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CsHT11 encodes a pollen-specific hexose transporter and is induced under high level sucrose in pollen tubes of cucumber (Cucumis sativus)

  • Suying Wen
  • Tianyang Bao
  • Xiangwei Zeng
  • Zhilong Bie
  • Jintao ChengEmail author
Original paper
  • 14 Downloads

Abstract

Pollen tubes require a high amount of sugars to sustain high growth rate. Sucrose, the main transport form of sugars, can serve as energy supply and as signaling molecules for pollen tube growth. We report the functional characterization of CsHT11, which is a sugar transporter protein/hexose transport protein (STP/HT). CsHT11 shares high homology with the characterized cucumber hexose transporter CsHT1, a pollen-specific gene. Analysis of CsHT11 mRNA and CsHT11 promoter-reporter gene studies revealed CsHT11 specifically expressed in pollen and pollen tubes. Subcellular localization indicated that CsHT11 is a plasma membrane transporter. Heterologous expression in yeast suggests that CsHT11 is an energy-dependent hexose/H+ symporter, with a wide variety of substrate specificity, including glucose, fructose, galactose, and mannose. In vitro pollen germination of different sugars shows that the expression of CsHT11 is significantly increased with higher sucrose content, but not with higher glucose or fructose content, thereby implying that CsHT11 may be involved in sucrose signal transduction. Thus, CsHT11 might have an essential effect on pollen development and pollen tube growth in cucumber.

Keywords

Hexose transporter Cucumber Male flower Pollen Pollen tubes 

Abbreviations

HT

Hexose transport protein

STP

Sucrose transport protein

SWEETs

Sugars will eventually be exported transports

SUC/SUT

Sucrose transport protein

CWINV

Cell wall invertases

VIN

Vacuolar invertase

SuSy

Sucrose synthase

Glc

Glucose

Fru

Fructose

Suc

Sucrose

Man

Mannose

Mat

Mannitol

HXK

Hexokinase

Gal

Galactose

Man

Mannose

GUS

β-Glucuronidase

Notes

Acknowledgements

We thank Fareeha Shireen for helpful discussions. This work was supported by the National Key Research and Development Program of China (2019YFD1000300) to Jintao Cheng, the National Natural Science Foundation of China (31972435 and 31601774) to Jintao Cheng and the Fundamental Research Funds for the Central Universities (2662018QD062) to Jintao Cheng.

Authors contributions

JTC designed research. JTC and ZLB found the experiments. SYW, TYB and XWZ conducted experiments. SYW analyzed data and wrote the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10725_2020_573_MOESM1_ESM.tif (1.6 mb)
Supplementary Fig. S1. Membrane-spanning model of CsHT11 by TMHMM. (TIF 1653 kb)
10725_2020_573_MOESM2_ESM.tif (6.4 mb)
Supplementary Fig. S2 Comparison of CsHT11 amino acid sequences. The protein sequence of CsHT11 is compared with protein sequences of previously-characterized pollen-specific monosaccharide transporters CsHT1, AtSTP2, 4, 6, 9 ,10, and AtSTP11 from Arabidopsis. Black boxes indicate identical amino acid residues. Dark gray boxes represent amino acid residues with identity of more than 50%. Light gray boxes represent similarity of more than 50%. Black bars indicate transmembrane domains of CsHT11 predicted by SOAP program in PCgene. The sequence alignment was performed using DNAMAN software package. The GenBank accession numbers of the sequences used for the analyses, as shown in Supplementary Table S1. (TIF 6536 kb)
10725_2020_573_MOESM3_ESM.tif (371 kb)
Supplementary Fig. S3. Spatiotemporal expression analysis of CsHT11 in different cucumber tissues. RPKM: normalized reads per million sequences. Project: PRINA80169. Data from the database of cucurbitgenomics (http://cucurbitgenomics.org/) (TIF 370 kb)
10725_2020_573_MOESM4_ESM.pdf (370 kb)
Supplementary Table S1. The GenBank accession numbers of the sequences used for the analysis in Fig. 1. (PDF 369 kb)
10725_2020_573_MOESM5_ESM.pdf (459 kb)
Supplementary Table S2. Primers used in the paper. The restriction enzyme sites or recombination connector sequence are underlined. (PDF 459 kb)
10725_2020_573_MOESM6_ESM.pdf (545 kb)
Supplementary Table S3. Potential cis-acting regulatory elements identified in promoter regions of CsHT11 genes. (PDF 544 kb)

