Hexose/hexitol transporter gene family

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Contents

Monosaccharide/sugar alcohol transporter family

Sylvie Lalonde & Wolf B. Frommer, Department of Plant Biology, Carnegie Institution for Science, slalonde@stanford.edu

Analysis of the family that comprised the ubiquitous hexose transporters as well as sugar alcohol transporters gene superfamily in Selaginella moellendorfii revealed:

1. The presence of 49 genes

2. The genes fall into 6 clades (STP like transporters - these typically function as high affinity monosaccharide proton cotransporters, here called MST (monosaccharide transporters since they transport pentoses and various hexoses); ERD6-like transporters, the function has not been demonstrated yet; GLTs are plastidic glucose transporters Weber et al., 2000); VGT-like; a homolog in Arabidopsis was found in vacuolar membranes and functions as a hexose transporter (Buettner 2007); TMTs have extended loops and function as vacuolar monsaccharide transporters (Wormit et al., 2006); INT-like transporters for inositol transport (Schneider et al., 2008) and PLTs for polyol transport (Reinders et al., 2005).

3. Many similarities exist with homologs from Physcomitrella patens (Johnson & Thomas 2007). However the annotation in Physcomitrella needs to be improved.

4. Close homologs are found in Chlorella, Chlamydomonas, cyanobacteria, fungi and in the animal kingdom including the important GLUT glucose facilitators.

Hexose uptake in mosses

Bryophytes and Pteridophytes contain glucose, fructose and sucrose (Allsopp, 1951). However, Selaginella kraussiana and Selaginella caulescens did not appear to contain significant amounts of sucrose but rather trehalose. Trehalose appears to be a dominant sugar in many Selaginella species (cf. ref. in Allsopp, 1951). Due to the high levels, trehalose can be isolated from Selaginella lepidophylla, the resurrection plant. This desiccation-tolerant Selaginella lepidophylla contains very high trehalose levels (2% of sugar) and a very high activity trehalose-6-phosphate synthase as compared to other plants, potentially suggesting that trehalose accumulation is related to the resurrection phenotype (Van Dijck et al., 2002). Physcomitrella growth seems unaffected by the presence of 0.5% glucose (Thornton et al., 2005[1]). While in the case of Physcomitrella the sugar could not be used as an alternative carbon source when photosynthesis was blocked by DCMU, nor did it grow in darkness, while Ceratodon showed some growth on glucose and sucrose (Thornton et al., 2005[2]). The ligule of Selaginella kraussiana has been shown to take up 3H-glucose (Sigee, 1976).

Consistent with the sugar alcohols being involved in resurrection, there are both inositol and polyol transporter homologs. Both types of vacuolar monosaccharide transporters are found in Selaginella as well as plastidic glucose and Mex1-like maltose transporters (see MEX). The overall composition is similar in Selaginella as in monocots such as rice, although there are less MSTs (STP-like transporters). Arabidopsis has a lot more ERD6-like transporters than monocots and Selaginella.

Below is a phylogeny tree based on the predicted sequences of the gene models (red). Purple label of genes indicates an incomplete annotation of the genes (the protein ID of the sequence used in the tree is indicated). The tree was obtained by nearest neighbor method.


Image:hexose_tree_v2.jpg

References

  • Allsopp, A. (1951) The sugars and non-volatile acids of some Archegoniates: A survey using paper chromatography. J. Exp. Bot. 2:121-124.
  • Sigee D.C. (1976) Structure and function in the ligule of Selaginella kraussiana. 3. The uptake of tritiated glucose. Protoplasma 90:333-341.
  • Lalonde S, Wipf D, Frommer WB. (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol. 55:341-72.[3]
  • Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG. (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141:196-207.[4]
  • Caspari T, Will A, Opekarová M, Sauer N, Tanner W. (1994) Hexose/H+ symporters in lower and higher plants. J Exp Biol. 196:483-91.[5]
  • Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12:787-802.
  • Reinders A, Panshyshyn JA, Ward JM. (2005) Analysis of transport activity of Arabidopsis sugar alcohol permease homolog AtPLT5. J Biol Chem. 280:1594-602.
  • Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata K, Tanaka D, Watanabe M, Okuda T. (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci USA 104:11585-90[6]
  • Van Dijck P, Mascorro-Gallardo JO, De Bus M, Royackers K, Iturriaga G, Thevelein JM. (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J. 366:63-71.[7]
  • Johnson DA, Thomas MA. (2007) The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence. Mol Biol Evol. 24:2412-23.[8]
  • Thornton LE, Keren N, Ohad I, Pakrasi HB. (2005) Physcomitrella patens and Ceratodon purpureus, mosses as model organisms in photosynthesis studies. Photosynth Res. 2005;83(1):87-96.[9]
  • Büttner M. (2007) The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett. 2007 May 25;581(12):2318-24.
  • Aluri S, Büttner M. (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc Natl Acad Sci USA 104:2537-42.
  • Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE. (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell. 18:3476-90.
  • Schneider S, Beyhl D, Hedrich R, Sauer N. (2008) Functional and Physiological Characterization of Arabidopsis INOSITOL TRANSPORTER1, a Novel Tonoplast-Localized Transporter for myo-Inositol. Plant Cell 20:1073-87.

Table of gene numbers

Gene functions Gene Gene used as a query The number of putative orthologs
Arabidopsis thaliana Oryza sativa Selaginalla moellendorffii Physcomitrella patens
Monosaccharide Transport MST AtSTP1 (AT1G11260) 12 25 11 (22) 2 (4)
Monosaccharide Transport ERD6 AtSTP1 (AT1G11260) 19 2 1 (2) 0
Monosaccharide Transport pGLT AtGLT1 (AT5G16150) 4 3 4 (8) 3 (6)
Monosaccharide Transport VGT AtSTP1 (AT1G11260) 3 0 1 (2) 0
Monosaccharide Transport TMT AtTMT1 (AT1G20840) 3 3 4 (8) 2 (4)
INOSITOL Transport INT AtSTP1 (AT1G11260) 4 1 2 (4) 0
Polyol Transport PLT AtSTP1 (AT1G11260) 6 6 3 (6) 1
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