Abstract
Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB), and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincided with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type I and Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms.
Highlights
Sucrose is among the most abundant photoassimilates and the principal transport form of carbohydrates in many plants
sucrose transporters (SUTs) genes involved in phloem loading have been localized to the companion cells and sieve elements (Riesmeier et al, 1993; Stadler et al, 1995; Truernit and Sauer, 1995), while those involved in sucrose uptake and other sink functions were preferentially expressed in tissues like pollen (Lemoine et al, 1999; Stadler et al, 1999), root (Flemetakis et al, 2003) or xylem (Decourteix et al, 2006)
The strong support for the two land plant clades descending from the algal clade suggests that modern plant SUT genes evolved from two different ancestors, hereafter referred to as ancient groups Ancient Group 1 (AG1) and Ancient Group 2 (AG2)
Summary
Sucrose is among the most abundant photoassimilates and the principal transport form of carbohydrates in many plants. SUTs are proton-coupled symporters that transport sucrose either intercellularly across plasma membranes or intracellularly from the vacuole to the cytoplasm (reviewed in Kühn and Grof, 2010; Ayre, 2011). SUT genes are expressed throughout the plant body, with varying tissue- or cell-specificity depending on the isoform function. SUT genes involved in phloem loading have been localized to the companion cells and sieve elements (Riesmeier et al, 1993; Stadler et al, 1995; Truernit and Sauer, 1995), while those involved in sucrose uptake and other sink functions were preferentially expressed in tissues like pollen (Lemoine et al, 1999; Stadler et al, 1999), root (Flemetakis et al, 2003) or xylem (Decourteix et al, 2006). With the growing number of SUT genes identified, especially from the grasses, four distinct phylogenetic groups (Group 1 to Group 4)
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