Plasma membrane-localized SlSWEET7a and SlSWEET14 regulate sugar transport and storage in tomato fruits

Xinsheng Zhang , Chaoyang Feng , Manning Wang , Tianlai Li , Xin Liu , Jing Jiang

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 186

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :186 DOI: 10.1038/s41438-021-00624-w
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Plasma membrane-localized SlSWEET7a and SlSWEET14 regulate sugar transport and storage in tomato fruits
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Abstract

Sugars, especially glucose and fructose, contribute to the taste and quality of tomato fruits. These compounds are translocated from the leaves to the fruits and then unloaded into the fruits by various sugar transporters at the plasma membrane. SWEETs, are sugar transporters that regulate sugar efflux independently of energy or pH. To date, the role of SWEETs in tomato has received very little attention. In this study, we performed functional analysis of SlSWEET7a and SlSWEET14 to gain insight into the regulation of sugar transport and storage in tomato fruits. SlSWEET7a and SlSWEET14 were mainly expressed in peduncles, vascular bundles, and seeds. Both SlSWEET7a and SlSWEET14 are plasma membrane-localized proteins that transport fructose, glucose, and sucrose. Apart from the resulting increase in mature fruit sugar content, silencing SlSWEET7a or SlSWEET14 resulted in taller plants and larger fruits (in SlSWEET7a-silenced lines). We also found that invertase activity and gene expression of some SlSWEET members increased, which was consistent with the increased availability of sucrose and hexose in the fruits. Overall, our results demonstrate that suppressing SlSWEET7a and SlSWEET14 could be a potential strategy for enhancing the sugar content of tomato fruits.

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Xinsheng Zhang, Chaoyang Feng, Manning Wang, Tianlai Li, Xin Liu, Jing Jiang. Plasma membrane-localized SlSWEET7a and SlSWEET14 regulate sugar transport and storage in tomato fruits. Horticulture Research, 2021, 8 (1) : 186 DOI:10.1038/s41438-021-00624-w

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References

[1]

Braun, D. M., Wang, L. & Ruan, Y. L. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J. Exp. Bot. 65, 1713-1735 (2014).

[2]

Ruan, Y. L. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 65, 33-67 (2014).

[3]

Li, Y., Feng, S., Ma, S., Sui, X. & Zhang, Z. Spatiotemporal expression and substrate specificity analysis of the cucumber SWEET gene family. Front. Plant Sci. 8, 1855 (2017).

[4]

Zhang, C., Bian, Y., Hou, S. & Li, X. Sugar transport played a more important role than sugar biosynthesis in fruit sugar accumulation during Chinese jujube domestication. Planta 248, 1187-1199 (2018).

[5]

Zhang, S. et al. Spatiotemporal transcriptome provides insights into early fruit development of tomato (Solanum lycopersicum) . Sci. Rep. 6, 23173 (2016).

[6]

Sagor, G. H. et al. A novel strategy to produce sweeter tomato fruits with high sugar contents by fruit-specific expression of a single bZIP transcription factor gene. Plant Biotechnol. J. 14, 1116-1126 (2016).

[7]

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. 96, 343-357 (2018).

[8]

Damon, S., Hewitt, J., Nieder, M. & Bennett, B. B. Sink metabolism in tomato fruit: II. phloem unloading and sugar uptake. Plant Physiol. 87, 731-736 (1988).

[9]

Osorio, S., Ruan, Y. L. & Fernie, A. R. An update on source-to-sink carbon partitioning in tomato. Front. Plant Sci. 5, 516 (2014).

[10]

Wan, H., Wu, L., Yang, Y., Zhou, G. & Ruan, Y. L. Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trends Plant Sci. 23, 163-177 (2018).

[11]

Julius, B. T., Leach, K. A., Tran, T. M., Mertz, R. A. & Braun, D. M. Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol. 58, 1442-1460 (2017).

[12]

Hackel, A. et al. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J. 45, 180-192 (2006).

[13]

Dibley, S. J. et al. Temporal and spatial expression of hexose transporters in developing tomato (Lycopersicon esculentum) fruit . Funct. Plant Biol. 32, 777 (2005).

[14]

Reuscher, S. et al. The sugar transporter inventory of tomato: genome-wide identification and expression analysis. Plant Cell Physiol. 55, 1123-1141 (2014).

[15]

Reinders, A. et al. Protein-protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell 14, 1567-1577 (2002).

[16]

McCurdy, D. W., Dibley, S., Cahyanegara, R., Martin, A. & Patrick, J. W. Functional characterization and RNAi-mediated suppression reveals roles for hexose transporters in sugar accumulation by tomato fruit. Mol. Plant 3, 1049-1063 (2010).

[17]

Bologa, K. L., Fernie, A. R., Leisse, A., Loureiro, M. E. & Geigenberger, P. A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol. 132, 2058-2072 (2003).

[18]

Ayre, B. G. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol. Plant 4, 377-394 (2011).

[19]

Slewinski, T. L. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol. Plant 4, 641-662 (2011).

[20]

Chen, L. Q. et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207-211 (2012).

[21]

Eom, J. S. et al. SWEETs, transporters for intracellular and intercellular sugar translocation. Curr. Opin. Plant Biol. 25, 53-62 (2015).

[22]

Chen, L. Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527-532 (2010).

[23]

Sun, W. et al. Cotton fiber elongation requires the transcription factor GhMYB212 to regulate sucrose transportation into expanding fibers. New Phytol. 222, 864-881 (2018).

[24]

Abelenda, J. A. et al. Source-sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr. Biol. 29, 1178-1186 (2019).

[25]

Lin, I. W. et al. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508, 546-549 (2014).

[26]

Sosso, D. et al. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat. Genet. 47, 1489-1493 (2015).

