Fructokinase is required for carbon partitioning to cellulose in aspen wood

Plant Journal

Volumn 70, Issue 6, 2012, Pages 967-977

  Roach, Melissa ^a   Gerber, Lorenz ^a   Sandquist, David ^a   Gorzsás, András ^a   Hedenström, Mattias ^b   Kumar, Manoj ^a   Steinhauser, Marie Caroline ^c   Feil, Regina ^c   Daniel, Geoffrey ^a   Stitt, Mark ^c   Sundberg, Björn ^a   Niittylä, Totte ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

aspen; carbon partitioning; cell wall; cellulose; fructokinase; fructose; Populus; sucrose

Indexed keywords

ASPEN; CARBON PARTITIONING; CELL WALLS; FRUCTOKINASE; POPULUS;

CARBON; CELLS; CELLULOSE; CYTOLOGY; FORESTRY; FRUCTOSE; GLUCOSE; METABOLISM; PHYSIOLOGY; SUGAR (SUCROSE);

WOOD;

CARBON; CELLULOSE; FRUCTOKINASE; ISOENZYME; SUCROSE; VEGETABLE PROTEIN;

ARTICLE; CARBOHYDRATE METABOLISM; CELL WALL; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; PLANT STEM; POPULUS; RNA INTERFERENCE; WOOD;

CARBOHYDRATE METABOLISM; CARBON; CELL WALL; CELLULOSE; FRUCTOKINASES; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; METABOLOME; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT PROTEINS; PLANT STEMS; POPULUS; RNA INTERFERENCE; SUCROSE; WOOD;

CARBON; CELLULOSE; FORESTRY; FRUCTOSE; GLUCOSE; METABOLISM; PHYSIOLOGY; POPULUS; SUCROSE; WOOD;

POPULUS; POPULUS TREMULA;

EID: 84862231642     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04929.x     Document Type: Article

References (71)

