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International Journal of Plant Genomics
Volume 2009 (2009), Article ID 407426, 23 pages
http://dx.doi.org/10.1155/2009/407426
Research Article

Transcriptomic Analysis of Starch Biosynthesis in the Developing Grain of Hexaploid Wheat

1Genomics and Gene Discovery Unit, USDA-ARS WRRC, 800 Buchanan Street, Albany, CA 94710, USA
2Department of Plant Sciences MS3, University of California-Davis, 1 Shields Avenue, Davis, CA 95618, USA
3Department of Neurology, School of Medicine, M.I.N.D Institute, University of California Medical Center, 2805 50th Street, Sacramento, CA 95817, USA

Received 12 May 2009; Revised 19 September 2009; Accepted 19 November 2009

Academic Editor: Hikmet Budak

Copyright © 2009 Boryana S. Stamova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. R. Morrison and J. Karkalas, “Starch,” in Methods in Plant Biochemistry, P. M. Day, Ed., Academic Press, San Diego, Calif, USA, 1990.
  2. A. M. Myers, M. K. Morell, M. G. James, and S. G. Ball, “Recent progress toward understanding biosynthesis of the amylopectin crystal,” Plant Physiology, vol. 122, no. 4, pp. 989–997, 2000. View at Scopus
  3. J. P. Davis, N. Supatcharee, R. L. Khandelwal, and R. N. Chibbar, “Synthesis of novel starches in planta: opportunities and challenges,” Starch-Stärke, vol. 55, no. 3-4, pp. 107–120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. J. D. Wilson, D. B. Bechtel, T. C. Todd, and P. A. Seib, “Measurement of wheat starch granule size distribution using image analysis and laser diffraction technology,” Cereal Chemistry, vol. 83, no. 3, pp. 259–268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. C. E. Hughes and L. G. Briarty, “Stereological analysis of contribution made to mature wheat endosperm starch by large and small granules,” Starch-Stärke, vol. 28, no. 10, pp. 336–337, 1976.
  6. S. M. J. Langeveld, R. Van Wijk, N. Stuurman, J. W. Kijne, and S. De Pater, “B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression,” Journal of Experimental Botany, vol. 51, no. 349, pp. 1357–1361, 2000. View at Scopus
  7. D. B. Bechtel and J. D. Wilson, “Amyloplast formation and starch granule development in hard red winter wheat,” Cereal Chemistry, vol. 80, no. 2, pp. 175–183, 2003. View at Scopus
  8. L. G. Briarty, C. E. Hughes, and A. D. Evers, “The developing endosperm of wheat: a stereological analysis,” Annals of Botany, vol. 44, no. 6, pp. 641–658, 1979. View at Scopus
  9. M. L. Parker, “The relationship between A-type and B-type starch granules in the developing endosperm of wheat,” Journal of Cereal Science, vol. 3, no. 4, pp. 271–278, 1985.
  10. S. Sahlström, E. Bråthen, P. Lea, and K. Autio, “Influence of starch granule size distribution on bread characteristics,” Journal of Cereal Science, vol. 28, no. 2, pp. 157–164, 1998. View at Scopus
  11. N. Lindeboom, P. R. Chang, and R. T. Tyler, “Analytical, biochemical and physicochemical aspects of starch granule size, with emphasis on small granule starches: a review,” Starch-Stärke, vol. 56, no. 3-4, pp. 89–99, 2004. View at Scopus
  12. P. G. Yonemoto, M. A. Calori-Domingues, and C. M. L. Franco, “Effect of granule size on the structural and physicochemical characteristics of wheat starch,” Ciencia e Tecnologia de Alimentos, vol. 27, no. 4, pp. 761–771, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Preiss, K. Ball, B. Smith-White, A. Iglesias, G. Kakefuda, and L. Li, “Starch biosynthesis and its regulation,” Biochemical Society Transactions, vol. 19, no. 3, pp. 539–547, 1991. View at Scopus
  14. P. Geigenberger, M. Stitt, and A. R. Fernie, “Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers,” Plant, Cell and Environment, vol. 27, no. 6, pp. 655–673, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. I. J. Tetlow, R. Wait, Z. Lu, et al., “Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions,” The Plant Cell, vol. 16, no. 3, pp. 694–708, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Koch, “Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development,” Current Opinion in Plant Biology, vol. 7, no. 3, pp. 235–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Price, A. Laxmi, S. K. St. Martin, and J.-C. Jang, “Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis,” The Plant Cell, vol. 16, no. 8, pp. 2128–2150, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. N. G. Halford and M. J. Paul, “Carbon metabolite sensing and signalling,” Plant Biotechnology Journal, vol. 280, pp. 25590–25595, 2003.
