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Tea plant SWEET transporters: expression profiling, sugar transport, and the involvement of CsSWEET16 in modifying cold tolerance in Arabidopsis

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Thirteen SWEET transporters were identified in Camellia sinensis and the cold-suppression gene CsSWEET16 contributed to sugar compartmentation across the vacuole and function in modifying cold tolerance in Arabidopsis.

Abstract

The sugars will eventually be exported transporters (SWEET) family of sugar transporters in plants is a recently identified protein family of sugar uniporters that contain seven transmembrane helices harbouring two MtN3 motifs. SWEETs play important roles in various biological processes, including plant responses to environmental stimuli. In this study, 13 SWEET transporters were identified in Camellia sinensis and were divided into four clades. Transcript abundances of CsSWEET genes were detected in various tissues. CsSWEET1a/1b/2a/2b/2c/3/9b/16/17 were expressed in all of the selected tissues, whereas the expression of CsSWEET5/7/9a/15 was not detected in some tissues, including those of mature leaves. Expression analysis of nine CsSWEET genes in leaves in response to abiotic stresses, natural cold acclimation and Colletotrichum camelliae infection revealed that eight CsSWEET genes responded to abiotic stress, while CsSWEET3 responded to C. camelliae infection. Functional analysis of 13 CsSWEET activities in yeast revealed that CsSWEET1a/1b/7/17 exhibit transport activity for glucose analogues and other types of hexose molecules. Further characterization of the cold-suppression gene CsSWEET16 revealed that this gene is localized in the vacuolar membrane. CsSWEET16 contributed to sugar compartmentation across the vacuole and function in modifying cold tolerance in Arabidopsis. Together, these findings demonstrate that CsSWEET genes play important roles in the response to abiotic and biotic stresses in tea plants and provide insights into the characteristics of SWEET genes in tea plants, which could serve as the basis for further functional identification of such genes.

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Abbreviations

BLAST:

Basic local alignment search tool

Col-0:

Columbia-0

eGFP:

Enhanced green fluorescent protein

EL:

Electrolyte leakage

EST:

Expressed sequence tags

F v /F m :

Maximal quantum efficiency of photosystem II

GUS:

β-glucuronidase

MS:

Murashige and Skoog

OE:

Overexpression

ORF:

Open reading frame

qRT-PCR:

Quantitative RT-PCR

RT-PCR:

Reverse transcription PCR

SWEET:

Sugars will eventually be exported transporters

TM:

Transmembrane

WT:

Wild type

References

  • Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao H, Wang L, Yue C, Hao X, Wang X, Yang Y (2015) Isolation and expression analysis of 18 CsbZIP genes implicated in abiotic stress responses in the tea plant (Camellia sinensis). Plant Physiol Biochem 97:432–442

    Article  CAS  PubMed  Google Scholar 

  • Chandran D (2015) Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life 67:461–471

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532

    Article  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 335:207–211

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Huh JH, Yu YC, Ho LH, Chen LQ, Tholl D, Frommer WB, Guo WJ (2015a) The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. Plant J 83:1046–1058

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015b) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chong J, Piron MC, Meyer S, Merdinoglu D, Bertsch C, Mestre P (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot 65:6589–6601

    Article  CAS  PubMed  Google Scholar 

  • Ding Z, Li C, Shi H, Wang H, Wang Y (2015) Pattern of CsICE1 expression under cold or drought treatment and functional verification through analysis of transgenic Arabidopsis. Genet Mol Res 14:11259–11270

    Article  CAS  PubMed  Google Scholar 

  • Ehlert B, Hincha DK (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Etxeberria E, Pozueta-Romero J, Gonzalez P (2012) In and out of the plant storage vacuole. Plant Sci 190:52–61

    Article  CAS  PubMed  Google Scholar 

  • Feng CY, Han JX, Han XX, Jiang J (2015) Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene 573:261–272

    Article  CAS  PubMed  Google Scholar 

  • Gray GR, Hope BJ, Qin X, Taylor BG, Whitehead CL (2003) The characterization of photoinhibition and recovery during cold acclimation in Arabidopsis thaliana using chlorophyll fluorescence imaging. Physiol Plant 119:365–375

