Skip to main content

Advertisement

Log in

Decoding Sugar Regulation and Homeostasis in Plants: Cracking Functional Roles Under Stresses

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The plant system has been endowed with highly extensive defence system in order to protect them under severe environmental conditions. In response to adversities, plants have well developed and complexed metabolic network that comprises stress-responsive genes and metabolites for stress acclimation. Sugars are the part of many metabolic processes such as photosynthesis that plays crucial role in maintaining osmotic balance as well as sugar homeostasis. During stresses, they play critical role in stress perception as well as signalling and act as regulatory circuit for stress-mediated responses encoding for osmotic adjustments, ROS scavenging and cellular homeostasis. Numerous sugar transporters have been identified in carbohydrate partitioning along with signal transduction pathways in plants subjected to stresses. Specific sugar transporters, namely, SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER (SWEETs), POLYOLS TRANSPORTERS, SUCROSE TRANSPORTERS (SUTs), ORGANELLES SUGAR TRANSPORTERS, MONOSACCHARIDE TRANSPORTERS (MSTs) and SUGAR TRANSPORTER PROTEIN are predominantly involved for sugar loading/unloading and long-distance transport followed by stress tolerance. Therefore, it is essential to gain knowledge about structure and functions of sugar transporters and homeostasis in plants under stressed conditions. Advancement in studies have explored different sugar signalling cascades and their crosstalk during stressed conditions. Moreover, integrated approaches also enable the identification as well as characterisation of sugar transporters that may act as targets for stress resistance in plants along with enhancing crop yield and productivity. The present review aims at updated knowledge about sugar homeostasis in plants during stressed conditions along with detailed understanding about sugar transporters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdelrahman M, Burritt DJ, Gupta A, Tsujimoto H, Tran LS (2020) Heat stress effects on source–sink relationships and metabolome dynamics in wheat. J Exp Bot 71(2):543–554

    CAS  PubMed  Google Scholar 

  • Abelenda JA, Bergonzi S, Oortwijn M, Sonnewald S, Du M, Visser RG, Sonnewald U, Bachem CW (2019) Source-sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr Biol 29(7):1178–1186

    CAS  PubMed  Google Scholar 

  • Ahmad F, Singh A, Kamal A (2020) Osmoprotective role of sugar in mitigating abiotic stress in plants. Protective Chem Agents Amelioration Plant Abiotic Stress 22:53–70

    Google Scholar 

  • Ahmad IZ (2019) Role of sugars in abiotic stress signaling in plants. In Plant Signaling Molecules (pp. 207–217). Woodhead Publishing.

  • Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155(1):64–69

    CAS  PubMed  Google Scholar 

  • Aliche EB, Theeuwen TP, Oortwijn M, Visser RG, van der Linden CG (2020) Carbon partitioning mechanisms in potato under drought stress. Plant Physiol Biochem 146:211–219

    CAS  PubMed  Google Scholar 

  • Aluri S, Büttner M (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc Natl Acad Sci 104(7):2537–2542

    CAS  PubMed  PubMed Central  Google Scholar 

  • An J, Zeng T, Ji C, de Graaf S, Zheng Z, Xiao TT, Deng X, Xiao S, Bisseling T, Limpens E, Pan Z (2019) A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytol 224(1):396–408

    CAS  PubMed  Google Scholar 

  • Andrés F, Kinoshita A, Kalluri N, Fernández V, Falavigna VS, Cruz TM, Jang S, Chiba Y, Seo M, Mettler-Altmann T, Huettel B (2020) The sugar transporter SWEET10 acts downstream of FLOWERING LOCUS T during floral transition of Arabidopsis thaliana. BMC Plant Biol 20(1):1–4

    Google Scholar 

  • Aoki N, Whitfeld P, Hoeren F, Scofield G, Newell K, Patrick J, Offler C, Clarke B, Rahman S, Furbank RT (2002) Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Mol Biol 50(3):453–462

    CAS  PubMed  Google Scholar 

  • Asai Y, Kobayashi Y, Kobayashi I (2016) Increased expression of the tomato SlSWEET15 gene during grey mold infection and the possible involvement of the sugar efflux to apoplasm in the disease susceptibility. J Plant Pathol Microbiol. https://doi.org/10.4172/2157-7471.1000329

    Article  Google Scholar 

  • Bezrutczyk M, Yang J, Eom JS, Prior M, Sosso D, Hartwig T, Szurek B, Oliva R, Vera-Cruz C, White FF, Yang B (2018) Sugar flux and signaling in plant–microbe interactions. Plant J 93(4):675–685

