Evolutionary gain of oligosaccharide hydrolysis and sugar transport enhanced carbohydrate partitioning in sweet watermelon fruits

Abstract

How raffinose (Raf) family oligosaccharides (RFOs), the major translocated sugars in the vascular bundle in cucurbits, are hydrolyzed and subsequently partitioned has not been fully elucidated. By performing reciprocal grafting of watermelon (Citrullus lanatus) fruits to branch stems, we observed that Raf was hydrolyzed in the fruit of cultivar watermelons but was backlogged in the fruit of wild ancestor species. Through a genome-wide association study (GWAS), the alkaline alpha-galactosidase ClAGA2 was identified as the key factor controlling stachyose (Sta) and Raf hydrolysis, and it was determined to be specifically expressed in the vascular bundle. Analysis of transgenic plants confirmed that ClAGA2 controls fruit Raf hydrolysis and reduces sugar content in fruits. Two SNPs within the ClAGA2 promoter affect the recruitment of the transcription factor ClNF-YC2 (nuclear transcription factor Y subunit C) to regulate ClAGA2 expression. Moreover, this study demonstrates that C. lanatus Sugars Will Eventually Be Exported Transporter 3 (ClSWEET3) and Tonoplast Sugar Transporter (ClTST2) participate in plasma membrane sugar transport and sugar storage in fruit cell vacuoles, respectively. Knocking out ClAGA2, ClSWEET3 and ClTST2 affected fruit sugar accumulation. Genomic signatures indicate that the selection of ClAGA2, ClSWEET3 and ClTST2 for carbohydrate partitioning led to the derivation of modern sweet watermelon from non-sweet ancestors during domestication.

Cellular export of sugars and amino acids: role in feeding other cells and organisms

“…Several SWEETs and UmamiTs from various species are known to be expressed in different sink tissues ( Figure 4 ; e.g. Kryvoruchko et al, 2016 ; Zhen et al, 2018 ; Jeena et al, 2019 ; Wang et al, 2019 ; Ren et al, 2021 ). Impaired activity of SWEETs or UmamiTs causes defects in basic physiological processes reflecting their broad role.…”

Molecular basis for optimizing sugar metabolism and transport during fruit development

“…In addition, raffinose family oligosaccharides are also major sugars translocated in the vascular bundle in cucurbits. ClAGA2, ClSWEET3 (a plasma membrane-localized clade I hexose transporter) and ClTST2 function in raffinose hydrolysis, transmembrane sugar transport and sugar storage in vacuoles, respectively, thereby contributing to the derivation of sweet watermelon from non-sweet ancestors during domestication (Ren et al 2021). Moreover, it was reported recently that MdERDL6-1, a tonoplast glucose/H ?…”

Advances in CRISPR/Cas9-mediated genome editing on vegetable crops

“…Genome editing of five genes in the carotenoid metabolic pathway was conducted to promote lycopene biosynthesis, and at the same time inhibit its conversion to βand αcarotene (Li et al 2018f). Using CRISPR/cas9 technology, Ren et al (2020Ren et al ( , 2021 revealed several important node genes of sugar accumulation in the process of watermelon domestication, which laid a foundation for watermelon improvement in the future.…”