    Article  CAS  Google Scholar 

  • Guan Y, Huang X, Zhu J, Gao J, Zhang H, Yang Z (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 147:852–863

    Article  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 164:777–789

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Horvath D, Chao W, Yang Y, Wang X, Xiao B (2014) Identification and evaluation of reliable reference genes for quantitative real-time PCR analysis in tea plant (Camellia sinensis (L). O. Kuntze). Int J Mol Sci 15:22155–22172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao XY, Yang YJ, Yue C, Wang L, Horvath DP, Wang XC (2017) Comprehensive transcriptome analyses reveal differential gene expression profiles of Camellia sinensis axillary buds at para-, endo-, ecodormancy, and bud flush stages. Front Plant Sci 8:553

    PubMed  PubMed Central  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. Nat Commun 7:13245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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 171:554–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurusu T et al (2012) Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol 12:11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lemoine R et al (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X, Feng Z, Yang H, Zhu X, Liu J, Yuan H (2010) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt- and dehydration-tolerance in tobacco. Biochem Biophys Res Commun 394:354–359

    Article  CAS  PubMed  Google Scholar 

  • Li J, Qin M, Qiao X, Cheng Y, Li X, Zhang H, Wu J (2017a) A new insight into the evolution and functional divergence of SWEET transporters in Chinese White Pear (Pyrus bretschneideri). Plant Cell Physiol 58:839–850

    Article  PubMed  Google Scholar 

  • Li N, Qian W, Wang L, Cao H, Hao X, Yang Y, Wang X (2017b) Isolation and expression features of hexose kinase genes under various abiotic stresses in the tea plant (Camellia sinensis). J Plant Physiol 209:95–104

    Article  CAS  PubMed  Google Scholar 

  • Lin I et al (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508:546–549

    Article  CAS  PubMed  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 58:863–873

    Article  PubMed  Google Scholar 

  • Patil G et al (2015) Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genom 16:520

    Article  Google Scholar 

  • Poschet G, Hannich B, Raab S, Jungkunz I, Klemens PAW, Krueger S, Wic S, Neuhaus HE, Büttner M (2011) A novel Arabidopsis vacuolar glucose exporters is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol 157:1664–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian W, Yue C, Wang YC, Cao HL, Li NN, Wang L, Hao XY, Wang XC, Xiao B, Yang YJ (2016) Identification of the invertase gene family (INVs) in tea plant and their expression analysis under abiotic stress. Plant Cell Rep 35:2269–2283

    Article  CAS  PubMed  Google Scholar 

  • Schulze WX, Schneider T, Starck S, Martinoia E, Trentmann O (2012) Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J 69:529–541

    Article  CAS  PubMed  Google Scholar 

  • Seo P, Park J, Kang S, Kim S, Park C (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233:189–200

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sun MX, Huang XY, Yang J, Guan YF, Yang ZN (2013) Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reprod 26:83–91

    Article  CAS  PubMed  Google Scholar 

  • Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48:296–306

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Li X, Zhao Q, Jing S, Chen S, Yuan H (2009) Identification of genes induced in response to low-temperature treatment in tea leaves. Plant Mol Biol Rep 27:257–265

    Article  CAS  Google Scholar 

  • Wang Y, Jiang CJ, Li YY, Wei CL, Deng WW (2012) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant Cell Rep 31:27–34

    Article  PubMed  Google Scholar 

  • Wang L, Ying YH, Narsai R, Ye LX, Zheng LQ, Tian JL, Whelan J, Shou HX (2013a) Identification of OsbHLH133 as a regulator of iron distribution between roots and shoots in Oryza sativa. Plant Cell Environ 36:224–236

    Article  CAS  PubMed  Google Scholar 

  • Wang X et al (2013b) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genom 14:415