[27]

Yang, J., Luo, D., Yang, B., Frommer, W. B. & Eom, J. S. SWEET11 and 15 as key players in seed filling in rice. New Phytol. 218, 604-615 (2018).

[28]

Chen, L. Q. et al. A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27, 607-619 (2015).

[29]

Ma, L. et al. Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol. 58, 863-873 (2017).

[30]

Ho, L. H. et al. SlSWEET1a is involved in glucose import to young leaves in tomato plants . J. Exp. Bot. 70, 3241-3254 (2019).

[31]

Ko, H.-Y., Ho, L.-H., Neuhaus, H. E. & Guo, W.-J. Transporter SlSWEET15 unloads sucrose from phloem and seed coat for fruit and seed development in tomato. Plant Physiol. https://doi.org/10.1093/plphys/kiab290 (2021).

[32]

Feng, C. Y., Han, J. X., Han, X. X. & Jiang, J. Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene 573, 261-272 (2015).

[33]

Xuan, Y. H. et al. Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc. Natl Acad. Sci. USA 110, E3685-E3694 (2013).

[34]

Jeena, G. S., Kumar, S. & Shukla, R. K. Structure, evolution and diverse physiological roles of SWEET sugar transporters in plants. Plant Mol. Biol. 100, 351-365 (2019).

[35]

Le Hir, R. et al. Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular development and freezing tolerance in Arabidopsis. Mol. Plant 8, 1687-1690 (2015).

[36]

Zhang, Z. et al. VvSWEET10 mediates sugar accumulation in grapes. Genes 10, 255 (2019).

[37]

Kanno, Y. et al. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat. Commun. 7, 13245 (2016).

[38]

Selvam, B., Yu, Y. C., Chen, L. Q. & Shukla, D. Molecular basis of the glucose transport mechanism in plants. ACS Cent. Sci. 5, 1085-1096 (2019).

[39]

Tao, Y. et al. Structure of a eukaryotic SWEET transporter in a homotrimeric complex. Nature 527, 259-263 (2015).

[40]

Guo, C., Li, H., Xia, X., Liu, X. & Yang, L. Functional and evolution characterization of SWEET sugar transporters in Ananas comosus . Biochem. Biophys. Res. Commun. 496, 407-414 (2018).

[41]

Zhen, Q. et al. Developing gene-tagged molecular markers for evaluation of genetic association of apple SWEET genes with fruit sugar accumulation. Hortic. Res. 5, 14 (2018).

[42]

Jin, Y., Ni, D. A. & Ruan, Y. L. Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21, 2072-2089 (2009).

[43]

Rottmann, T., Fritz, C., Sauer, N. & Stadler, R. Glucose uptake via STP transporters inhibits in vitro pollen tube growth in a HEXOKINASE1-dependent manner in Arabidopsis thaliana . Plant Cell 30, 2057-2081 (2018).

[44]

Shen, S. et al. Cell wall invertase and sugar transporters are differentially activated in tomato styles and ovaries during pollination and fertilization. Front. Plant Sci. 10, 506 (2019).

[45]

Griffiths, C. A., Paul, M. J. & Foyer, C. H. Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochim. Biophys. Acta 1857, 1715-1725 (2016).

[46]

Breia, R. et al. VvSWEET7 is a mono- and disaccharide transporter up-regulated in response to Botrytis cinerea infection in grape berries. Front. Plant Sci. 10, 1753 (2020).

[47]

Guo, W. J. et al. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164, 777-789 (2014).

[48]

Claeyssen, E. & Rivoal, J. Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68, 709-731 (2007).

[49]

Eveland, A. L. & Jackson, D. P. Sugars, signalling, and plant development. J. Exp. Bot. 63, 3367-3377 (2012).

[50]

Beauvoit, B. P. et al. Model-assisted analysis of sugar metabolism throughout tomato fruit development reveals enzyme and carrier properties in relation to vacuole expansion. Plant Cell 26, 3224-3242 (2014).

[51]

Qin, G. et al. A tomato vacuolar invertase inhibitor mediates sucrose metabolism and influences fruit ripening. Plant Physiol. 172, 1596-1611 (2016).

[52]

Yu, S. M., Lo, S. F. & Ho, T. D. Source-sink communication: regulated by hormone, nutrient, and stress cross-signaling. Trends Plant Sci. 20, 844-857 (2015).

[53]

Sakr, S. et al. The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. Int. J. Mol. Sci. 19, 2506 (2018).

[54]

Lastdrager, J., Hanson, J. & Smeekens, S . Sugar signals and the control of plant growth and development. J. Exp. Bot. 65, 799-807 (2014).

[55]

Wang, Z. et al. Heterologous expression of the apple hexose transporter MdHT2.2 altered sugar concentration with increasing cell wall invertase activity in tomato fruit. Plant Biotechnol. J. 18, 540-552 (2019).

[56]

Kim, P. et al. Tissue-specific activation of DOF11 promotes rice resistance to sheath blight disease and increases grain weight via activation of SWEET14. Plant Biotechnol. J. 19, 409-411 (2021).

[57]

Guo, M., Zhang, Y. L., Meng, Z. J. & Jiang, J. Optimization of factors affecting agrobacterium-mediated transformation of Micro-Tom tomatoes. Genet. Mol. Res. 11, 661-671 (2012).

[58]

Kim, J. G. et al. Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like Kinase and TFT1 . Plant Cell 21, 1305-1323 (2009).

[59]

Nelson, B. K., Cai, X. & Nebenfuhr, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136 (2007).

[60]

Zhang, N., Shi, J., Zhao, H. & Jiang, J. Activation of small heat shock protein (SlHSP17.7) gene by cell wall invertase inhibitor (SlCIF1) gene involved in sugar metabolism in tomato . Gene 679, 90-99 (2018).

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