    CAS  PubMed  Google Scholar 

  • Bhattacharya S, Kundu A (2020) Sugars and sugar polyols in overcoming environmental stresses. Protective Chem Agents Amelioration Plant Abiotic Stress 22:71–101

    Google Scholar 

  • Bihmidine S, Julius BT, Dweikat I, Braun DM (2016) Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems. Plant Signaling & Behavior. 11(1):e1117721

    Google Scholar 

  • Bogdanove AJ (2014) Principles and applications of TAL effectors for plant physiology and metabolism. Curr Opi Plant Biol 19:99–104

    CAS  Google Scholar 

  • Breia R, Conde A, Conde C, Fortes AM, Granell A, Gerós H (2020) VvERD6l13 is a grapevine sucrose transporter highly up-regulated in response to infection by Botrytis cinerea and Erysiphe necator. Plant Physiol Biochem 154:508–516

    CAS  PubMed  Google Scholar 

  • Büttner M (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biol 12:35–41

    PubMed  Google Scholar 

  • Cai Y, Tu W, Zu Y, Yan J, Xu Z, Lu J, Zhang Y (2017) Overexpression of a grapevine sucrose transporter (VvSUC27) in tobacco improves plant growth rate in the presence of sucrose in vitro. Front Plant Sci 8:1069

    PubMed  PubMed Central  Google Scholar 

  • Cai Y, Yan J, Li Q, Deng Z, Liu S, Lu J, Zhang Y (2019) Sucrose transporters of resistant grapevine are involved in stress resistance. Plant Mol Biol 100(1):111–132

    CAS  PubMed  Google Scholar 

  • Cai Y, Yan J, Tu W, Deng Z, Dong W, Gao H, Xu J, Zhang N, Yin L, Meng Q, Zhang Y (2020) Expression of sucrose transporters from Vitis vinifera confer high yield and enhances drought resistance in Arabidopsis. International J Mol Sci 21(7):2624

    CAS  Google Scholar 

  • Chang Q, Liu J, Lin X, Hu S, Yang Y, Li D, Chen L, Huai B, Huang L, Voegele RT, Kang Z (2017) A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection. New Phytol 215(4):1548–1561

    CAS  PubMed  Google Scholar 

  • Chauhan S, Forsthoefel N, Ran Y, Quigley F, Nelson DE, Bohnert HJ (2000) Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum. Plant J 24(4):511–522

    CAS  PubMed  Google Scholar 

  • Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468(7323):527–532

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335(6065):207–211

    CAS  PubMed  Google Scholar 

  • Chen LQ, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of sugars. Ann Rev Biochem 84:865–894

    CAS  PubMed  Google Scholar 

  • Cho JI, Burla B, Lee DW, Ryoo N, Hong SK, Kim HB, Eom JS, Choi SB, Cho MH, Bhoo SH, Hahn TR (2010) Expression analysis and functional characterization of the monosaccharide transporters, OsTMTs, involving vacuolar sugar transport in rice (Oryza sativa). New Phytol 186(3):657–668

    CAS  PubMed  Google Scholar 

  • Cohn M, Bart RS, Shybut M, Dahlbeck D, Gomez M, Morbitzer R, Hou BH, Frommer WB, Lahaye T, Staskawicz BJ (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector–mediated induction of a SWEET sugar transporter in cassava. Mol Plant-Microbe Interac 27(11):1186–1198

    Google Scholar 

  • Conde A, Silva P, Agasse A, Conde C, Gerós H (2011) Mannitol transport and mannitol dehydrogenase activities are coordinated in Olea europaea under salt and osmotic stresses. Plant Cell Physiol 52(10):1766–1775

    CAS  PubMed  Google Scholar 

  • Cox KL, Meng F, Wilkins KE, Li F, Wang P, Booher NJ, Carpenter SC, Chen LQ, Zheng H, Gao X, Zheng Y (2017) TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton. Nature Commun 8(1):1–4

    Google Scholar 

  • Deng X, An B, Zhong H, Yang J, Kong W, Li Y (2019) A novel insight into functional divergence of the MST gene family in rice based on comprehensive expression patterns. Genes 10(3):239

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doidy J, Vidal U, Lemoine R (2019) Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum. PLoS ONE 14(9):e0223173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong S, Beckles DM (2019) Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J Plant Physiol 234:80–93

    PubMed  Google Scholar 

  • Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N (2016) Water deficit enhances C export to the roots in Arabidopsis thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiol 170(3):1460–1479

