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Hu, Y. Physiological Functions of Rice SUT and SWEET transporters. Encyclopedia. Available online: https://encyclopedia.pub/entry/16155 (accessed on 16 November 2024).
Hu Y. Physiological Functions of Rice SUT and SWEET transporters. Encyclopedia. Available at: https://encyclopedia.pub/entry/16155. Accessed November 16, 2024.
Hu, Yibing. "Physiological Functions of Rice SUT and SWEET transporters" Encyclopedia, https://encyclopedia.pub/entry/16155 (accessed November 16, 2024).
Hu, Y. (2021, November 18). Physiological Functions of Rice SUT and SWEET transporters. In Encyclopedia. https://encyclopedia.pub/entry/16155
Hu, Yibing. "Physiological Functions of Rice SUT and SWEET transporters." Encyclopedia. Web. 18 November, 2021.
Physiological Functions of Rice SUT and SWEET transporters
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This entry is adapted from the peer-reviewed paper 10.3390/ijms222011198

Sugar transporters play important or even indispensable roles in sugar translocation among adjacent cells in the plant. They are mainly composed of sucrose–proton symporter SUT family members and SWEET family members. SUT works as sucrose positive transporter locates at the donor cell side; SWEET usually works at the acceptor cell side as efflux transporter. 

rice SUT(C) SWEET

1. Introduction of  plant SUT and SWEET transporters

Sugar is the most important component of cells. It provides not only cell structure materials but also energy-producing substances for organisms. For single-cell organisms that live on sugar, they need to produce or acquire sugar from their environments. For multiple-cell organisms such as plants and animals, they also need to allocate sugar from one cell to another in addition to producing or acquiring sugar from their environments. In most cases, sugar needs to be transported across the plasma membranes[1]. Two pathways are identified to be involved in sugar transport between cells[2]. One is the symplastic pathway that depends on plasmodesmata, the other is the apoplastic pathway that depends on membrane-located transporters[1][2].

In plants, SUT and SWEET represent the most important sugar transporters[3]. SUT is a class of sucrose–proton symporters only present in plants[4], they are extremely important for the acquisition of sucrose from the intercellular apoplast outside of the cell into the cytosol, particularly when no plasmodesma exists between cells undergoing sugar translocation, and a membrane transporter or channel is the only pathway for material exchange[5]. Moreover, in long-distance transport of sugar via the symplastic pathway, sucrose must be first uploaded into the phloem[6][7]. The uploading process relies on SUT transporter(s) since very few plasmodesmata exist between the SE–CC complexes and their surrounding cells. Additionally, during symplastic transport within the phloem, a small portion of sucrose may leak into the apoplast outside of the SE–CC complexes; retrieving this portion of sucrose back to phloem also requires the SUT transporter's participation[6]. Before being taken into the acceptor cell, sugar needs to be released first from the donor cell. As SUT sucrose transporters need a proton gradient to drive the transport process, it cannot accomplish sucrose export from the cytosol to the apoplast outside of the cell because the proton concentration in the cytosol is usually lower than that of the intercellular apoplast[8]. The presence of SWEET transporter solves the problem. SWEET is a class of unidirectional sugar transporters that can transport sugar in and out of the cell depending only on the concentration gradient across the membrane[8]. They are passive sugar transporters that can only transport sugar from higher concentration to lower concentration across the membrane. As a result, they can be used to export sugar including sucrose and glucose from the cytosol of the donor cell to the interface between the donor cell and the accepter cell[9]. Subsequently, the plasma membrane-located SUT transporter at the acceptor cell imports the sugar by active transport. Moreover,  SWEET transporters can also mediate sugar influx at the acceptor cell side. 

2. Physiological functions of rice SUT transporters

Rice is one of the most important crops for the human diet. It is widely cultivated in the world particularly in Asia. How to improve rice products and quality is a long-term mission to ensure food security. Understanding sugar transporter's function in rice is fundamental work to achieve this goal.