  19. F. Rolland, E. Baena-Gonzalez, and J. Sheen, “Sugar sensing and signaling in plants: conserved and novel mechanisms,” Annual Review of Plant Biology, vol. 57, pp. 675–709, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Sun, S. Palmqvist, H. Olsson, M. Borén, S. Ahlandsberg, and C. Jansson, “A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter,” The Plant Cell, vol. 15, no. 9, pp. 2076–2092, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. D. L. Laudencia-Chingcuanco, B. S. Stamova, F. M. You, G. R. Lazo, D. M. Beckles, and O. D. Anderson, “Transcriptional profiling of wheat caryopsis development using cDNA microarrays,” Plant Molecular Biology, vol. 63, no. 5, pp. 651–668, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Wan, R. L. Poole, A. K. Huttly, et al., “Transcriptome analysis of grain development in hexaploid wheat,” BMC Genomics, vol. 9, article 121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. F. L. Stoddard, “Survey of starch particle-size distribution in wheat and related species,” Cereal Chemistry, vol. 76, no. 1, pp. 145–149, 1999. View at Scopus
  24. R. A. Irizarry, B. Hobbs, F. Collin, et al., “Exploration, normalization, and summaries of high density oligonucleotide array probe level data,” Biostatistics, vol. 4, no. 2, pp. 249–264, 2003. View at Scopus
  25. R. P. Wise, R. A. Caldo, L. Hong, L. Shen, E. Cannon, and J. A. Dickerson, “BarleyBase/PLEXdb: a unified expression profiling database for plants and plant pathogens,” Methods in Molecular Biology, vol. 406, pp. 347–363, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. O. Thimm, O. Bläsing, Y. Gibon, et al., “MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes,” The Plant Journal, vol. 37, no. 6, pp. 914–939, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Abou-Guendia and B. L. D'Appolonia, “Changes in carbohydrate components during wheat maturation I. Changes in free sugars,” Cereal Chemistry, vol. 49, pp. 664–676, 1972.
  28. C. F. Jenner, “Uptake of sucrose and its conversion to starch in detached ears of wheat,” Journal of Experimental Botany, vol. 24, pp. 295–306, 1973.
  29. P. L. Keeling, J. R. Wood, R. H. Tyson, and I. G. Bridges, “Starch biosynthesis in developing wheat grain: evidence against the direct involvement of triose phosphates in the metabolic pathway,” Plant Physiology, vol. 87, no. 2, pp. 311–319, 1988.