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm Identification of male gamete promoters in Arabidopsis. Plant Physiol 138(4):2124–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eom JS, Chen LQ, Sosso D, Julius BT, Lin IW, Qu XQ, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opi Plant Biol 25:53–62

    CAS  Google Scholar 

  • Feng L, Frommer WB (2015) Structure and function of SemiSWEET and SWEET sugar transporters. Trends Biochem Sci 40(8):480–486

    CAS  PubMed  Google Scholar 

  • Gamas P, de Carvalho NF, Lescure N, Cullimore JV (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. MPMI-Mol Plant Microbe Interact 9(4):233–242

    CAS  Google Scholar 

  • Gao Y, Zhang C, Han X, Wang ZY, Ma L, Yuan DP, Wu JN, Zhu XF, Liu JM, Li DP, Hu YB (2018) Inhibition of OsSWEET11 function in mesophyll cells improves resistance of rice to sheath blight disease. Mol Plant Pathol 19(9):2149–2161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ge YX, Angenent GC, Dahlhaus E, Franken J, Peters J, Wullens GJ, Creemers-Molenaar J (2001) Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida. Mol Genet Genom 265:414–423

    CAS  Google Scholar 

  • Geng Y, Wu M, Zhang C (2020) Sugar transporter ZjSWEET2. 2 mediates sugar loading in leaves of Ziziphus jujuba mill. Front Plant Sci 11:1081

    PubMed  PubMed Central  Google Scholar 

  • Ghate T, Barvkar V, Deshpande S, Bhargava S (2019) Role of ABA signaling in regulation of stem sugar metabolism and transport under post-flowering drought stress in sweet sorghum. Plant Mol Biol Rep 37(4):303–313

    CAS  Google Scholar 

  • Gong X, Liu M, Zhang L, Ruan Y, Ding R, Ji Y, Zhang N, Zhang S, Farmer J, Wang C (2015) Arabidopsis AtSUC2 and AtSUC4, encoding sucrose transporters, are required for abiotic stress tolerance in an ABA-dependent pathway. Physiol Plant 153(1):119–136

    CAS  PubMed  Google Scholar 

  • Gong X, Liu ML, Wang C, Zhang LJ, Liu W (2013) Sucrose transporter gene AtSUC4 regulates sucrose distribution and metabolism in response to salt stress in Arabidopsis thaliana. Adv Mater Res 726:217–221

    Google Scholar 

  • Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147(2):852–863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo WJ, Nagy R, Chen HY, Pfrunder S, Yu YC, Santelia D, Frommer WB, Martinoia E (2014) SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol 164(2):777–789

    CAS  PubMed  Google Scholar 

  • Guo C, Li H, Xia X, Liu X, Yang L (2018) Functional and evolution characterization of SWEET sugar transporters in Ananas comosus. Biochem Biophys Res Commun 496(2):407–414

    CAS  PubMed  Google Scholar 

  • Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytol 211(2):386–403

    CAS  PubMed  Google Scholar 

  • Hennion N, Durand M, Vriet C, Doidy J, Maurousset L, Lemoine R, Pourtau N (2019) Sugars en route to the roots: transport, metabolism and storage within plant roots and towards microorganisms of the rhizosphere. Physiol Plant 165(1):44–57

    CAS  PubMed  Google Scholar 

  • Ho LH, Klemens PA, Neuhaus HE, Ko HY, Hsieh SY, Guo WJ (2019) Sl SWEET1a is involved in glucose import to young leaves in tomato plants. J Exp Bot 70(12):3241–3254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer WB, Yang B, White FF, Wang N, Jones JB (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci 111(4):E521–E529

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu LP, Zhang F, Song SH, Tang XW, Hui XU, Liu GM, Yaqin WA, HE HJ, (2017) Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. J Int Agric 16(7):1486–1501

    CAS  Google Scholar 

  • Hu B, Wu H, Huang W, Song J, Zhou Y, Lin Y (2019) SWEET gene family in Medicago truncatula: genome-wide identification, expression and substrate specificity analysis. Plants 8(9):338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang BL, Li X, Liu P, Ma L, Wu W, Zhang X, Li Z, Huang B (2019) Transcriptomic analysis of Eruca vesicaria subs sativa lines with contrasting tolerance to polyethylene glycol-simulated drought stress. BMC Plant Biol 19(1):1–1

    Google Scholar 

  • Ibraheem O, Dealtry G, Roux S, Bradley G (2011) The effect of drought and salinity on the expressional levels of sucrose transporters in rice (‘Oryza sativa’Nipponbare) cultivar plants. Plant Omics 4(2):68–74

