Plant Cell Reports

, Volume 33, Issue 2, pp 337–347 | Cite as

The role of hexokinases from grape berries (Vitis vinifera L.) in regulating the expression of cell wall invertase and sucrose synthase genes

  • X. Q. Wang
  • L. M. Li
  • P. P. Yang
  • C. L. Gong
Original Paper


Key message

The activity and content of hexokinases (HXKs) had an inverse relationship with glucose and/or fructose levels during grape berry development. HXK subcellular localization was investigated in grape berry.


In plants, hexokinase (HXK, EC involved in hexose phosphorylation, plays an important role in sugar sensing and signaling. In this study, we found that at Phase I of grape berry development, lower hexose (glucose or fructose) levels were concomitant with higher HXK activities and protein levels. After the onset of ripening, we demonstrated a drastic reduction in HXK activity and protein levels accompanied by a rising hexose level. Therefore, our results revealed that HXK activity and protein levels had an inverse relationship with the endogenous glucose or fructose levels during grape berry development. A 51 kDa HXK protein band was detected throughout grape berry development. In addition, HXK located in the vacuoles, cytoplasm, nucleus, proplastid, chloroplast, and mitochondrion of the berry flesh cells. During grape berry development, HXK transcriptional level changed slightly, while cell wall invertase (CWINV) and sucrose synthase (SuSy) expression was enhanced after véraison stage. Intriguingly, when sliced grape berries were incubated in different glucose solutions, CWINV and SuSy expression was repressed by glucose, and the intensity of repression depended on glucose concentration and incubation time. After sliced, grape berries were treated with different glucose analogs, CWINV and SuSy expression analyses revealed that phosphorylation of hexoses by hexokinase was an essential component in the glucose-dependent CWINV and SuSy expression. In the meantime, mannoheptulose, a specific inhibitor of hexokinase, blocked the repression induced by glucose on CWINV and SuSy expression. It suggested that HXK played a major role in regulating CWINV and SuSy expression during grape berry development.


Cell wall invertase Hexokinase Grape berry Sucrose synthase Sugar 



Cell wall invertase


Day after full bloom








Parenchyma cells




Sucrose synthase



The authors are most grateful to Prof. Sheen J. (Harvard Medical School Department of Molecular Biology, 185 Cambridge St., CPZN7624E, Massachusetts General Hospital, Boston, MA, 02114, USA) for her providing us HXK polyclonal antibody. This research was supported by the National Natural Science Foundation of China (Grant Nos. 30871698, 31372036, and 31071764).

Conflict of interest

The authors declare no conflict of interest.