References

  1. Bai S, Peng Y, Cui J, Gu H, Xu L, Li Y, Xu Z, Bai S (2004) Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber. Planta 220(2):230–240PubMedCrossRefGoogle Scholar
  2. Büttner M (2007) The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett 581(12):2318–2324PubMedCrossRefGoogle Scholar
  3. Büttner M (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biol 12:35–41PubMedCrossRefGoogle Scholar
  4. Büttner M, Truernit E, Baier K, Scholzstarke J, Sontheim M, Lauterbach C, Huss VAR, Sauer N (2000) AtSTP3, a green leaf-specific, low affinity monosaccharide-H+ symporter of Arabidopsis thaliana. Plant Cell Environ 23(2):175–184CrossRefGoogle Scholar
  5. Chardon F, Bedu M, Calenge F, Klemens PAW, Spinner L, Clement G, Chietera G, Leran S, Ferrand M, Lacombe B (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23(8):697–702PubMedCrossRefGoogle Scholar
  6. Cheng J, Li X, Yao F, Shan N, Li Y, Zhang Z, Sui X (2015a) Functional characterization and expression analysis of cucumber (Cucumis sativus L.) hexose transporters, involving carbohydrate partitioning and phloem unloading in sink tissues. Plant Sci 237:46–56PubMedCrossRefGoogle Scholar
  7. Cheng J, Wang Z, Yao F, Gao L, Ma S, Sui X, Zhang Z (2015b) Down-regulating CsHT1, a cucumber pollen-specific hexose transporter, inhibits pollen germination, tube growth and seed development. Plant Physiol 168(2):635–647PubMedPubMedCentralCrossRefGoogle Scholar
  8. Cheng J, Wen S, Xiao S, Lu B, Ma M, Bie Z (2018) Overexpression of the tonoplast sugar transporter CmTST2 in melon fruit increases sugar accumulation. J Exp Bot 69(3):511–523PubMedCrossRefGoogle Scholar
  9. Chung P, Hsiao H-H, Chen H-J, Chang C-W, Wang S-J (2014) Influence of temperature on the expression of the rice sucrose transporter 4 gene, OsSUT4, in germinating embryos and maturing pollen. Acta Physiol Plant 36(1):217–229CrossRefGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cordoba E, Aceveszamudio DL, Hernandezbernal AF, Ramosvega M, Leon P (2015) Sugar regulation of SUGAR TRANSPORTER PROTEIN 1 (STP1) expression in Arabidopsis thaliana. J Exp Bot 66(1):147–159PubMedCrossRefPubMedCentralGoogle Scholar
  12. Dewitt ND, Harper JF, Sussman MR (1991) Evidence for a plasma membrane proton pump in phloem cells of higher plants. Plant J 1(1):121–128PubMedCrossRefPubMedCentralGoogle Scholar
  13. Fan R, Peng C, Xu Y, Wang X, Li Y, Shang Y, Du S, Zhao R, Zhang X, Zhang L (2009) Apple sucrose transporter SUT1 and sorbitol transporter SOT6 interact with cytochrome b5 to regulate their affinity for substrate sugars. Plant Physiol 150(4):1880–1901PubMedPubMedCentralCrossRefGoogle Scholar
  14. Faure J, Rotman N, Fortune P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30(4):481–488PubMedCrossRefGoogle Scholar
  15. Gear ML, Mcphillips M, Patrick JW, Mccurdy DW (2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Mol Biol 44(5):687–697PubMedCrossRefGoogle Scholar
  16. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8(1):93–102PubMedCrossRefGoogle Scholar
  17. Goetz M, Godt DE, Guivarch A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98(11):6522–6527PubMedCrossRefGoogle Scholar
  18. 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(2):852–863PubMedPubMedCentralCrossRefGoogle Scholar
  19. Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kuhn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45(2):180–192PubMedCrossRefGoogle Scholar