Rice possesses 5 SUT transporters in its genome[10]. They are mainly expressed in the tissues where sugar synthesis, translocation, and storage take place[11][12]. These activities include uploading sucrose into phloem for sugar long-distance transport, retrieving leaked sucrose back into the cytosol, absorbing sucrose from the matrix for pollen tube growth, transferring sucrose from the vacuole to the cytosol, and mobilizing sucrose from the endosperm for seed germination[13][14], etc. Interestingly, a single SUT gene may play a variety of physiological roles in rice growth and development[15]. For example, OsSUT1 is expressed in pollen, caryopsis, leaf, stem and root of rice[11][16]. It is strongly expressed in the peduncle and caryopsis that best represents sugar translocation from the source organ to the sink organ. The critical role that OsSUT1 played is probably in rice fertility[16]. Knockout of the gene sterilized rice since the mutant rice cannot bore viable seeds. The underlying reason is probably that the disruption of the nucellar and aleurone-strongly expressed OsSUT1 impedes sugar transport from the pericarp to the developing embryo. Consistent with its multiple physiological functions, OsSUT1 can transcribe at least 6 alternative splicing transcripts[16]. OsSUT2 is identified to locate on cell tonoplast[17]. Knockout of OsSUT2 reduced tiller number, plant height, grain weight, and root dry weight of rice. OsSUT3 is a protein specifically expressed in pollen, and it may be important for pollen and starch accumulation[18]. OsSUT4 is expressed in the vascular tissue of the embryo and coleoptile in the germinated seed; it is also expressed in the floret and the aleurone layer of the caryopsis at the seed-filling stage[19]. Knockout of OsSUT4 dwarfed the mutant rice lines, reduced their tiller number and grain yield. OsSUT5 is expressed widely in rice tissues; knockout of OsSUT5 reduced the rice seed-setting rate and conferred a chalky endosperm of the mutant caryopses[20].

3. Physiological functions of rice SWEET transporters

Rice SWEET transporter family possesses 21 members[21]. The first rice SWEET gene characterized with physiological function is OsSWEET4[22]. It encodes a glucose transporter that is expressed in the caryopsis. Knockout of the gene resulted in a serious defect in rice seed-filling and almost no viable seed is available in the mutant lines of the gene. Another SWEET gene that plays an important part in rice seed-filling is OsSWEET11[23]. The gene encodes a sucrose transporter[24]. It is strongly expressed in the developing caryopsis and stem of rice, particularly in the nucellar epidermis, ovule vascular, and phloem which represent the transport and sink organs where sucrose translocation is intensively taking place[23][24]. Knockout of the gene significantly reduces the 1000-grain weight of the mutant rice since their seed-filling is impaired[23][24]. Moreover, the seed-setting rate of the mutant rice is markedly reduced and the maturation of the grain is also prolonged compared with the wild-type rice[23]. OsSWEET15 encodes a sucrose transporter. It shares a very similar expression pattern with OsSWEET11, particularly in the caryopsis of rice during the early stage of seed development after pollination. Double mutation of OsSWEET11 and OsSWEET15 leads to complete infertility of rice[24]. Knockout of OsSWEET14 alone did not cause any abnormal phenotype; however, double mutation of OsSWEET11 and OsSWEET14 confers heavier impairment of seed-filling than single mutation of OsSWEET11[25].

In the rice SWEET gene family, members from the clade III including OsSWEET11, OsSWEET12, OsSWEET13, OsSWEET14, OsSWEET15 are identified to encode sucrose transporters although they can transport glucose as well[5]. In addition, OsSWEET11, OsSWEET13, and OsSWEET14 are pathogen-related genes[26]. By targeting effector-binding elements (EBEs) in the promoters of susceptible SWEET genes with transcription activator-like effectors (TALe), pathogens such as Xanthomonas oryzae pv. Oryzae (Xoo) or Rhizoctonia solani induce SWEET gene expression to grab sugar from the host plant cell for their propagations[27][28][29][30][31]. Recent research shows that mutation of the EBEs in the promoter regions of OsSWEET11, OsSWEET13, and OsSWEET14 conferred a broad-spectrum resistance of rice to Xoo variety infections[26][32]. Therefore, these SWEET genes are important for future breeding to obtain pathogen-resistant rice.

Despite the proceeding in the characterization of the SWEET gene’s functions listed above, many SWEET gene functions are still waiting to be addressed.

