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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 J. 2018 10; 96(2):343-357.PJ

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. 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.

Authors+Show Affiliations

Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Zeraim-Syngenta Seed Co., Gedera, Israel.Zeraim-Syngenta Seed Co., Gedera, Israel.Zeraim-Syngenta Seed Co., Gedera, Israel.Department of Molecular Genetics, Weizmann Institute, Rehovot, Israel.Department of Molecular Genetics, Weizmann Institute, Rehovot, Israel.Department of Plant Physiology, University of Kaiserslautern, Kaiserslautern, Germany.Department of Plant Physiology, University of Kaiserslautern, Kaiserslautern, Germany.Syngenta Seed Co., Jeallott's Hill Research Centre, Bracknell, UK.Syngenta Seed Co., Jeallott's Hill Research Centre, Bracknell, UK.Syngenta Seed Co., Toulouse Innovation Center, Saint Sauveur, France.USDA-ARS and Boyce-Thompson Institute, Ithaca, NY, USA.USDA-ARS and Boyce-Thompson Institute, Ithaca, NY, USA.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.Institute of Plant Sciences Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

30044900

Citation

Shammai, Arik, et al. "Natural Genetic Variation for Expression of a SWEET Transporter Among Wild Species of Solanum Lycopersicum (tomato) Determines the Hexose Composition of Ripening Tomato Fruit." The Plant Journal : for Cell and Molecular Biology, vol. 96, no. 2, 2018, pp. 343-357.
Shammai A, Petreikov M, Yeselson Y, et al. 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 J. 2018;96(2):343-357.
Shammai, A., Petreikov, M., Yeselson, Y., Faigenboim, A., Moy-Komemi, M., Cohen, S., Cohen, D., Besaulov, E., Efrati, A., Houminer, N., Bar, M., Ast, T., Schuldiner, M., Klemens, P. A. W., Neuhaus, E., Baxter, C. J., Rickett, D., Bonnet, J., White, R., ... Schaffer, A. (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. The Plant Journal : for Cell and Molecular Biology, 96(2), 343-357. https://doi.org/10.1111/tpj.14035
Shammai A, et al. 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 J. 2018;96(2):343-357. PubMed PMID: 30044900.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit. AU - Shammai,Arik, AU - Petreikov,Marina, AU - Yeselson,Yelena, AU - Faigenboim,Adi, AU - Moy-Komemi,Michal, AU - Cohen,Shahar, AU - Cohen,Dvir, AU - Besaulov,Eduard, AU - Efrati,Ari, AU - Houminer,Naomi, AU - Bar,Moshe, AU - Ast,Tslil, AU - Schuldiner,Maya, AU - Klemens,P A W, AU - Neuhaus,Ekkehard, AU - Baxter,Charles J, AU - Rickett,Dan, AU - Bonnet,Julien, AU - White,Ruth, AU - Giovannoni,James J, AU - Levin,Ilan, AU - Schaffer,Arthur, Y1 - 2018/09/01/ PY - 2018/03/19/received PY - 2018/06/19/revised PY - 2018/06/26/accepted PY - 2018/7/26/pubmed PY - 2019/7/31/medline PY - 2018/7/26/entrez KW - SWEET transporter KW - Solanum species KW - fructose KW - fruit sugars KW - introgression SP - 343 EP - 357 JF - The Plant journal : for cell and molecular biology JO - Plant J VL - 96 IS - 2 N2 - 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. 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. SN - 1365-313X UR - https://www.unboundmedicine.com/medline/citation/30044900/Natural_genetic_variation_for_expression_of_a_SWEET_transporter_among_wild_species_of_Solanum_lycopersicum__tomato__determines_the_hexose_composition_of_ripening_tomato_fruit_ L2 - https://doi.org/10.1111/tpj.14035 DB - PRIME DP - Unbound Medicine ER -