  20. Hanson J, Smeekens S (2009) Sugar perception and signaling-an update. Curr Opin Plant Biol 12(5):562–567PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hayes MA, Davies C, Dry IB (2007) Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential roles in sink and source tissues. J Exp Bot 58(8):1985–1997PubMedCrossRefPubMedCentralGoogle Scholar
  22. He Z, Zhang H, Gao S, Lercher MJ, Chen W-H, Hu S (2016) Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res 44(W1):W236–W241PubMedPubMedCentralCrossRefGoogle Scholar
  23. Hirose T, Zhang Z, Miyao A, Hirochika H, Ohsugi R, Terao T (2010) Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. J Exp Bot 61(13):3639–3646PubMedPubMedCentralCrossRefGoogle Scholar
  24. Hirsche J, Fernandez JMG, Stabentheiner E, Groskinsky DK, Roitsch T (2017) Differential effects of carbohydrates on Arabidopsis pollen germination. Plant Cell Physiol 58(4):691–701PubMedCrossRefPubMedCentralGoogle Scholar
  25. Holsters M, Silva B, Van Vliet F, Genetello C, De Block M, Dhaese PC, Depicker A, Inze D, Engler G, Villarroel R (1980) The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 3(2):212–230PubMedCrossRefPubMedCentralGoogle Scholar
  26. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907PubMedPubMedCentralCrossRefGoogle Scholar
  27. Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198(2):453–465PubMedCrossRefPubMedCentralGoogle Scholar
  28. Kim KI, Sunter G, Bisaro DM, Chung I (2007) Improved expression of recombinant GFP using a replicating vector based on Beet curly top virus in leaf-disks and infiltrated Nicotiana benthamiana leaves. Plant Mol Biol 64:103–112PubMedCrossRefPubMedCentralGoogle Scholar
  29. Klemens PAW, Patzke K, Deitmer JW, Spinner L, Hir RL, 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):1338–1352PubMedPubMedCentralCrossRefGoogle Scholar
  30. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Biol 47(1):509–540CrossRefGoogle Scholar
  31. Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11(4):707–726PubMedPubMedCentralCrossRefGoogle Scholar
  32. Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochem Biophys Acta 1465(1):246–262PubMedCrossRefGoogle Scholar
  33. Lemoine R, Burkle L, Barker L, Sakr S, Kuhn C, Regnacq M, Gaillard C, Delrot S, Frommer WB (1999) Identification of a pollen-specific sucrose transporter-like protein NtSUT3 from tobacco. FEBS Lett 454(3):325–330PubMedCrossRefGoogle Scholar
  34. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, De Peer YV, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327PubMedPubMedCentralCrossRefGoogle Scholar
  35. Li Y, Feng S, Ma S, Sui X, Zhang Z (2017) Spatiotemporal expression and substrate specificity analysis of the cucumber SWEET gene family. Front Plant Sci 8:1855PubMedPubMedCentralCrossRefGoogle Scholar
  36. Li-Ping HU, Feng Z, Shu-Hui S, Xiao-Wei T, Hui XU, Guang-Min L, Ya-Qin W, Hong-Ju HE (2017) Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. J Integr Agric 16(7):1486–1501CrossRefGoogle Scholar
  37. Li-Qing C, Xiao-Qing Q, Bi-Huei H, Davide S, Sonia O, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335(6065):207CrossRefGoogle Scholar
  38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408CrossRefGoogle Scholar
  39. Loreti E, De Bellis L, Alpi A, Perata P (2001) Why and how do plant cells sense sugars? Ann Bot 88(5):803–812CrossRefGoogle Scholar
  40. Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004) Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. Plant Physiol 134(2):684–693PubMedPubMedCentralCrossRefGoogle Scholar
