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

Authors: SHAMMAI, ARIK - Agricultural Research Organization Of Israel; PETREIKOV, MARINA - Agricultural Research Organization Of Israel; YESELSON, YELENA - Agricultural Research Organization Of Israel; FAIGENBOIM, ADI - Agricultural Research Organization Of Israel; COHEN, SHAHAR - Agricultural Research Organization Of Israel; COHEN, DVIR - Agricultural Research Organization Of Israel; WHITE, RUTH - Former ARS Employee; Giovannoni, James; LEVIN, ILAN - Agricultural Research Organization Of Israel; KATZIR, NURIT - Agricultural Research Organization Of Israel

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/26/2018
Publication Date: 7/25/2018
Citation: Shammai, A., Petreikov, M., Yeselson, Y., Faigenboim, A., Cohen, S., Cohen, D., White, R., Giovannoni, J.J., Levin, I., Katzir, N. 2018. Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit. Plant Journal. https://doi.org/10.1111/tpj.14035.
DOI: https://doi.org/10.1111/tpj.14035

Interpretive Summary: The quality of tomato fruit is largely determined by its soluble sugar content, which in the cultivated tomato is composed primarily of the hexoses fructose and glucose, in near-equal quantities. As fructose is approximately twice as sweet as glucose, altering hexose partitioning in the fruit towards increased fructose levels can contribute to the improvement of fruit taste. We explored genetic diversity in a wild, inedible relative of tomato and identified a gene encoding a SWEET class sugar transporter which elevated the ratio of fructose to glucose when crossed with cultivated tomato. As such, the identity of the underlying gene was identified and we importantly demonstrated that crossable wild relatives who produce inedible tissues may still harbor useful genetic diversity for crop improvement.

Technical 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 FgrH 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. 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.