Role of tomato hexose kinases
David GranotA Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel. Email: granot@agri.gov.il
B This paper originates from a presentation at the 8th International Congress of Plant Molecular Biology, Adelaide, Australia, August 2006.
Functional Plant Biology 34(6) 564-570 https://doi.org/10.1071/FP06207
Submitted: 11 September 2006 Accepted: 10 November 2006 Published: 1 June 2007
Abstract
Hexose phosphorylation is an essential step of sugar metabolism. Only two classes of glucose and fructose phosphorylating enzymes, hexokinases (HXK) and fructokinases (FRK), have been found in plants. Tomato (Lycopersicon esculentum Mill.) is the only plant species from which four HXK and four FRK genes have been identified and characterised. One HXK and one FRK isozyme are located within plastids. The other three HXK isozymes are associated with the mitochondria, and the other three FRK isozymes are dispersed in the cytosol. These differences in location suggest that the cytoplasmic HXK and FRK have distinct roles to play in sugar metabolism. The specific roles of each of the HXK and FRK genes have been investigated using transgenic plants with modified expression of the genes. Sugar signalling effects were obtained with modified expression of the mitochondria associated HXK. In contrast, modified expression of the cytosolic FRK affected fructose metabolism rather than sugar signalling. Future research efforts will aim to determining the roles of specific hexose phosphorylating enzymes in tomato plants, the source of the hexose monomers to be phosphorylated, and their intracellular trafficking route.
Additional keywords: fructokinase, green fluorescent protein, hexokinase, hexose phosphorylation, intracellular localisation, Lycopersicon esculentum.
Acknowledgements
This research was supported by The Israel Science Foundation grant No. 890/06 and by research grants No. IS-3897–06 and CA-9100–06 from BARD, the United States–Israel Binational Agricultural Research and Development Fund.
al-Habori M
(1995) Microcompartmentation, metabolic channeling and carbohydrate metabolism. The International Journal of Biochemistry and Cell Biology 27, 123–132.
| Crossref | GoogleScholarGoogle Scholar |
Dai N,
German MA,
Matsevitz T,
Hanael R,
Swartzberg D,
Yeselson Y,
Petreikov M,
Schaffer AA, Granot D
(2002a) LeFRK2, a gene encoding the major fructokinase in tomato fruits, is not required for starch accumulation in developing fruits. Plant Science 162, 423–430.
| Crossref | GoogleScholarGoogle Scholar |
Dai N,
Kandel M,
Petreikov M,
Levine I,
Ricard B,
Rothan C,
Schaffer AA, Granot D
(2002b) The tomato hexokinase LeHXK1: cloning, mapping, expression pattern and phylogenetic relationships. Plant Science 163, 581–590.
| Crossref | GoogleScholarGoogle Scholar |
Dai N,
Schaffer A,
Petreikov M, Granot D
(1997) Potato (Solanum tuberosum L.) fructokinase expressed in yeast exhibits inhibition by fructose of both in vitro enzyme activity and rate of cell proliferation. Plant Science 128, 191–197.
| Crossref | GoogleScholarGoogle Scholar |
Dai N,
Schaffer A,
Petreikov M,
Shahak Y,
Giller Y,
Ratner K,
Levine A, Granot D
(1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. The Plant Cell 11, 1253–1266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Damari-Weissler H,
Kfir MK,
Gidoni D,
Mett A,
Belausov E, Granot D
(2006) Evidence for intracellular spatial separation of hexokinases and fructokinases in tomato plants. Planta In press ,
Davies HV,
Shepherd LV,
Burrell MM,
Carrari F, Urbanczyk-Wochniak E , et al.
(2005) Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. Plant and Cell Physiology 46, 1103–1115.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delmer DP, Haigler CH
(2002) The regulation of metabolic flux to cellulose, a major sink for carbon in plants. Metabolic Engineering 4, 22–28.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Deuschle K,
Chaudhuri B,
Okumoto S,
Lager I,
Lalonde S, Frommer WB
(2006) Rapid metabolism of glucose detected with FRET glucose nanosensors in epidermal cells and intact roots of Arabidopsis RNA-silencing mutants. The Plant Cell 18, 2314–2325.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eshed Y,
Abu Abied M,
Saranga Y, Zamir D
(1992) Lycopersicon esculentum lines containing small overlapping introgressions from L. pennellii. Theoretical and Applied Genetics 83, 1027–1034.
| Crossref | GoogleScholarGoogle Scholar |
Eshed Y, Zamir D
(1994a) A genomic library of Lycopersicon pennellii in L. esculentum: a tool for fine mapping of genes. Euphytica 79, 175–179.