    CAS  Google Scholar 

  • Jackson RS (2014) Specific and distinctive wine styles: wine science: principles and practices, 4th edn. Academic Press, San Diego, p 714

    Google Scholar 

  • Janz D, Behnke K, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Polle A (2010) Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol 10(1):1–7

    Google Scholar 

  • Jeena GS, Kumar S, Shukla RK (2019) Structure, evolution and diverse physiological roles of SWEET sugar transporters in plants. Plant Mol Biol 100(4):351–365

    CAS  PubMed  Google Scholar 

  • Jia W, Zhang L, Wu D, Liu S, Gong X, Cui Z, Cui N, Cao H, Rao L, Wang C (2015) Sucrose transporter AtSUC9 mediated by a low sucrose level is involved in Arabidopsis abiotic stress resistance by regulating sucrose distribution and ABA accumulation. Plant Cell Physiol 56(8):1574–1587

    CAS  PubMed  Google Scholar 

  • Jing LU, Sun MH, Hui KA, Liu YJ, Hao YJ, You CX (2019) MdSWEET17, a sugar transporter in apple, enhances drought tolerance in tomato. J Int Agric 18(9):2041–2051

    Google Scholar 

  • Juchaux-Cachau M, Landouar-Arsivaud L, Pichaut JP, Campion C, Porcheron B, Jeauffre J, Noiraud-Romy N, Simoneau P, Maurousset L, Lemoine R (2007) Characterization of AgMaT2, a plasma membrane mannitol transporter from celery, expressed in phloem cells, including phloem parenchyma cells. Plant Physiol 145(1):62–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Julius BT, Leach KA, Tran TM, Mertz RA, Braun DM (2017) Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol 58(9):1442–1460

    CAS  PubMed  Google Scholar 

  • Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T, Sano N, Koshiba T, Kamiya Y, Ueda M, Seo M (2016) AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nature Commun 7(1):1–1

    Google Scholar 

  • Kanwar P, Jha G (2019) Alterations in plant sugar metabolism: signatory of pathogen attack. Planta 249(2):305–318

    CAS  PubMed  Google Scholar 

  • Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44(5):730–743

    CAS  PubMed  Google Scholar 

  • Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40(2):482–487

    CAS  Google Scholar 

  • Kiyosue T, Abe H, Yamaguchi-Shinozaki K, Shinozaki K (1998) ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochimica et Biophysica Acta (BBA). 1370(2):187–91

    CAS  PubMed  Google Scholar 

  • Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163(3):1338–1352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klemens PA, Patzke K, Trentmann O, Poschet G, Büttner M, Schulz A, Marten I, Hedrich R, Neuhaus HE (2014) Overexpression of a proton-coupled vacuolar glucose exporter impairs freezing tolerance and seed germination. New Phytol 202(1):188–197

    CAS  PubMed  Google Scholar 

  • Kong W, An B, Zhang Y, Yang J, Li S, Sun T, Li Y (2019) Sugar transporter proteins (STPs) in Gramineae crops: comparative analysis, phylogeny, evolution, and expression profiling. Cells 8(6):560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kretschmer M, Croll D, Kronstad JW (2017) Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation. Mol Plant Pathol 18(9):1222–1237

    CAS  PubMed  Google Scholar 

  • Kryvoruchko IS, Sinharoy S, Torres-Jerez I, Sosso D, Pislariu CI, Guan D, Murray J, Benedito VA, Frommer WB, Udvardi MK (2016) MtSWEET11, a nodule-specific sucrose transporter of Medicago truncatula. Plant Physiol 171(1):554–565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opinion Plant Biol 13(3):287–297

    Google Scholar 

  • Le Hir R, Spinner L, Klemens PA, Chakraborti D, de Marco F, Vilaine F, Wolff N, Lemoine R, Porcheron B, Géry C, Téoulé E (2015) Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular development and freezing tolerance in Arabidopsis. Mol Plant 8(11):1687–1690

    PubMed  Google Scholar 

  • Lemonnier P, Gaillard C, Veillet F, Verbeke J, Lemoine R, Coutos-Thévenot P, La Camera S (2014) Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Mol Biol 85(4):473–484

    CAS  PubMed  Google Scholar 

  • Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opi Plant Biol 33:116–125

    Google Scholar 

  • Li Y, Wang Y, Zhang H, Zhang Q, Zhai H, Liu Q, He S (2017) The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. Front Plant Sci 8:197

    PubMed  PubMed Central  Google Scholar 

  • Li W, Ren Z, Wang Z, Sun K, Pei X, Liu Y, He K, Zhang F, Song C, Zhou X, Zhang W (2018) Evolution and stress responses of Gossypium hirsutum SWEET genes. Int J Mol Sci 19(3):769