  1. Arroyo A, Bossi F, Finkelstein RR, León P (2003) Three genes that affect sugar sensing are differentially regulated by glucose in Arabidopsis. Plant Physiol 133:231–242PubMedCentralPubMedCrossRefGoogle Scholar
  2. Barkla BJ, Vera-Estrella R, Herna′ndez-Coronado M, Pantoja O (2009) Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell 21:4044–4058PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bolouri-Moghaddam MR, Roy KL, Xiang L, Rolland F, Ende WV (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037PubMedCrossRefGoogle Scholar
  4. Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in sucrose signaling. Cell 127:579–589PubMedCrossRefGoogle Scholar
  5. Copeland L, Morelli M (1985) Hexose kinases from the plant cytosolic fraction of soybean nodules. Plant Physiol 79:114–117PubMedCentralPubMedCrossRefGoogle Scholar
  6. D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and sucrose unloading capacity of young fruit. Plant Cell 11:2407–2418PubMedCentralPubMedGoogle Scholar
  7. Damari-Weissler H, Ginzburg A, Gidoni D et al (2007) Spinach SoHXK1 is a mitochondria-associated hexokinase. Planta 226:1053–1058PubMedCrossRefGoogle Scholar
  8. da-Silva WS, Rezende GL, Galina A (2001) Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation. J Exp Bot 52:1191–1201PubMedCrossRefGoogle Scholar
  9. Germain V, Ricard B, Raymond P, Saglio PH (1997) The role of sugars, hexokinase, and sucrose synthase in the determination of hypoxically induced tolerance to anoxia in tomato roots. Plant Physiol 114:167–175PubMedCentralPubMedGoogle Scholar
  10. Giese JO, Herbers K, Hoffmann M, Klösgen RB, Sonnewald U (2005) Isolation and functional characterization of a novel plastidic hexokinase from Nicotiana tabacum. FEBS Lett 579:827–831PubMedCrossRefGoogle Scholar
  11. Graham JWA, Williams TCR, Morgan M et al (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19:3723–3738PubMedCentralPubMedCrossRefGoogle Scholar
  12. Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Plant Physiol. doi: 10.3389/fpls.2013.00044 Google Scholar
  13. Hanson J, Smeekens S (2009) Sugar perception and signaling. Curr Opin Plant Biol 12:562–567PubMedCrossRefGoogle Scholar
  14. Hayes MA, Feechan A, Dry IB (2010) Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiol 153:211–221PubMedCentralPubMedCrossRefGoogle Scholar
  15. Jaquinod M, Villiers F, Kieffer-Jaquinod S et al (2007) Proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol Cell Proteomics 6:394–412PubMedCentralPubMedCrossRefGoogle Scholar
  16. Kim WM, Lim JH, Ahn CS et al (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18:2341–2355PubMedCentralPubMedCrossRefGoogle Scholar
  17. Kim YM, Heinzel N, Giese JO, Koeber J, Melzer M et al (2013) A dual role of tobacco hexokinase1 in primary metabolism and sugar sensing. Plant Cell Environ 36:1311–1327CrossRefGoogle Scholar
  18. Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefGoogle Scholar
  19. Moore B, Zhou L, Rolland F et al (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300:332–336PubMedCrossRefGoogle Scholar
  20. Oesterhelt C, Gross W (2002) Different sugar kinases are involved in the sugar sensing of Galdieria sulphuraria. Plant Physiol 128:291–299PubMedCentralPubMedCrossRefGoogle Scholar
  21. Olsson T, Thelander M, Ronne H (2003) A nowel type of chloroplast stromal hexokinase is the major glucosephosphorylating enzyme in the moss Physcomitrella patens. J Biol Chem 278:44439–44447PubMedCrossRefGoogle Scholar
  22. Polita JT, Ciereszko I (2009) In situ activities of hexokinase and fructokinase in relation to phosphorylation status of root meristem cells of Vicia faba during reactivation from sugar starvation. Physiol Plant 135:342–350CrossRefGoogle Scholar
  23. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14(Suppl):S185–S205PubMedCentralPubMedGoogle Scholar
  24. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  25. Sinha AK, Hofmann MG, Römer U et al (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128:1480–1489PubMedCentralPubMedCrossRefGoogle Scholar
  26. Stettler M, Eicke S, Mettler T et al (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2:1233–1246PubMedCrossRefGoogle Scholar
  27. Wang XQ, Huang WD, Zhan JC (2005) Effects of weak light on the sucrose synthase in source leaves of nectarine trees (Prunus persica L. var. nectarine Ait.). J Hortic Sci Biotech 80:356–362Google Scholar
  28. Wen PF, Chen JY, Kong WF, Wan SB, Huang WD (2005) Salicylic acid induced the expression of phenylalanine ammonialyase gene in grape berry. Plant Sci 169:928–934CrossRefGoogle Scholar
  29. Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525PubMedCrossRefGoogle Scholar
  30. Yima HK, Lima MN, Leea SE, Lima J, Leeb Y, Hwanga YS (2012) Hexokinase-mediated sugar signaling controls expression of the calcineurin B-like interacting protein kinase 15 gene and is perturbed by oxidative phosphorylation inhibition. J Plant Physiol 169:1551–1558CrossRefGoogle Scholar
  31. Zhang XY, Wang XL, Wang XF et al (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • X. Q. Wang
    • 1
  • L. M. Li
    • 1
  • P. P. Yang
    • 1
  • C. L. Gong
    • 1
  1. 1.College of Food Science and Nutritional EngineeringChina Agricultural UniversityBeijingChina

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