  30. S. B. Altenbach and K. M. Kothari, “Transcript profiles of genes expressed in endosperm tissue are altered by high temperature during wheat grain development,” Journal of Cereal Science, vol. 40, no. 2, pp. 115–126, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. W. J. Hurkman, K. F. McCue, S. B. Altenbach, et al., “Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm,” Plant Science, vol. 164, no. 5, pp. 873–881, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Kawaura, K. Mochida, and Y. Ogihara, “Expression profile of two storage-protein gene families in hexaploid wheat revealed by large-scale analysis of expressed sequence tags,” Plant Physiology, vol. 139, no. 4, pp. 1870–1880, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Rosti and K. Denyer, “Two paralogous genes encoding small subunits of ADP-glucose pyrophosphorylase in maize, Bt2 and L2, replace the single alternatively spliced gene found in other cereal species,” Journal of Molecular Evolution, vol. 65, no. 3, pp. 316–327, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Thorbjørnsen, P. Villand, L. A. Kleczkowski, and O.-A. Olsen, “A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare),” Biochemical Journal, vol. 313, no. 1, pp. 149–154, 1996. View at Scopus
  35. M. Leterrier, L. D. Holappa, K. E. Broglie, and D. M. Beckles, “Cloning, characterisation and comparative analysis of a starch synthase IV gene in wheat: functional and evolutionary implications,” BMC Plant Biology, vol. 8, article 98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Gao, D. K. Fisher, K.-N. Kim, J. C. Shannon, and M. J. Guiltinan, “Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization,” Plant Molecular Biology, vol. 30, no. 6, pp. 1223–1232, 1996. View at Scopus
  37. M. K. Morell, A. Blennow, B. Kosar-Hashemi, and M. S. Samuel, “Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm,” Plant Physiology, vol. 113, no. 1, pp. 201–208, 1997. View at Scopus
  38. M. Peng, M. Gao, M. Baga, P. Hucl, and R. N. Chibbar, “Starch-branching enzymes preferentially associated with A-type starch granules in wheat endosperm,” Plant Physiology, vol. 124, no. 1, pp. 265–272, 2000. View at Scopus
  39. M. Baga, R. B. Nair, A. Repellin, G. J. Scoles, and R. N. Chibbar, “Isolation of a cDNA encoding a granule-bound 152-kilodalton starch-branching enzyme in wheat,” Plant Physiology, vol. 124, no. 1, pp. 253–263, 2000. View at Scopus
  40. C. Colleoni, D. Dauvillee, G. Mouille, et al., “Biochemical characterization of the Chlamydomonas reinhardtii α-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis,” Plant Physiology, vol. 120, no. 4, pp. 1005–1014, 1999. View at Scopus
  41. A. Repellin, M. Båga, and R. N. Chibbar, “In vitro pullulanase activity of wheat (Triticum aestivum L.) limit-dextrinase type starch debranching enzyme is modulated by redox conditions,” Journal of Cereal Science, vol. 47, no. 2, pp. 302–309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. K. A. Duncan, S. C. Hardin, and S. C. Huber, “The three maize sucrose synthase isoforms differ in distribution, localization, and phosphorylation,” Plant and Cell Physiology, vol. 47, no. 7, pp. 959–971, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. Z. Bieniawska, D. H. P. Barratt, A. P. Garlick, et al., “Analysis of the sucrose synthase gene family in Arabidopsis,” The Plant Journal, vol. 49, no. 5, pp. 810–828, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. C. K. Castleden, N. Aoki, V. J. Gillespie, et al., “Evolution and function of the sucrose-phosphate synthase gene families in wheat and other grasses,” Plant Physiology, vol. 135, no. 3, pp. 1753–1764, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Sreenivasulu, L. Altschmied, V. Radchuk, S. Gubatz, U. Wobus, and W. Weschke, “Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains,” The Plant Journal, vol. 37, no. 4, pp. 539–553, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Geigenberger, A. Kolbe, and A. Tiessen, “Redox regulation of carbon storage and partitioning in response to light and sugars,” Journal of Experimental Botany, vol. 56, no. 416, pp. 1469–1479, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Sun, A.-S. Höglund, H. Olsson, E. Mangelsen, and C. Jansson, “Antisense oligodeoxynucleotide inhibition as a potent strategy in plant biology: identification of SUSIBA2 as a transcriptional activator in plant sugar signalling,” The Plant Journal, vol. 44, no. 1, pp. 128–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. H.