    PubMed  PubMed Central  Google Scholar 

  • Li J, Chen D, Jiang GL, Song HY, Tu MY, Sun SX (2020) Molecular cloning and expression analysis of EjSWEET15, enconding for a sugar transporter from loquat. Sci Horti 272:109552

    CAS  Google Scholar 

  • Lin IW, Sosso D, Chen LQ, Gase K, Kim SG, Kessler D, Klinkenberg PM, Gorder MK, Hou BH, Qu XQ, Carter CJ (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508(7497):546–549

    CAS  PubMed  Google Scholar 

  • Liu Q, Yuan M, Zhou YA, Li X, Xiao J, Wang S (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ 34(11):1958–1969

    CAS  PubMed  Google Scholar 

  • Liu X, Zhang Y, Yang C, Tian Z, Li J (2016) AtSWEET4, a hexose facilitator, mediates sugar transport to axial sinks and affects plant development. Sci Rep 6(1):1–2

    Google Scholar 

  • Loreti E, Perata P (2020) The many facets of hypoxia in plants. Plants 9(6):745

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y (2017) Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol 58(5):863–873

    CAS  PubMed  Google Scholar 

  • Ma QJ, Sun MH, Lu J, Kang H, You CX, Hao YJ (2019) An apple sucrose transporter MdSUT2. 2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought. Plant Biotechnol J 17(3):625–37

    CAS  PubMed  Google Scholar 

  • Manck-Götzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487

    PubMed  PubMed Central  Google Scholar 

  • Martínez-Noël GM, Tognetti JA (2018) Sugar signaling under abiotic stress in plants. In Plant metabolites and regulation under environmental stress 2018 Jan 1 (pp. 397–406). Academic Press.

  • Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58(1):83–102

    CAS  PubMed  Google Scholar 

  • Meteier E, La Camera S, Goddard ML, Laloue H, Mestre P, Chong J (2019) Overexpression of the VvSWEET4 transporter in grapevine hairy roots increases sugar transport and contents and enhances resistance to Pythium irregulare, a soilborne pathogen. Front Plant Sci 10:884

    PubMed  PubMed Central  Google Scholar 

  • Miao H, Sun P, Liu Q, Miao Y, Liu J, Zhang K, Hu W, Zhang J, Wang J, Wang Z, Jia C (2017) Genome-wide analyses of SWEET family proteins reveal involvement in fruit development and abiotic/biotic stress responses in banana. Sci Rep 7(1):1–5

    Google Scholar 

  • Morii M, Sugihara A, Takehara S, Kanno Y, Kawai K, Hobo T, Hattori M, Yoshimura H, Seo M, Ueguchi-Tanaka M (2020) The dual function of OsSWEET3a as a gibberellin and glucose transporter is important for young shoot development in rice. Plant Cell Physiol 61(11):1935–1945

    CAS  PubMed  Google Scholar 

  • Moriyama EN, Strope PK, Opiyo SO, Chen Z, Jones AM (2006) Mining the Arabidopsis thaliana genome for highly-divergent seven transmembrane receptors. Gen Biol 7(10):1–9

    Google Scholar 

  • Navarro C, Abelenda JA, Cruz-Oró E, Cuellar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478(7367):119–122

    CAS  PubMed  Google Scholar 

  • Ni J, Li J, Zhu R, Zhang M, Qi K, Zhang S, Wu J (2020) Overexpression of sugar transporter gene PbSWEET4 of pear causes sugar reduce and early senescence in leaves. Gene 743:144582

    CAS  PubMed  Google Scholar 

  • Niño-González M, Novo-Uzal E, Richardson DN, Barros PM, Duque P (2019) More transporters, more substrates: the Arabidopsis major facilitator superfamily revisited. Mol Plant 2(9):1182–1202

    Google Scholar 

  • Noiraud N, Maurousset L, Lemoine R (2001) Transport of polyols in higher plants. Plant Physiol Biochem 39(9):717–728

    CAS  Google Scholar 

  • Oliva R, Quibod IL (2017) Immunity and starvation: new opportunities to elevate disease resistance in crops. Curr Opi Plant Biol 38:84–91

    CAS  Google Scholar 

  • Patel TK, Williamson JD (2016) Mannitol in plants, fungi, and plant–fungal interactions. Trends Plant Sci 21(6):486–497

    CAS  PubMed  Google Scholar 

  • Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L) cultivars differing in salinity tolerance. Indian J Exp Biol 46(10):736–42

