Sucrose transporter gene family

From Purdue Genomics Database Facility

Contents 1 Sucrose/maltose transporter 2 Sucrose/maltose transport in mosses 3 Sucrose/maltose transporters in Selaginella 4 References 5 Table of gene numbers

Sucrose/maltose transporter

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

Sucrose is the major transport form in many higher plants. Sucrose is a disaccharide composed of glucose and fructose (α-D-glucopyranosyl- (1↔2)-β-D-fructofuranoside). Sucrose has a low viscosity even at high concentrations (soluble to several molar) and has no reducing end and is thus considered more inert than glucose, which is the major transport form in animals. Sucrose is produced in the mesophyll cells of plant leaves (as well as other organs) by the action of sucrose phosphate synthase and sucrose phosphate phosphatase or by sucrose synthase. Sucrose is exported into the cell wall space by unknown mechanisms. The extracellular sucrose is then loaded into the long distance transport system of higher plants, the phloem, with the help of secondary active transporters in the membrane of the sieve element companion cell complex. The first sucrose transporter gene SUT1 was identified by suppression cloning in yeast from spinach and potato leaf cDNA libraries (Riesmeier et al., 1992[1]; 1993[2]). Interestingly, the transporter also mediates maltose transport. SUT1 has an affinity for sucrose in the low mM range (around 1 mM). SUT1 is essential for sucrose export from the leaves of potato and tobacco as shown by antisense repression (Riesmeier et al., 1994; Buerkle et al., 1998[3]). The Arabidopsis homolog was called SUC2 and a mutation in SUC2 is lethal (Gottwald et al., 2000[4]). Two more distantly related sucrose transporter homologs SUT2 and SUT4 were functionally characterized in the yeast expression system and shown to also transport sucrose and maltose (Weise et al., 2000; Barker et al., 2000). All three transporters have been localized to enucleate sieve elements (Kuehn et al., 1997, Weise et al., 2000; Barker et al., 2000). A recent proteomic analysis identified thebarely SUT4 homolog in the tonoplast membrane (Endler et al., 2006[5]). SUT2 and SUT4 are low affinity sucrose transporters in Solanaceae and Arabidopsis. SUT2 is characterized by an extended central loop that contains conserved domains CCB1 and CCB2 (Lalonde et al., 2004). In tomato, LeSUT1 and LeSUT2 inhibition affects tomato fruit development, while the potato SUT4 appears to be important for a variety of functions flowering, tuberization, and shade avoidance response (Hackel et al., 2006; Chincinska et al., 2008).

Note that the nomenclature of sucrose transporters in Arabidopsis may differ. SUT1 and SUT3 are paralogs in tobacco (Lemoine et al.) the corresponding genes in Arabidopsis are called SUC2 as well as SUC1, 5, 6, 7, 8 and 9. SUT2 has been called SUC3 and SUT4 has been called SUC4.

Trehalose transporters have been identified in insects, function as facilitators and belong to the hexose transporter family (MFS; Kikawada et al. 2007).

Sucrose/maltose transport 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). The desiccation-tolerant Selaginella lepidophylla contains very high trehalose levels 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).

To our knowledge, sucrose transport has not been studied in detail in mosses. However, sucrose can be used in media for axenic culture of mosses.

 

Sucrose/maltose transporters in Selaginella

The genomes of Selaginella were screened for the occurance of plant sucrose transporters. The analysis identified close homologs of the Physcomitrella and higher plant sucrose transporter family. The haploid Selaginella genome encodes 5 sucrose transporter genes. The Selaginella genes fall into 2 clades, the SUT2 and SUT4 clades (Lalonde et al., 2004[6]). One member falls into the SUT2 clade and was named SUT2-1 (the allele from the second haploid line was called SUT2-2 as well as four genes (SUT4L1, SUT4L2, SUT4L3, SUT4L4), which fall into the SUT4 clade. No ortholog of the SUT1 clade was found. This classification supported by similarities in the intron structure and presence of an extended central loop containing a conserved domain CCB2 in the Selaginella and higher plant SUT2s. Monocots also do not have a SUT1 homolog, which is interesting since this transporter is essential for several dicots. Monocots have two types of SUT2, one with and one without a central loop.

Distant homologs have been identified in fungi (Reinders & Ward, 2001[7]). The Shizosacchacharomyces pombe homolog was shown to function primarily as a maltose transporter, but also transports sucrose (Reinders & Ward, 2001). Homologs also exist in the animal kingdom, e.g. medaka and mouse, which are directly or indirectly involved in melanin accumulation (Fukamachi et al., 2001[8]). Interestingly, no sucrose transporter homologs have been found in green algae, while glucose transporters are well conserved in algae (Caspari et al., 1994[9]).

References

• Allsopp, A. (1951) The sugars and non-volatile acids of some Archegoniates: A survey using paper chromatography. J. Exp. Bot. 2:121-124.

• 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.[10]

• Reinders A, Ward JM. (2001) Functional characterization of the alpha-glucoside transporter Sut1p from Schizosaccharomyces pombe, the first fungal homologue of plant sucrose transporters. Mol Microbiol. 39:445-54.[11]

• Schulze W, Weise A, Frommer WB, Ward JM. (2000) Function of the cytosolic N-terminus of sucrose transporter AtSUT2 in substrate affinity. FEBS Lett. 485:189-94.[12]

• Fukamachi S, Shimada A, Shima A. (2001) Mutations in the gene encoding B, a novel transporter protein, reduce melanin content in medaka. Nat Genet. 28:381-5.[13]

• Riesmeier JW, Willmitzer L, Frommer WB. (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705-13.[14]

• Riesmeier JW, Hirner B, Frommer WB. (1993) Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell. 5:1591-8.[15]

• Riesmeier JW, Willmitzer L, Frommer WB. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J. 13:1-7.[16]

• Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB, Ward JM. (2000) A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell. 12:1345-55[17].

• Buerkle L, Hibberd JM, Quick WP, Kuhn C, Hirner B, Frommer WB. (1998) The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol. 118:59-68.[18]

• Barker L, Kühn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB. (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153-64[19].

• 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.[20]

• Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kühn C. (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways.

Plant J. 45:180-92.

• Chincinska IA, Liesche J, Krügel U, Michalska J, Geigenberger P, Grimm B, Kühn C. (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol. 146:515-28

• 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.[21]

• Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR. (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 97:13979-84.[22]

• 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[23]

• 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.[24]

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
Sucrose Transport	SUT1	StSUT1 (CAA48915)	7	0	0	0
Sucrose Transport	SUT2	StSUT1 (CAA48915)	1	5	1 (2)	1 (2)
Sucrose Transport	SUT4	StSUT1 (CAA48915)	1	1	4 (8)	2 (4)