| Crossref | GoogleScholarGoogle Scholar |
Eshed Y, Zamir D
(1994b) Introgressions from Lycopersicon pennellii can improve the soluble-solids yield of tomato hybrids. Theoretical and Applied Genetics 88, 891–897.
| Crossref | GoogleScholarGoogle Scholar |
Fu H, Park WD
(1995) Sink- and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. The Plant Cell 7, 1369–1385.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Geigenberger P,
Langenberger S,
Wilke I,
Heineke D,
Heldt HW, Stitt M
(1993) Sucrose is metabolised by sucrose synthase and glycolysis within the phloem complex of Ricinis communis L. seedlings. Planta 190, 446–453.
| Crossref | GoogleScholarGoogle Scholar |
German MA,
Asher I,
Petreikov M,
Dai N,
Schaffer AA, Granot D
(2004) Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Science 166, 285–291.
| Crossref | GoogleScholarGoogle Scholar |
German MA,
Dai N,
Chmelnitsky I,
Sobolev I,
Salts Y,
Barg R,
Schaffer AA, Granot D
(2002) LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. Plant Science 163, 607–613.
| Crossref | GoogleScholarGoogle Scholar |
German MA,
Dai N,
Matsevitz T,
Hanael R,
Petreikov M,
Bernstein N,
Ioffe M,
Shahak Y,
Schaffer AA, Granot D
(2003) Suppression of fructokinase encoded by LeFRK2 in tomato stem inhibits growth and causes wilting of young leaves. The Plant Journal 34, 837–846.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Giege P,
Heazlewood JL,
Roessner-Tunali U,
Millar AH,
Fernie AR,
Leaver CJ, Sweetlove LJ
(2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. The Plant Cell 15, 2140–2151.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gonzali S,
Pistelli L,
De Bellis L, Alpi A
(2001) Characterization of two Arabidopsis thaliana fructokinases. Plant Science 160, 1107–1114.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Granot D, Dai N
(1997) Sugar induced cell death in yeast is dependent on the rate of sugar phosphorylation as determined by Arabidopsis thaliana hexokinase. Cell Death and Differentiation 4, 555–559.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Granot D,
Levine A, Dor-Hefetz E
(2003) Sugar-induced apoptosis in yeast cells. FEMS Yeast Research 4, 7–13.
| Crossref |
PubMed |
Jang JC, Sheen J
(1994) Sugar sensing in higher plants. The Plant Cell 6, 1665–1679.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jang JC,
Leon P,
Zhou L, Sheen J
(1997) Hexokinase as a sugar sensor in higher plants. The Plant Cell 9, 5–19.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jiang H,
Dian W,
Liu F, Wu P
(2003) Isolation and characterization of two fructokinase cDNA clones from rice. Phytochemistry 62, 47–52.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kanayama Y,
Dai N,
Granot D,
Petreikov M,
Schaffer A, Bennett AB
(1997) Divergent fructokinase genes are differentially expressed in tomato. Plant Physiology 113, 1379–1384.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kanayama Y,
Granot D,
Dai N,
Petreikov M,
Schaffer A,
Powell A, Bennett AB
(1998) Tomato fructokinases exhibit differential expression and substrate regulation. Plant Physiology 117, 85–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kandel-Kfir M,
Damari-Weissler H,
German MA,
Gidoni D,
Mett A,
Belausov E,
Petreikov M,
Adir N, Granot D
(2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta 224, 1341–1352.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim M,
Lim JH,
Ahn CS,
Park K,
Kim GT,
Kim WT, Pai HS
(2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. The Plant Cell 18, 2341–2355.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Menu T,
Rothan C,
Dai N,
Petreikov M,
Etienne C,
Destrac-Irvine A,
Schaffer A,
Granot D, Ricard B
(2001) Cloning and characterization of a cDNA encoding hexokinase from tomato. Plant Science 160, 209–218.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moore B,
Zhou L,
Rolland F,
Hall Q,
Cheng WH,
Liu YX,
Hwang I,
Jones T, Sheen J
(2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nakashima RA,
Mangan PS,
Colombini M, Pedersen PL
(1986) Hexokinase receptor complex in hepatoma mitochondria: evidence from N,N’-dicyclohexylcarbodiimide-labeling studies for the involvement of the pore-forming protein VDAC. Biochemistry 25, 1015–1021.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niittyla T,
Messerli G,
Trevisan M,
Chen J,
Smith AM, Zeeman SC
(2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303, 87–89.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Odanaka S,
Bennett AB, Kanayama Y
(2002) Distinct physiological roles of fructokinase isozymes revealed by gene-specific suppression of frk1 and frk2 expression in tomato. Plant Physiology 129, 1119–1126.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Olsson T,
Thelander M, Ronne H
(2003) A novel type of chloroplast stromal hexokinase is the major glucose-phosphorylating enzyme in the moss Physcomitrella patens. Journal of Biological Chemistry 278, 44439–44447.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ovadi J, Saks V
(2004) On the origin of intracellular compartmentation and organized metabolic systems. Molecular and Cellular Biochemistry 256–257, 5–12.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pego JV, Smeekens SC
(2000) Plant fructokinases: a sweet family get-together. Trends in Plant Science 5, 531–536.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Petreikov M,
Dai N,
Granot D, Schaffer AA
(2001) Characterization of native and yeast-expressed tomato fruit fructokinase enzymes. Phytochemistry 58, 841–847.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pourtau N,
Jennings R,
Pelzer E,
Pallas J, Wingler A
(2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224, 556–558.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Renz A, Stitt M
(1993) Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta 190, 166–175.
