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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 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). Fungal carboxylate transporters have been reviewed (Wu et al. 2023).

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. Stomatal movement is orchestrated by diverse signaling cascades and metabolic activities in guard cells (Chang et al. 2023). Light triggers the opening of the pores through the phototropin-mediated pathway, which leads to the activation of plasma membrane H+-ATPase and thereby facilitates potassium accumulation through K+(in) channels. Chang et al. 2023 showed that the stomatal response to light is negatively regulated by 12-oxo-phytodienoic acid (OPDA), an oxylipin metabolite produced through enzymatic oxygenation of polyunsaturated fatty acids (PUFAs). A set of phospholipase-encoding genes, phospholipase (PLIP)1/2/3 are transactivated rapidly in guard cells upon illumination in a phototropin-dependent manner. These phospholipases release PUFAs from the chloroplast membrane, which is oxidized by guard-cell lipoxygenases and further metabolized to OPDA. OPDA-deficient mutants have wider stomatal pores, whereas mutants containing elevated levels of OPDA showed the opposite effect on the stomatal aperture. Transmembrane solute fluxes that drive stomatal aperture were enhanced in lox6-1 guard cells, indicating that OPDA signaling ultimately impacts on activities of proton pumps and K+(in) channels. The accelerated stomatal kinetics in lox6-1 leads to increased plant growth without cost in water or macronutrient use. Thus, a new role is revealed for chloroplast membrane oxylipin metabolism in stomatal regulation. The accelerated stomatal opening kinetics in OPDA-deficient mutants benefits plant growth and water use efficiency (Chang et al. 2023).

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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