2000). Can also export nitrite and nitrate (Cabrera et al. 2014).  SSU1 has a putative 10 TMS topology in a (S-L)5 arrangement where S= a small putative TMS and L= a large TMS. 

Yeast

SSU1 of Saccharomyces cerevisiae (P41930)

 
2.A.16.3.2

Sulfite, nitrate exporter of 384 aas, Ssu1 (Cabrera et al. 2014).

Fungi

Ssu1 of Pichia angusta (Yeast) (Hansenula polymorpha)

 
2.A.16.3.3

Sulfite/nitrate exporter of 392 aas, Ssu2 (Cabrera et al. 2014).

Fungi

Ssu2 of Pichia angusta (Yeast) (Hansenula polymorpha)

 
Examples:

TC#NameOrganismal TypeExample
2.A.16.4.1

The unknown homologue, UnkH (same topology as 2.A.16.3.1)

Fungi

UnkH of Aspergillus niger (A2QYD7)

 
2.A.16.4.2Sulfite efflux pump, Ssul (Sulfite sensitivity protein) (Lechenne et al., 2007). FungiSsul of Arthroderma benhamiea (A3R044)
 
2.A.16.4.3Sulfite efflux pump, Ssul (Lechenne et al., 2007).FungiSsul of Aspergillus fumigatus (Q2TJJ2)
 
2.A.16.4.4Uncharacterized transporter MJ0762ArchaeaMJ0762 of Methanocaldococcus jannaschii
 
2.A.16.4.5

TDT homolouge

Archaea

TDT homologue of Sulfolobus acidocaldarius

 
2.A.16.4.6

TDT homologue

Actinobacteria

TDT homologue of Streptomyces coelicolor

 
Examples:

TC#NameOrganismal TypeExample
2.A.16.5.1

The plant guard cell S (Slow)-type anion channel, SLAC1 (based on activation kinetics of anion channel currents in response to voltage changes); functions in stomatal signalling, controls turgor pressure, and regulates the exchange of water and CO2 (Chen et al. 2010). Also called carbon dioxide insensitive (CDI3) and ozone sensitive (OZS1) (Kollist et al., 2011). Heterotrimeric G proteins regulate guard cell ion channels (Zhang, 2011). Evolutionary studies have been reported (Dreyer et al. 2012). The transmembrane region of guard cell SLAC1 channels detect CO2 signals via an abscisic acid (ABA)-independent pathway (Yamamoto et al. 2016).  SLAC1 is activated by the protein kinase OST1 (OPEN STOMATA 1), the Ca2+-dependent protein kinases (CPKs), the GHR1 (GUARD CELL HYDROGEN PEROXIDE-RESISTANT 1) transmembrane receptor-like protein (TC# 1.A.87.2.8), or the PYL5 abscisic acid (ABA) receptor (Q9FLB1)  (Wang et al. 2017).

Plants

SLAC1 of Arabidopsis thaliana
(Q9LD83)

 
2.A.16.5.2

Slow anion channel homologue-3, SLAH3; nitrate is both a substrate and a gate opener (Geiger et al. 2011). Slow, weak voltage-dependent S-type anion efflux channel involved in maintenance of anion homeostasis (Negi et al. 2008). Binds to the highly selective inward-rectifying potassium channel KAT1 and inhibits its activity. Functions as an essential negative regulator of inward potassium channels in guard cells. Essential for the efficient stomatal closure and opening in guard cells (Zhang et al. 2016). The plasma membrane Glycine soja (soy bean) GsSLAH3 protein contains ten TMSs. GsSLAH3 expression is induced by NaHCO3 treatment, suggesting an involvement to alkaline stress, and ectopic expression of GsSLAH3 in yeast increased sensitivity to alkali treatment (Duan et al. 2017). Overexpression of GsSLAH3 in Arabidopsis thaliana enhanced alkaline tolerance during germination, seedling and adult stages. Transgenic lines improved plant tolerance to KHCO3 rather than high pH treatment. Overexpressing lines accumulated more NO3- than wild type (Duan et al. 2017).

 

Plants

SLAH3 of Arabidopsis thaliana

 
Examples:

TC#NameOrganismal TypeExample
2.A.16.6.1

TDT homologue, TehA of 302aas and 10 TMSs

Firmicutes

TehA of Streptococcus pyogenes (Q9A061)

 
2.A.16.6.2

TehA homologue of 314aas and 10 TMSs

Firmicutes

TehA of Clostridium butyricum (C4IKV8)

 
2.A.16.6.3

Uncharacterized protein of 332 aas and 10 TMSs.

UP of Lactobacillus dextrinicus