Rezende GL,
Logullo C,
Meyer L,
Machado LB,
Oliveira-Carvalho AL,
Zingali RB,
Cifuentes D, Galina A
(2006) Partial purification of tightly bound mitochondrial hexokinase from maize (Zea mays L.) root membranes. Brazilian Journal of Medical and Biological Research 39, 1159–1169.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rolland F, Sheen J
(2005) Sugar sensing and signalling networks in plants. Biochemical Society Transactions 33, 269–271.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schaffer AA, Petreikov M
(1997a) Inhibition of fructokinase and sucrose synthase by cytosolic levels of fructose in young tomato fruit undergoing transient starch synthesis. Physiologia Plantarum 101, 800–806.
| Crossref | GoogleScholarGoogle Scholar |
Schaffer AA, Petreikov M
(1997b) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiology 113, 739–746.
| PubMed |
Schnarrenberger C
(1990) Characterization and compartmentation in green leaves, of hexokinases with different specificities for glucose, fructose, and mannose and for nucleoside triphosphates. Planta 181, 249–255.
| Crossref | GoogleScholarGoogle Scholar |
Singh KK,
Chen C,
Epstein DK, Gibbs M
(1993) Respiration of sugars in spinach (Spinacia oleracea), maize (Zea mays), and Chlamydomonas reinhardtii F-60 chloroplasts with emphasis on the hexose kinases. Plant Physiology 102, 587–593.
| PubMed |
Taylor MA,
Ross HA,
Gardner A, Davies HV
(1995) Characterization of a cDNA encoding fructokinase from potato (Solanum tuberosum L.). Journal of Plant Physiology 145, 253–256.
Tiessen A,
Prescha K,
Branscheid A,
Palacios N,
McKibbin R,
Halford NG, Geigenberger P
(2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. The Plant Journal 35, 490–500.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Veramendi J,
Fernie AR,
Leisse A,
Willmitzer L, Trethewey RN
(2002) Potato hexokinase 2 complements transgenic Arabidopsis plants deficient in hexokinase 1 but does not play a key role in tuber carbohydrate metabolism. Plant Molecular Biology 49, 491–501.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Veramendi J,
Roessner U,
Renz A,
Willmitzer L, Trethewey RN
(1999) Antisense repression of hexokinase 1 leads to an overaccumulation of starch in leaves of transgenic potato plants but not to significant changes in tuber carbohydrate metabolism. Plant Physiology 121, 123–134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wiese A,
Groner F,
Sonnewald U,
Deppner H,
Lerchl J,
Hebbeker U,
Flugge U, Weber A
(1999) Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Letters 461, 13–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weise SE,
Weber AP, Sharkey TD
(2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218, 474–482.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wilson JE
(1980) Brain hexokinase, the prototype ambiquitous enzyme. Current Topics in Cellular Regulation 16, 1–54.
| PubMed |
Xiao W,
Sheen J, Jang JC
(2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Molecular Biology 44, 451–461.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang NS, Russell D
(1990) Maize sucrose synthase-1 promoter directs phloem cell-specific expression of Gus gene in transgenic tobacco plants. Proceedings of the National Academy of Sciences USA 87, 4144–4148.
| Crossref | GoogleScholarGoogle Scholar |
Zhang S,
Nichols SE, Dong JG
(2003) Cloning and characterization of two fructokinases from maize. Plant Science 165, 1051–1058.
| Crossref | GoogleScholarGoogle Scholar |