Comprehensive identification of sugar transporters in the Malus spp. genomes reveals their potential functions in sugar accumulation in apple fruits

Abstract

• 130 sugar transporter genes were identified in the updated apple genome GDDH13 v1.1. • 57 ST genes were expressed in the cultivar Greensleeves, and 59 in the cultivar Fuji. • MdHT14.1 could transport glucose and fructose, while MdSUT2.1/2.2 and MdSWEET15.2 could transport sucrose. • Overexpression MdVGT1 or MdpGlcT2.1 in apple fruits significantly increased glucose, while overexpression of MdSUT2.1 increased sucrose or of MdSOT1 increased sorbitol. The transport of sugar across membranes is essential for maintaining cellular sugar homeostasis and metabolic balance in plant cells, but there is limited information about the sugar transporter family in economically important fleshy fruits. Here, 130 sugar transporter genes were identified in the updated apple genome (GDDH13 v1.1). The sugar transporter (ST) genes clustered into ten subfamilies. The apple ST genes mapped to all 17 apple chromosomes and had experienced whole-genome duplication (WGD)/segmental duplication and tandem duplication during the process of apple domestication. Expression profiles of the STs were analyzed in different tissues and during the stages of fruit development. In Malus × domestica , 57 ST genes were expressed in the cultivar ‘Greensleeves’, and 59 in ‘Fuji’. Different ST genes were highly expressed in mature leaves, shoot tips, young fruits, and mature fruits, indicating their divergent functions in different tissues. Heterologous expression experiments in yeast strains lacking STs indicated that MdHT14.1 is the sugar transporter with the highest affinity for glucose and fructose, while MdSUT2.1/2.2 and MdSWEET15.2 had the highest affinity for sucrose. Transient overexpression in apple fruits of MdVGT1 and MdpGlcT2.1 significantly increased glucose concentration, while overexpression of MdSUT2.1 increased sucrose level or of MdSOT1 increased sorbitol concentration. This study demonstrated the expansion and functional divergence of the sugar transporter gene family in domesticated apple and will enable further investigation of the molecular mechanisms of sugar transport and metabolism in apple and other important fleshy fruit crops.