Evolutionary trajectory and functional diversity of SWEET sugar transporters in plants

SWEET (sugars will eventually be exported transporter) proteins are vital for sugar transport in plants, mediating the movement of glucose, fructose, and sucrose, and playing key roles in growth, development, and stress responses. This study identified 1246 SWEET proteins across 59 plant species, spanning from chlorophytes to eudicots. Phylogenetic analysis revealed that SWEET proteins originated in chlorophytes and diverged into four clades (I-IV). Chlorophyte SWEETs, classified in clade II, lacked transport activity and were localized on the vacuolar membrane. In charophytes, clade I SWEETs acquired the ability to transport glucose and fructose, marking a significant adaptation during the transition to terrestrial plants. In bryophytes, clade II SWEETs transport glucose and fructose, localized on the vacuolar membrane. In vascular plants, clade IV SWEETs, which emerged in lycophytes, exhibited fructose transport activity and localized to the plasma or vacuolar membranes. Clade III SWEETs, exclusive to seed plants, are specialized in sucrose transport, which is crucial for long-distance sugar distribution. Sequence and structural analysis revealed that the highly conserved transmembrane regions form the triple-helix bundle essential for sugar transport. In contrast, the N-terminal and C-terminal regions contribute to substrate specificity and structural folding. Functional assays confirmed that removal of these non-conserved regions abolishes transport activity. In conclusion, this study provides a comprehensive analysis of the evolutionary origins, functional diversification, and structural significance of SWEET proteins, underscoring their pivotal roles in carbohydrate metabolism and plant diversification. These findings offer valuable insights into the molecular mechanisms underlying sugar transport and its evolutionary adaptations in plants.