    CAS  PubMed  Google Scholar 

  • Patzke K, Prananingrum P, Klemens PA, Trentmann O, Rodrigues CM, Keller I, Fernie AR, Geigenberger P, Bölter B, Lehmann M, Schmitz-Esser S (2019) The plastidic sugar transporter pSuT influences flowering and affects cold responses. Plant Physiol 179(2):569–587

    CAS  PubMed  Google Scholar 

  • Pereira A (2016) Plant abiotic stress challenges from the changing environment. Front Plant Sci 7:1123

    PubMed  PubMed Central  Google Scholar 

  • Pertl-Obermeyer H, Trentmann O, Duscha K, Neuhaus HE, Schulze WX (2016) Quantitation of vacuolar sugar transporter abundance changes using QconCAT synthtetic peptides. Front Plant Sci 7:411

    PubMed  PubMed Central  Google Scholar 

  • Phukan UJ, Jeena GS, Tripathi V, Shukla RK (2018) Ma RAP 2–4, a waterlogging-responsive ERF from Mentha, regulates bidirectional sugar transporter At SWEET 10 to modulate stress response in Arabidopsis. Plant Biotechnol J 16(1):221–233

    CAS  PubMed  Google Scholar 

  • Qazi HA, Rao PS, Kashikar A, Suprasanna P, Bhargava S (2014) Alterations in stem sugar content and metabolism in sorghum genotypes subjected to drought stress. Functional Plant Biol 41(9):954–962

    CAS  Google Scholar 

  • Ren R, Yue X, Li J, Xie S, Guo S, Zhang Z (2020) Coexpression of sucrose synthase and the SWEET transporter, which are associated with sugar hydrolysis and transport, respectively, increases the hexose content in Vitis vinifera L grape berries. Front Plant Sci 11:321

    PubMed  PubMed Central  Google Scholar 

  • Reuscher S, Akiyama M, Yasuda T, Makino H, Aoki K, Shibata D, Shiratake K (2014) The sugar transporter inventory of tomato: genome-wide identification and expression analysis. Plant Cell Physiol 55(6):1123–1141

    CAS  PubMed  Google Scholar 

  • Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11(13):4705–4713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez M, Parola R, Andreola S, Pereyra C, Martínez-Noël G (2019) TOR and SnRK1 signaling pathways in plant response to abiotic stresses: do they always act according to the “yin-yang” model? Plant Sci 288:110220

    CAS  PubMed  Google Scholar 

  • Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29(3):426–434

    CAS  PubMed  Google Scholar 

  • Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars: metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4(5):388–393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saddhe AA, Kundan K, Padmanabh D (2017) Mechanism of ABA signaling in response to abiotic stress in plants. Mechanism Plant Hormone Signaling Under Stress 1:173–195

    CAS  Google Scholar 

  • Sakr S, Wang M, Dédaldéchamp F, Perez-Garcia MD, Ogé L, Hamama L, Atanassova R (2018) The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. Int J Mol Sci 19(9):2506

    PubMed  PubMed Central  Google Scholar 

  • Salmon Y, Lintunen A, Dayet A, Chan T, Dewar R, Vesala T, Hölttä T (2020) Leaf carbon and water status control stomatal and nonstomatal limitations of photosynthesis in trees. New Phytol 226(3):690–703

    CAS  PubMed  Google Scholar 

  • Sambe MA, He X, Tu Q, Guo Z (2015) A cold-induced myo-inositol transporter-like gene confers tolerance to multiple abiotic stresses in transgenic tobacco plants. Physiol Plant 153(3):355–364

    CAS  PubMed  Google Scholar 

  • Schmidt RR, Weits DA, Feulner CF, van Dongen JT (2018) Oxygen sensing and integrative stress signaling in plants. Plant Physiol 176(2):1131–1142

    CAS  PubMed  Google Scholar 

  • Schneider S (2015) Inositol transport proteins. FEBS Lett 589(10):1049–1058

    CAS  PubMed  Google Scholar 

  • Schneider S, Schneidereit A, Udvardi P, Hammes U, Gramann M, Dietrich P, Sauer N (2007) Arabidopsis INOSITOL TRANSPORTER2 mediates H+ symport of different inositol epimers and derivatives across the plasma membrane. Plant Physiol 145(4):1395–1407

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sellami S, Le Hir R, Thorpe MR, Vilaine F, Wolff N, Brini F, Dinant S (2019) Salinity effects on sugar homeostasis and vascular anatomy in the stem of the Arabidopsis thaliana inflorescence. Int J Mol Sci 20(13):3167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Park JM, Kang SK, Kim SG, Park CM (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233(1):189–200