  41. Morita T, Takegawa K (2004) A simple and efficient procedure for transformation of Schizosaccharomyces pombe. Yeast 21(8):613–617PubMedCrossRefGoogle Scholar
  42. Ngampanya B, Sobolewska A, Takeda T, Toyofuku K, Narangajavana J, Ikeda A, Yamaguchi J (2003) Characterization of rice functional monosaccharide transporter, OsMST5. Biosci Biotechnol Biochem 67(3):556–562PubMedCrossRefGoogle Scholar
  43. Norholm MHH, Noureldin HH, Brodersen P, Mundy J, Halkier BA (2006) Expression of the Arabidopsis high-affinity hexose transporter STP13 correlates with programmed cell death. FEBS Lett 580(9):2381–2387PubMedCrossRefGoogle Scholar
  44. Poschet G, Hannich B, Büttner M (2010) Identification and characterization of AtSTP14, a novel galactose transporter from Arabidopsis. Plant Cell Physiol 51(9):1571–1580PubMedCrossRefGoogle Scholar
  45. Price JW, Laxmi A, Martin SKS, Jang J (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16(8):2128–2150PubMedPubMedCentralCrossRefGoogle Scholar
  46. Qin Y, Leydon AR, Manziello A, Pandey R, Mount DB, Denic SZ, Vasic BV, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5(8):e1000621PubMedPubMedCentralCrossRefGoogle Scholar
  47. Reinders A (2016) Fuel for the road—sugar transport and pollen tube growth. J Exp Bot 67(8):2121–2123PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ren Y, Guo S, Zhang J, He H, Sun H, Tian S, Gong G, Zhang H, Levi A, Tadmor Y, Xu Y (2018) A tonoplast sugar transporter underlies a sugar accumulation QTL in watermelon. Plant Physiol 176(1):836–850PubMedCrossRefGoogle Scholar
  49. Rodriguez-Enriquez MJ, Mehdi S, Dickinson HG, Grant-Downton RT (2013) A novel method for efficient in vitro germination and tube growth of Arabidopsis thaliana pollen. New Phytol 197(2):668–679PubMedCrossRefGoogle Scholar
  50. Rottmann TM, Zierer W, Subert C, Sauer N, Stadler R (2016) STP10 encodes a high-affinity monosaccharide transporter and is induced under low-glucose conditions in pollen tubes of Arabidopsis. J Exp Bot 67(8):2387–2399PubMedPubMedCentralCrossRefGoogle Scholar
  51. Rottmann TM, Fritz C, Sauer N, Stadler R (2018a) Glucose uptake via STP transporters inhibits in vitro pollen tube growth in a HEXOKINASE1-dependent manner in Arabidopsis thaliana. Plant Cell 30(9):2057–2081PubMedPubMedCentralCrossRefGoogle Scholar
  52. Rottmann TM, Klebl F, Schneider S, Kischka D, Ruscher D, Sauer N, Stadler R (2018b) Sugar transporter STP7 specificity for L-arabinose and D-xylose contrasts with the typical hexose transporters STP8 and STP12. Plant Physiol 176(3):2330–2350PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ruan Y (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65(1):33–67PubMedPubMedCentralCrossRefGoogle Scholar
  54. Schneidereit A, Scholzstarke J, Büttner M (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiol 133(1):182–190PubMedPubMedCentralCrossRefGoogle Scholar
  55. Schneidereit A, Scholzstarke J, Sauer N, Büttner M (2005) AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis. Planta 221(1):48–55PubMedCrossRefPubMedCentralGoogle Scholar
  56. Schofield RA, Bi Y, Kant S, Rothstein SJ (2009) Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant Cell Environ 32(3):271–285PubMedCrossRefPubMedCentralGoogle Scholar
  57. Scholzstarke J, Büttner M, Sauer N (2003) AtSTP6, a new nollen-specific H+-monosaccharide symporter from Arabidopsis. Plant Physiol 131(1):70–77CrossRefGoogle Scholar