    Article  Google Scholar 

  • Wang C, Yue WH, Ying YH, Wang SD, Secco D, Liu Y, Whelan J, Tyerman SD, Shou HX (2015) Rice SPX-Major facility superfamily3, a vacuolar phosphate efflux transporter, is involved in maintaining phosphate homeostasis in rice. Plant Physiol 169:2822–2831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Cao HL, Qian EJ, Yao LN, Hao XY, Li NN, Yang YJ, Wang XC (2017) Identification of a novel bZIP transcription factor in Camellia sinensis as a negative regulator of freezing tolerance in transgenic Arabidopsis. Ann Bot 119:1195–1209

    Article  PubMed  Google Scholar 

  • Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg C, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464:123–128

    Article  CAS  PubMed  Google Scholar 

  • Wingenter K, Trentmann O, Winschuh I, Hörmiller II, Heyer AG, Reinders J, Schulz A, Geiger D, Hedrich R, Neuhaus HE (2011) A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J 68:890–900

    Article  CAS  PubMed  Google Scholar 

  • Xia EH et al (2017) The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Mol Plant 10:866–877

    Article  CAS  PubMed  Google Scholar 

  • Xuan YH, Hu YB, Chen LQ, Sosso D, Ducat DC, Hou BH, Frommer WB (2013) Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci USA 110: E3685–E3694

    Article  Google Scholar 

  • Yu F (1986) Discussion on the originating place and the originating centre of tea plant. J Tea Sci 6:1–8

    Google Scholar 

  • Yuan M, Wang S (2013) Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. Mol Plant 6:665–674

    Article  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 Integr Plant Biol 56:559–570

    Article  CAS  PubMed  Google Scholar 

  • Yue C, Cao HL, Wang L, Zhou YH, Hao XY, Zeng JM, Wang XC, Yang YJ (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76

    Article  CAS  PubMed  Google Scholar 

  • Yue C, Cao HL, Wang L, Zhou YH, Huang YT, Hao XY, Wang YC, Wang B, Yang YJ, Wang XC (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88:591–608

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y et al (2017) Molecular cloning and characterization of galactinol synthases in Camellia sinensis with different responses to biotic and abiotic stressors. J Agric Food Chem 65:2751–2759

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31500564), the Young Elite Scientist Sponsorship Program by CAST (2016QNRC001), the Central Public-interest Scientific Institution Basal Research Fund (1610212016006), the Earmarked Fund for China Agriculture Research System (CARS-19) and the Chinese Academy of Agricultural Sciences through an Innovation Project for Agricultural Sciences and Technology (CAAS-ASTIP-2017-TRICAAS). We thank Professor Dr. Eckhard Boles of institut für molekulare biowissenschaften Goethe-Universität Frankfurt for providing yeast strains EBY.VW4000 and Professor Dr. Huixia Shou of Zhejiang University for providing the vectors ADHpr-Yeplac195 and pBI101.3.

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  1. Lu Wang and Lina Yao have equally contributed to this work.

Authors and Affiliations

  1. National Center for Tea Plant Improvement, Tea Research Institute, Chinese Academy of Agricultural Sciences, 9th South of Meiling Road, Hangzhou, 310008, China

    Lu Wang, Lina Yao, Xinyuan Hao, Nana Li, Wenjun Qian, Chuan Yue, Changqing Ding, Jianming Zeng, Yajun Yang & Xinchao Wang

  2. Key Laboratory of Tea Biology and Resources Utilization, Ministry of Agriculture, Hangzhou, 310008, China

    Lu Wang, Xinyuan Hao, Jianming Zeng, Yajun Yang & Xinchao Wang

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  1. Lu Wang
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Contributions

LW, XCW and YJY participated in the design and coordination of the study. LW, LNY, XYH, NNL, WJQ, CY, CQD and JMZ performed the experiments. LW, LNY and XCW analyzed and discussed the data. LW and XCW wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Yajun Yang or Xinchao Wang.

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Wang, L., Yao, L., Hao, X. et al. Tea plant SWEET transporters: expression profiling, sugar transport, and the involvement of CsSWEET16 in modifying cold tolerance in Arabidopsis. Plant Mol Biol 96, 577–592 (2018). https://doi.org/10.1007/s11103-018-0716-y

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