1. Amor, Y., Haigler, C.H., Johnson, S., Wainscott, M., and, Delmer, D.P., (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl Acad. Sci. USA, 92, 9353-9357.
2. Andersson-Gunnerås, S., Mellerowicz, E.J., Love, J., Segerman, B., Ohmiya, Y., Coutinho, P.M., Nilsson, P., Henrissat, B., Moritz, T., and, Sundberg, B., (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J. 45, 144-165. (Pubitemid 43382051)
3. Bonan, G.B., (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science, 320, 1444-1449. (Pubitemid 351929396)
4. Brown, D.M., Zeef, L.A., Ellis, J., Goodacre, R., and, Turner, S.R., (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell, 17, 2281-2295. (Pubitemid 41672947)
5. Chaffey, N., Cholewa, E., Regan, S., and, Sundberg, B., (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol. Plant, 114, 594-600. (Pubitemid 34463633)
6. Chen, H., Lai, Z., Shi, J., Xiao, Y., Chen, Z., and, Xu, X., (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol. 10, 281.
7. Coleman, H.D., Yan, J., and, Mansfield, S.D., (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc. Natl Acad. Sci. USA, 106, 13118-13123.
8. Currie, H.A., and, Perry, C.C., (2006) Resolution of complex monosaccharide mixtures from plant cell wall isolates by high pH anion exchange chromatography. J. Chromatogr. A, 1128, 90-96. (Pubitemid 44292737)
9. Dai, N., German, M.A., Matsevitz, T., Hanael, R., Swartzberg, D., Yeselson, Y., Petreikov, M., Schaffer, A.A., and, Granot, D., (2002) LeFRK2, the gene encoding the major fructokinase in tomato fruits, is not required for starch biosynthesis in developing fruits. Plant Sci. 162, 423-430.
10. Damari-Weissler, H., Kandel-Kfir, M., Gidoni, D., Mett, A., Belausov, E., and, Granot, D., (2006) Evidence for intracellular spatial separation of hexokinases and fructokinases in tomato plants. Planta, 224, 1495-1502. (Pubitemid 44769879)
11. Damari-Weissler, H., Rachamilevitch, S., Aloni, R., German, M.A., Cohen, S., Zwieniecki, M.A., Holbrook, N.M., and, Granot, D., (2009) LeFRK2 is required for phloem and xylem differentiation and the transport of both sugar and water. Planta, 230, 795-805.
12. Dauwe, R., Morreel, K., Goeminne, G., et al. (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J. 52, 263-285. (Pubitemid 47537580)
13. Davies, H.V., Shepherd, L.V.T., Burrell, M.M., et al. (2005) Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. Plant Cell Physiol. 46, 1103-1115. (Pubitemid 41373474)
14. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and, Zhen, S., (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70.
15. Duplessis, S., Major, I., Martin, F., and, Seguin, A., (2009) Poplar and pathogen interactions: insights from Populus genome-wide analyses of resistance and defense gene families and gene expression profiling. Crit. Rev. Plant Sci. 28, 309-334.
16. Faix, O., Fortmann, I., Bremer, J., and, Meier, D., (1991) Thermal-degradation products of wood-gas-chromatographic separation and mass-spectrometric characterization of polysaccharide derived products. Holz Roh Werkst. 49, 213-219.
17. Geigenberger, P., and, Stitt, M., (1993) Sucrose synthase catalyzes a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta, 189, 329-339.
18. Geigenberger, P., Langenberger, S., Wilke, I., Heineke, D., Heldt, H.W., and, Stitt, M., (1993) Sucrose is metabolized by sucrose synthase and glycolysis within the phloem complex of Ricinus communis L. seedlings. Planta, 190, 446-453.
19. German, M.A., Dai, N., Chmelnitsky, I., Sobolev, I., Salts, Y., Barg, R., Schaffer, A.A., and, Granot, D., (2002) LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. Plant Sci. 163, 607-613.
20. German, M.A., Dai, N., Matsevitz, T., Hanael, R., Petreikov, M., Bernstein, N., Ioffe, M., Shahak, Y., Schaffer, A.A., and, Granot, D., (2003) Suppression of fructokinase encoded by LeFRK2 in tomato stem inhibits growth and causes wilting of young leaves. Plant J. 34, 837-846. (Pubitemid 36796931)
21. German, M.A., Asher, I., Petreikov, M., Dai, N., Schaffer, A.A., and, Granot, D., (2004) Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Sci. 166, 285-291. (Pubitemid 38214919)
22. Gibon, Y., Vigeolas, H., Tiessen, A., Geigenberger, P., and, Stitt, M., (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. Plant J. 30, 221-235. (Pubitemid 34536242)
23. Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J.H.M., Palacios, N., Cross, J., Selbig, J., and, Stitt, M., (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell, 16, 3304-3325. (Pubitemid 41096008)
24. Gonzali, S., Pistelli, L., De Bellis, L., and, Alpi, A., (2001) Characterization of two Arabidopsis thaliana fructokinases. Plant Sci. 160, 1107-1114. (Pubitemid 32441206)
25. Gorzsás, A.S.H., Persson, P., Trygg, J., and, Sundberg, B., (2011) Cell-specific chemotyping and multivariate imaging by combined FT-IR microspectroscopy and orthogonal projections to latent structures (OPLS) analysis reveals the chemical landscape of secondary xylem. Plant J. 66, 903-914.
26. Granot, D., (2007) Role of tomato hexose kinases. Funct. Plant Biol. 34, 564-570. (Pubitemid 46869640)
27. Granot, D., (2008) Putting plant hexokinases in their proper place. Phytochemistry, 69, 2649-2654.
28. Gray-Mitsumune, M., Mellerowicz, E.J., Abe, H., Schrader, J., Winzell, A., Sterky, F., Blomqvist, K., McQueen-Mason, S., Teeri, T.T., and, Sundberg, B., (2004) Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiol. 135, 1552-1564. (Pubitemid 39009400)
29. Hamann, T., Bennett, M., Mansfield, J., and, Somerville, C., (2009) Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J. 57, 1015-1026.
30. Hedenström, M., Wiklund-Lindström, S., Ãman, T., Lu, F.C., Gerber, L., Schatz, P., Sundberg, B., and, Ralph, J., (2009) Identification of lignin and polysaccharide modifications in Populus wood by chemometric analysis of 2D NMR spectra from dissolved cell walls. Mol. Plant, 2, 933-942.
31. Hernández-Blanco, C., Feng, D.X., Hu, J., et al. (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell, 19, 890-903. (Pubitemid 46953235)
32. Hertzberg, M., Aspeborg, H., Schrader, J., et al. (2001) A transcriptional roadmap to wood formation. Proc. Natl Acad. Sci. USA, 98, 14732-14737. (Pubitemid 33121460)
33. Huber, S.C., and, Akazawa, T., (1986) A novel sucrose synthase pathway for sucrose degradation in cultured sycamore cells. Plant Physiol. 81, 1008-1013.
34. Jiang, H., Dian, W., Liu, F., and, Wu, P., (2003) Isolation and characterization of two fructokinase cDNA clones from rice. Phytochemistry, 62, 47-52. (Pubitemid 36869766)
35. Kanayama, Y., Granot, D., Dai, N., Petreikov, M., Schaffer, A., Powell, A., and, Bennett, A.B., (1998) Tomato fructokinases exhibit differential expression and substrate regulation. Plant Physiol. 117, 85-90. (Pubitemid 128652781)
36. Karimi, M., Inzé, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
37. Leplé, J.C., Dauwe, R., Morreel, K., et al. (2007) Downregulation of cinnamoyl-coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell, 19, 3669-3691.
38. Lerouxel, O., Cavalier, D.M., Liepman, A.H., and, Keegstra, K., (2006) Biosynthesis of plant cell wall polysaccharides-a complex process. Curr. Opin. Plant Biol. 9, 621-630. (Pubitemid 44537843)
39. Libault, M., Wan, J., Czechowski, T., Udvardi, M., and, Stacey, G., (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Plant Microbe Interact, 20, 900-911. (Pubitemid 47105723)
40. Liu, F., VanToai, T., Moy, L.P., Bock, G., Linford, L.D., and, Quackenbush, J., (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol. 137, 1115-1129. (Pubitemid 43138182)
41. Lunn, J.E., Feil, R., Hendriks, J.H., Gibon, Y., Morcuende, R., Osuna, D., Scheible, W.R., Carillo, P., Hajirezaei, M.R., and, Stitt, M., (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem. J. 397, 139-148. (Pubitemid 44032845)
42. Martinez-Barajas, E., and, Randall, D.D., (1996) Purification and characterization of fructokinase from developing tomato (Lycopersicon esculentum Mill) fruits. Planta, 199, 451-458. (Pubitemid 26263198)
43. Martinez-Barajas, E., Krohn, B.M., Stark, D.M., and, Randall, D.D., (1997) Purification and characterization of recombinant tomato fruit (Lycopersicon esculentum Mill.) fructokinase expressed in Escherichia coli. Protein Expr. Purif. 11, 41-46. (Pubitemid 27434130)
44. McHale, L., Tan, X., Koehl, P., and, Michelmore, R., (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol. 7, 212.
45. Meier, D., Fortmann, I., Odermatt, J., and, Faix, O., (2005) Discrimination of genetically modified poplar clones by analytical pyrolysis-gas chromatography and principal component analysis. J. Anal. Appl. Pyrol. 74, 129-137. (Pubitemid 40743544)