    CAS  PubMed  Google Scholar 

  • Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GP, Bali AS, Handa N, Kapoor D, Bhardwaj R, Zheng B (2019) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7):285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Wang B, Yang P, Li Y, Miao F (2016) Differences in sugar accumulation and mobilization between sequential and non-sequential senescence wheat cultivars under natural and drought conditions. PloS one 11(11):e0166155

    PubMed  PubMed Central  Google Scholar 

  • Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio/technol 14(3):407–426

    CAS  Google Scholar 

  • Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115(3):433–447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slewinski TL, Garg A, Johal GS, Braun DM (2010) Maize SUT1 functions in phloem loading. Plant Signal Behav 5(6):687–690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sosso D, Luo D, Li QB, Sasse J, Yang J, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47(12):1489–1493

    CAS  PubMed  Google Scholar 

  • Sugiyama A, Saida Y, Yoshimizu M, Takanashi K, Sosso D, Frommer WB, Yazaki K (2017) Molecular characterization of LjSWEET3, a sugar transporter in nodules of Lotus japonicus. Plant Cell Physiol 58(2):298–306

    CAS  PubMed  Google Scholar 

  • Suprasanna P, Nikalje GC, Rai AN (2016) Osmolyte accumulation and implications in plant abiotic stress tolerance. In: Iqbal N, Nazar R, Khan NA (eds) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, New Delhi, pp 1–12

    Google Scholar 

  • Suwa R, Nguyen NT, Saneoka H, Moghaieb R, Fujita K (2006) Effect of salinity stress on photosynthesis and vegetative sink in tobacco plants. Soil Science Plant Nutrit 52(2):243–250

    CAS  Google Scholar 

  • Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214(3):943–951

    CAS  PubMed  Google Scholar 

  • Tian L, Liu L, Yin Y, Huang M, Chen Y, Xu X, Wu P, Li M, Wu G, Jiang H, Chen Y (2017) Heterogeneity in the expression and subcellular localization of polyol/monosaccharide transporter genes in Lotus japonicus. PLoS ONE 12(9):e0185269

    PubMed  PubMed Central  Google Scholar 

  • Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59(11):2905–2916

    CAS  PubMed  Google Scholar 

  • Walker AS, Leroux P (2015) Grapevine gray mold in France. In: Ishii H, Hollomon DW (eds) Fungicide resistance in plant pathogens. Springer, Tokyo, pp 419–432

    Google Scholar 

  • Wang L, Yao L, Hao X, Li N, Qian W, Yue C, Ding C, Zeng J, Yang Y, Wang X (2018) Tea plant SWEET transporters: expression profiling, sugar transport, and the involvement of CsSWEET16 in modifying cold tolerance in Arabidopsis. Plant Mol Biol 96(6):577–592

    CAS  PubMed  Google Scholar 

  • Wang S, Yokosho K, Guo R, Whelan J, Ruan YL, Ma JF, Shou H (2019) The soybean sugar transporter GmSWEET15 mediates sucrose export from endosperm to early embryo. Plant Physiol 180(4):2133–2141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Liu S, Wang J, Yokosho K, Zhou B, Yu YC, Liu Z, Frommer WB, Ma JF, Chen LQ, Guan Y (2020) Simultaneous changes in seed size, oil content and protein content driven by selection of SWEET homologues during soybean domestication. Natl Sci Rev 7(11):1776–1786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wani SH, Kumar V, Khare T, Guddimalli R, Parveda M, Solymosi K, Suprasanna P, Kishor PK (2020) Engineering salinity tolerance in plants: progress and prospects. Planta 251(4):1–29

    Google Scholar 

  • Wingler A, Roitsch T (2008) Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol 10:50–62

    CAS  PubMed  Google Scholar 

  • Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18(12):3476–3490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wurzinger B, Nukarinen E, Nägele T, Weckwerth W, Teige M (2018) The SnRK1 kinase as central mediator of energy signaling between different organelles. Plant Physiol 176(2):1085–1094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XH, Wang C, Li SX, Su ZZ, Zhou HN, Mao LJ, Feng XX, Liu PP, Chen X, Snyder JH, Kubicek CP (2015) Friend or foe: differential responses of rice to invasion by mutualistic or pathogenic fungi revealed by RNAseq and metabolite profiling. Sci Rep 5(1):1–4

