RtSWEET6 drives the carbohydrate source-sink allocation and prevents berry ripening in Rhodomyrtus tomentosa

Rhodomyrtus tomentosa (Ait.) Hassk is an emerging berry fruit crop widely distributing across tropic and subtropic regions. The fruits of R. tomentosa, which contain abundant anthocyanins and sugar, are consumed freshly or processed as beverages, jams, and jellies. Improving the sugar content of fruits is one of the major efforts in R. tomentosa breeding, yet little is known. The SWEET (Sugars Will Eventually be Exported Transporters) family members play essential roles in sugar allocation and accumulation in plants. Here, we identified and characterized 21 RtSWEETs in the genome of R. tomentosa, which can be divided into four clades. Transcriptomic analysis showed that RtSWEETs expressed in different tissues and developmental stages; for example, RtSWEET6, RtSWEET10, and RtSWEET15 were specifically highly expressed in green fruits. The cell-membrane-localized RtSWEET6 functioned as a transporter of sugars, including glucose, fructose, and mannose. The soluble sugar and starch levels in RtSWEET6-overexpressing Arabidopsis and tomato were enhanced compared with wild-type plants. Moreover, overexpressing RtSWEET6 in tomato promoted the accumulation of glucose and sucrose in fruits, whereas the glucose content in mature leaves was reduced, indicating that RtSWEET6 facilitated the source-sink allocation of the carbohydrate. The transgenic tomato flowered earlier and ripened later without compromising fruit size. Overexpressing RtSWEET6 inhibited fruit ripening in R. tomentosa, whereas silencing RtSWEET6 accelerated fruit ripening. The alteration of ripening-related genes’ expression and sugar accumulation were parallel with these phenotypes. This study characterized SWEET transporters in R. tomentosa and demonstrated that RtSWEET6 simultaneously enhanced source-to-sink sugar allocation and delayed ripening by repressing ripening-related genes, uncovering a novel connection between carbohydrate metabolism and berry development. The bifunctional RtSWEET6 exhibits potential for extending the shelf life of fresh fruits.