46. Mueller, L.A., Solow, T.H., Taylor, N., et al. (2005) The SOL Genomics Network. A comparative resource for Solanaceae biology and beyond. Plant Physiol. 138, 1310-1317. (Pubitemid 43142079)
47. Nilsson, O., Aldén, T., Sitbon, F., Little, C.H.A., Chalupa, V., Sandberg, G., and, Olsson, O., (1992) Spatial pattern of cauliflower mosaic virus 35S promoter-luciferase expression in transgenic hybrid aspen trees monitored by enzymatic assay and non-destructive imaging. Transgenic Res. 1, 209-220.
48. Odanaka, S., Bennett, A.B., and, Kanayama, Y., (2002) Distinct physiological roles of fructokinase isozymes revealed by gene-specific suppression of Frk1 and Frk2 expression in tomato. Plant Physiol. 129, 1119-1126. (Pubitemid 34801082)
49. Pego, J.V., and, Smeekens, S.C., (2000) Plant fructokinases: a sweet family get-together. Trends Plant Sci. 5, 531-536. (Pubitemid 32099971)
50. Petreikov, M., Dai, N., Granot, D., and, Schaffer, A.A., (2001) Characterization of native and yeast-expressed tomato fruit fructokinase enzymes. Phytochemistry, 58, 841-847. (Pubitemid 33086208)
51. Pregitzer, K.S., and, Euskirchen, E.S., (2004) Carbon cycling and storage in world forests: biome patterns related to forest age. Glob. Change Biol. 10, 2052-2077. (Pubitemid 40015006)
52. Renz, A., and, Stitt, M., (1993) Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta, 190, 166-175.
53. Sato, T., (1968) A modified method for lead staining of thin sections. J. Electron Microsc. (Tokyo) 17, 158-159.
54. Sharples, S.C., and, Fry, S.C., (2007) Radioisotope ratios discriminate between competing pathways of cell wall polysaccharide and RNA biosynthesis in living plant cells. Plant J. 52, 252-262. (Pubitemid 47537577)
55. Smith, A.M., and, Zeeman, S., (2006) Quantification of starch in plant tissues. Nat. Protoc. 1, 1342-1345.
56. Speleman, F., Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., and, De Paepe, A., (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034-research0034.11.
57. Spurr, A.R., (1969) A low viscosity embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43.
58. Stenlund, H., Gorzsás, A., Persson, P., Sundberg, B., and, Trygg, J., (2008) Orthogonal projections to latent structures discriminant analysis modeling on in situ FT-IR spectral imaging of liver tissue for identifying sources of variability. Anal. Chem. 80, 6898-6906.
59. Stitt, M., Lilley, R.M., Gerhardt, R., and, Heldt, H.W., (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol. 174, 518-552. (Pubitemid 20046307)
60. Sturm, A., and, Tang, G.Q., (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 4, 401-407. (Pubitemid 29471623)
61. Tamura, K., Dudley, J., Nei, M., and, Kumar, S., (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. (Pubitemid 47236692)
62. Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R., and, Turner, S.R., (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell, 11, 769-779.
63. Taylor, N.G., Laurie, S., and, Turner, S.R., (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell, 12, 2529-2539. (Pubitemid 32106423)
64. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L., Rhee, S., and, Stitt, M., (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939. (Pubitemid 38370342)
65. Trygg, J., and, Wold, S., (2002) Orthogonal projections to latent structures (O-PLS). J. Chemom, 16, 119-128.
66. Trygg, J., and, Wold, S., (2003) O2-PLS, a two-block (X-Y) latent variable regression (LVR) method with an integral OSC filter. J. Chemom, 17, 53-64.
67. Turgeon, R., (1996) Phloem loading and plasmodesmata. Trends Plant Sci. 1, 418-423. (Pubitemid 27134222)
68. Updegraff, D., (1969) Semi-micro determination of cellulose in biological materials. Anal. Biochem. 32, 420-424.
69. Wheeler, E.A., Baas, P., and, Gasson, P., (1989) IAWA list of microscopic features for hardwood identification. IAWA Bull. (NS), 10, 219-332.
70. Yanhui, C., Xiaoyuan, Y., Kun, H., et al. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 60, 107-124. (Pubitemid 43194446)
71. Zhang, S.R., Nichols, S.E., and, Dong, J.G., (2003) Cloning and characterization of two fructokinases from maize. Plant Sci. 165, 1051-1058. (Pubitemid 37231803)