References

  1. Kühn, C.; Grof, C.P. Sucrose transporters of higher plants. Curr. Opin. Plant Biol. 2010, 13, 288–298.
  2. Zhang, W.H.; Zhou, Y.; Dibley, K.E.; Tyerman, S.D.; Furbank, R.T.; Patrick, J.W. Review: Nutrient loading of developing seeds. Funct. Plant Biol. 2007, 34, 314–331.
  3. Chen, L.Q.; Cheung, L.S.; Feng, L.; Tanner, W.; Frommer, W.B. Transport of sugars. Annu. Rev. Biochem. 2015, 84, 865–894.
  4. Riesmeier, J.W.; Willmitzer, L.; Frommer, W.B. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 1992, 11, 4705–4713.
  5. Chen, L.Q.; Hou, B.H.; Lalonde, S.; Takanaga, H.; Hartung, M.L.; Qu, X.Q.; Guo, W.J.; Kim, J.G.; Underwood, W.; Chaudhuri, B.; et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468, 527–532.
  6. Scofield, G.N.; Hirose, T.; Aoki, N.; Furbank, R.T. Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J. Exp. Bot. 2007, 58, 3155–3169.
  7. Chen, L.Q. SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 2014, 201, 1150–1155.
  8. Chen, L.Q.; Hou, B.H.; Lalonde, S.; Takanaga, H.; Hartung, M.L.; Qu, X.Q.; Guo, W.J.; Kim, J.G.; Underwood, W.; Chaudhuri, B.;et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468, 527–532.
  9. Chen, L.Q.; Qu, X.Q.; Hou, B.H.; Sosso, D.; Osorio, S.; Fernie, A.R.; Frommer, W.B. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 2012, 335, 207–211.
  10. Aoki, N.; Hirose, T.; Scofield, G.N.; Whitfeld, P.R.; Furbank, R.T. The sucrose transporter gene family in rice. Plant Cell Physiol. 2003, 44, 223–232.
  11. Hirose, T.; Imaizumi, N.; Scofield, G.N.; Furbank, R.T.; Ohsugi, R. cDNA cloning and tissue-specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol. 1997, 38, 1389–1396.
  12. Hu, Z.; Tang, Z.; Zhang, Y.;Niu, L.; Yang, F.; Zhang, D.; Hu, Y.Rice SUT and SWEET Transporters.Int. J. Mol. Sci. 2021, 22, 11198.
  13. 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. 2014, 65, 1713–1735.
  14. Scofield, G.N.; Aoki, N.; Hirose, T.; Takano, M.; Jenkins, C.L.; Furbank, R.T. The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants. J. Exp. Bot. 2007, 58, 483–495.
  15. Furbank, R.T.; Scofield, G.N.; Hirose, T.; Wang, X.D.; Patrick, J.; Offler, C.E. Cellular localization and function of a sucrose transporter OsSUT1 in developing rice seeds. Aust. J. Plant Physiol. 2001, 28, 1187–1196.
  16. Wang, X.; Liu, X.; Hu, Z.; Bao, S.; Xia, H.; Feng, B.; Ma, L.; Zhao, G.; Zhang, D.; Hu, Y. Essentiality for rice fertility and alternative splicing of OsSUT1. Plant Sci. 2021. doi.org/10.1016/j.plantsci.2021.111065
  17. Eom, J.S.; Cho, J.I.; Reinders, A.; Lee, S.W.; Yoo, Y.; Tuan, P.Q.; Choi, S.B.; Bang, G.; Park, Y.I.; Cho, M.H.; et al. Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol. 2011, 157, 109–119.
  18. Li, D.; Xu, R.; Lv, D.; Zhang, C.; Yang, H.; Zhang, J.; Wen, J.; Li, C.; Tan, X. Identification of the core pollen-specific regulation in the rice OsSUT3 promoter. Int. J. Mol. Sci. 2020, 21, 1909
  19. Chung, P.; Hsiao, H.H.; Chen, H.J.; Chang, C.W.; Wang, S.J. Influence of temperature on the expression of the rice sucrosetransporter 4 gene, OsSUT4, in germinating embryos and maturing pollen. Acta Physiol. Plant. 2014, 36, 217–229
  20. Zhang, Y.; Bao, S.; Tang, Z.; Wang, X.; Yang, F.; Zhang, D.; Hu, Y. Function of sucrose transporter OsSUT5 in rice pollendevelopment and seed setting. Sci. Agric. Sin. 2021, 55, 3369–3380. (In Chinese)
  21. Yuan, M.; Zhao, J.; Huang, R.; Li, X.; Xiao, J.; Wang, S. Rice MtN3/saliva/SWEET gene family: Evolution, expression profiling, and sugar transport. J. Integr. Plant Biol. 2014, 56, 559–570.
  22. Sosso, D.; Luo, D.; Li, Q.B.; Sasse, J.; Yang, J.; Gendrot, G.; Suzuki, M.; Koch, K.E.; McCarty, D.R.; Chourey, P.S.; et al. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat. Genet. 2015, 47, 1489–1493.
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  27. Yu, Y.; Streubel, J.; Balzergue, S.; Champion, A.; Boch, J.; Koebnik, R.; Feng, J.; Verdier, V.; Szurek, B. Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol. Plant Microbe Interact. 2011, 24, 1102–1113.
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