  58. Sheen J, Zhou L, Jang J (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2(5):410–418PubMedCrossRefPubMedCentralGoogle Scholar
  59. Sherson SM, Hemmann G, Wallace G, Forbes S, Germain V, Stadler R, Bechtold N, Sauer N, Smith SM (2000) Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J 24(6):849–857PubMedCrossRefGoogle Scholar
  60. Sivitz AB, Reinders A, Ward JM (2008) Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiol 147(1):92–100PubMedPubMedCentralCrossRefGoogle Scholar
  61. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13(3):274–279PubMedCrossRefPubMedCentralGoogle Scholar
  62. Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. Plant J 19(3):269–278PubMedCrossRefPubMedCentralGoogle Scholar
  63. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121(1):1–8PubMedPubMedCentralCrossRefGoogle Scholar
  64. Sun M, Huang X, Yang J, Guan Y, Yang Z (2013) Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Sex Plant Reprod 26(2):83–91CrossRefGoogle Scholar
  65. Sussman MR (1994) Molecular analysis of proteins in the plant plasma membrane. Annu Rev Plant Biol 45(1):211–234CrossRefGoogle Scholar
  66. Tamura K, Stecher G, Peterson DS, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis Version 6.0. Mol Biol Evol 30(12):2725–2729PubMedPubMedCentralCrossRefGoogle Scholar
  67. Tian L, Liu H, Ren L, Ku L, Wu L, Li M, Wang S, Zhou J, Song X, Zhang J (2018) MicroRNA 399 as a potential integrator of photo-response, phosphate homeostasis, and sucrose signaling under long day condition. BMC Plant Biol 18(1):290PubMedPubMedCentralCrossRefGoogle Scholar
  68. Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8(12):2169–2182PubMedPubMedCentralGoogle Scholar
  69. Truernit E, Stadler R, Baier K, Sauer N (1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J 17(2):191–201PubMedCrossRefPubMedCentralGoogle Scholar
  70. Wang Y, Zhang W, Song L, Zou J, Su Z, Wu W (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148(3):1201–1211PubMedPubMedCentralCrossRefGoogle Scholar
  71. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, 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(3):123–128PubMedCrossRefGoogle Scholar
  72. Wilhelmi LK, Preuss D (1996) Self-sterility in Arabidopsis due to defective pollen tube guidance. Science 274(5292):1535–1537PubMedCrossRefPubMedCentralGoogle Scholar
  73. Wind JJ, Smeekens S, Hanson J (2010) Sucrose: Metabolite and signaling molecule. Phytochemistry 71(14):1610–1614PubMedCrossRefPubMedCentralGoogle Scholar
  74. Ylstra B, Garrido D, Busscher J, Van Tunen AJ (1998) Hexose transport in growing petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter. Plant Physiol 118(1):297–304PubMedPubMedCentralCrossRefGoogle Scholar
  75. Zanor MI, Osorio S, Nunesnesi A, Carrari F, Lohse M, Usadel B, Kuhn C, Bleiss W, Giavalisco P, Willmitzer L (2009) RNA interference of LIN5 in Solanum lycopersicum confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol 150(3):1204–1218PubMedPubMedCentralCrossRefGoogle Scholar
  76. Zhang X, Wang X, Wang X, Xia G, Pan Q, Fan R, Wu F, Yu X, Zhang D (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142(1):220–232PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature B.V. 2020

Authors and Affiliations

  1. 1.College of Horticulture and Forestry Sciences, Huazhong Agricultural University and Key Laboratory of Horticultural Plant BiologyMinistry of EducationWuhanPeople’s Republic of China

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