Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit

Abstract

The sugar content of Solanum lycopersicum (tomato) fruit is a primary determinant of taste and quality. Cultivated tomato fruit are characterized by near-equimolar levels of the hexoses glucose and fructose, derived from the hydrolysis of translocated sucrose. As fructose is perceived as approximately twice as sweet as glucose, increasing its concentration at the expense of glucose can improve tomato fruit taste. Introgressions of the Fgr allele from the wild species Solanum habrochaites (LA1777) into cultivated tomato increased the fructose-to-glucose ratio of the ripe fruit by reducing glucose levels and concomitantly increasing fructose levels. In order to identify the function of the Fgr gene, we combined a fine-mapping strategy with RNAseq differential expression analysis of near-isogenic tomato lines. The results indicated that a SWEET protein was strongly upregulated in the lines with a high fructose-to-glucose ratio. Overexpressing the SWEET protein in transgenic tomato plants dramatically reduced the glucose levels and increased the fructose : glucose ratio in the developing fruit, thereby proving the function of the protein. The SWEET protein was localized to the plasma membrane and expression of the SlFgr gene in a yeast line lacking native hexose transporters complemented growth with glucose, but not with fructose. These results indicate that the SlFgr gene encodes a plasma membrane-localized glucose efflux transporter of the SWEET family, the overexpression of which reduces glucose levels and may allow for increased fructose levels. This article identifies the function of the tomato Fgr gene as a SWEET transporter, the upregulation of which leads to a modified sugar accumulation pattern in the fleshy fruit. The results point to the potential of the inedible wild species to improve fruit sugar accumulation via sugar transport mechanisms.

VvSWEET7 Is a Mono- and Disaccharide Transporter Up-Regulated in Response to Botrytis cinerea Infection in Grape Berries

“…The Arabidopsis VvSWEET7 homologue functions as a glucose transport and is expressed mainly in the flower and seed (Chen et al, 2010); the cucumber CsSWEET7b transports glucose and, to a minor degree, mannose and galactose (Li et al, 2017). Interestingly, the tomato VvSWEET7 homologue (SlSWEET6) is also strongly regulated during the early phases of tomato fruit development (Shammai et al, 2018).…”

“…Also, it regulates cell viability under high salinity (Seo et al, 2011) and is also involved, along with AtSWEET11 and AtSWEET12, in the sugar efflux required for seed filling (Chen et al, 2015a). In tomato, the not so well characterized SlSWEET15 showed a similar expression pattern to its grapevine homologue along with fruit development (Shammai et al, 2018), being more expressed in the mature stage.…”

Applying the Solanaceae Strategies to Strawberry Crop Improvement

“…Interestingly, strawberry and tomato wild relatives are significantly different from cultivated varieties, not only for fruit size but also for flavor attributes [5,6,[42][43][44]. In tomato, this diversity has been instrumental for the discovery by quantitative trait locus (QTL) mapping of allelic variants responsible for desirable flavor-related traits (e.g., starch and sugar content [45], fructose-to-glucose ratio [46], flavor volatiles [47]). In parallel, genome-wide association studies (GWASs) of hundreds of tomato modern varieties, landraces, and wild relatives led to the identification of causal SNPs associated with variations in fruit size [6], steroidal alkaloids [6], malate [48], fruit color [6,18], and flavor components [4,5].…”

Trait discovery and editing in tomato

“…The mutation allowing an extended gene expression led to higher starch accumulation during fruit development and subsequent increase in soluble solid content in ripe fruit. More recently a mutation in a SWEET transporter in wild species was shown to be responsible for a higher fructose to glucose ratio compared with that in S. lycopersicum (Shammai et al ., ).…”