    Google Scholar 

  • Xu Q, Yin S, Ma Y, Song M, Song Y, Mu S, Li Y, Liu X, Ren Y, Gao C, Chen S (2020) Carbon export from leaves is controlled via ubiquitination and phosphorylation of sucrose transporter SUC2. Proc Natl Acad Sci 117(11):6223–6230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2010) Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. J Biol Chem 285(2):1138–1146

    CAS  PubMed  Google Scholar 

  • Yamada K, Saijo Y, Nakagami H, Takano Y (2016) Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science 354(6318):1427–1430

    CAS  PubMed  Google Scholar 

  • Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci 103(27):10503–10508

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Luo D, Yang B, Frommer WB, Eom JS (2018) SWEET 11 and 15 as key players in seed filling in rice. New Phytol 218(2):604–615

    CAS  PubMed  Google Scholar 

  • Yang G, Xu H, Zou Q, Zhang J, Jiang S, Fang H, Wang Y, Su M, Wang N, Chen X (2020) The vacuolar membrane sucrose transporter MdSWEET16 plays essential roles in the cold tolerance of apple. Plant Cell Tissue Organ Culture (PCTOC) 140(1):129–142

    CAS  Google Scholar 

  • Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch-related α-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol 138(2):837–846

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Streubel J, Balzergue S, Champion A, Boch J, Koebnik R, Feng J, Verdier V, Szurek B (2011) 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 24(9):1102–13

    CAS  PubMed  Google Scholar 

  • Yuan M, Zhao J, Huang R, Li X, Xiao J, Wang S (2014) Rice MtN3/saliva/SWEET gene family: evolution, expression profiling, and sugar transport. J Int Plant Biol 56(6):559–570

    CAS  Google Scholar 

  • Zanella M, Borghi GL, Pirone C, Thalmann M, Pazmino D, Costa A, Santelia D, Trost P, Sparla F (2016) β-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress. J Exp Bot 67(6):1819–1826

    CAS  PubMed  Google Scholar 

  • Zhang Y, Lv Y, Jahan N, Chen G, Ren D, Guo L (2018) Sensing of abiotic stress and ionic stress responses in plants. Int J Mol Sci 19(11):3298

    PubMed  PubMed Central  Google Scholar 

  • Zhang W, Wang S, Yu F, Tang J, Shan X, Bao K, Yu L, Wang H, Fei Z, Li J (2019) Genome-wide characterization and expression profiling of SWEET genes in cabbage (Brassica oleracea var capitata L) reveal their roles in chilling and clubroot disease responses. BMC Genom 20(1):1–6

    Google Scholar 

  • Zhen Q, Fang T, Peng Q, Liao L, Zhao L, Owiti A, Han Y (2018) Developing gene-tagged molecular markers for evaluation of genetic association of apple SWEET genes with fruit sugar accumulation. Hortic Res 5(1):1–2

    CAS  Google Scholar 

  • Zhou Y, Liu L, Huang W, Yuan M, Zhou F, Li X, Lin Y (2014) Overexpression of OsSWEET5 in rice causes growth retardation and precocious senescence. PLoS ONE 9(4):e94210

    PubMed  PubMed Central  Google Scholar 

  • Zhou A, Ma H, Feng S, Gong S, Wang J (2018a) A novel sugar transporter from Dianthus spiculifolius, DsSWEET12, affects sugar metabolism and confers osmotic and oxidative stress tolerance in Arabidopsis. Int J Molecular Sci 19(2):497

    Google Scholar 

  • Zhou A, Ma H, Feng S, Gong S, Wang J (2018b) DsSWEET17, a tonoplast-localized sugar transporter from Dianthus spiculifolius, affects sugar metabolism and confers multiple stress tolerance in Arabidopsis. Int J Molecular Sci 19(6):1564

    Google Scholar 

  • Zulfiqar F, Akram NA, Ashraf M (2020) Osmoprotection in plants under abiotic stresses: new insights into a classical phenomenon. Planta 251(1):1–7

    Google Scholar 

Download references

Acknowledgements

None

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

KK performed conceptualization, analysis and interpretation, writing of the original draft and designing the figures. PO provided the critical feedback and shaped the manuscript. RB critically revised the manuscript.

Corresponding authors

Correspondence to Kanika Khanna or Renu Bhardwaj.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Handling Editor: Parvaiz Ahmad.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khanna, K., Ohri, P. & Bhardwaj, R. Decoding Sugar Regulation and Homeostasis in Plants: Cracking Functional Roles Under Stresses. J Plant Growth Regul 42, 4797–4817 (2023). https://doi.org/10.1007/s00344-022-10727-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10727-w

Keywords

Navigation