-J. Chung, P. C. Sehnke, and R. J. Ferl, “The 14-3-3 proteins: cellular regulators of plant metabolism,” Trends in Plant Science, vol. 4, no. 9, pp. 367–371, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. P. C. Sehnke, H.-J. Chung, K. Wu, and R. J. Ferl, “Regulation of starch accumulation by granule-associated plant 14-3-3 proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 2, pp. 765–770, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. R. D. Alexander and P. C. Morris, “A proteomic analysis of 14-3-3 binding proteins from developing barley grains,” Proteomics, vol. 6, no. 6, pp. 1886–1896, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. N. G. Halford, “Regulation of carbon and amino acid metabolism: roles of sucrose nonfermenting-1-related protein kinase-1 and general control nonderepressible-2-related protein kinase,” in Advances in Botanical Research Incorporating Advances in Plant Pathology, vol. 43, pp. 93–142, 2005. View at Publisher · View at Google Scholar
  52. S. Kempa, W. Rozhon, J. Šamaj, et al., “A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism,” The Plant Journal, vol. 49, no. 6, pp. 1076–1090, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. R. S. McKibbin, N. Muttucumaru, M. J. Paul, et al., “Production of high-starch, low-glucose potatoes through over-expression of the metabolic regulator SnRK1,” Plant Biotechnology Journal, vol. 4, no. 4, pp. 409–418, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Winter and S. C. Huber, “Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes,” Critical Reviews in Biochemistry and Molecular Biology, vol. 35, no. 4, pp. 253–289, 2000. View at Scopus
  55. H.-G. Kang, S. Park, M. Matsuoka, and G. An, “White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB),” The Plant Journal, vol. 42, no. 6, pp. 901–911, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Eulgem, P. J. Rushton, S. Robatzek, and I. E. Somssich, “The WRKY superfamily of plant transcription factors,” Trends in Plant Science, vol. 5, no. 5, pp. 199–206, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. R. L. Poole, G. L. A. Barker, K. Werner, et al., “Analysis of wheat SAGE tags reveals evidence for widespread antisense transcription,” BMC Genomics, vol. 9, article 475, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. N. X. Huo, J. P. Vogel, G. R. Lazo, et al., “Structural characterization of Brachypodium genome and its syntenic relationship with rice and wheat,” Plant Molecular Biology, vol. 70, no. 1-2, pp. 47–61, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. I. J. Tetlow, “Understanding storage starch biosynthesis in plants: a means to quality improvement,” Canadian Journal of Botany, vol. 84, no. 8, pp. 1167–1185, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. D. M. Beckles, A. M. Smith, and T. ap Rees, “A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs,” Plant Physiology, vol. 125, no. 2, pp. 818–827, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Y. Hirai, M. Klein, Y. Fujikawa, et al., “Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics,” The Journal of Biological Chemistry, vol. 280, no. 27, pp. 25590–25595, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Tohge, Y. Nishiyama, M. Y. Hirai, et al., “Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor,” The Plant Journal, vol. 42, no. 2, pp. 218–235, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Deeken, J. C. Engelmann, M. Efetova, et al., “An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach,” The Plant Cell, vol. 18, no. 12, pp. 3617–3634, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. D. C. Doehlert and T. M. Kuo, “Gene expression in developing kernels of some endosperm mutants of maize,” Plant and Cell Physiology, vol. 35, no. 3, pp. 411–418, 1994. View at Scopus
  65. M. J. Giroux, C. Boyer, G. Feix, and L. C. Hannah, “Coordinated transcriptional regulation of storage product genes in the maize endosperm,” Plant Physiology, vol. 106, no. 2, pp. 713–722, 1994. View at Scopus
  66. E. W. Storlie, R. J. Ihry, L. M. Baehr, et al., “Genomic regions influencing gene expression of the HMW glutenins in wheat,” Theoretical and Applied Genetics, vol. 118, no. 2, pp. 295–303, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Doll, B. Køie, and B. O. Eggum, “Induced high lysine mutants in barley,” Radiation Botany, vol. 14, no. 2, pp. 73–80, 1974. View at Scopus
  68. M. Kreis and H. Doll, “Starch and prolamin level in single and double high-lysine barley mutants,” Physiologia Plantarum, vol. 48, no. 1, pp. 139–143, 1980. View at Publisher · View at Google Scholar
  69. H. B. Krishnan, “Characterization of high-lysine mutants of rice,” Crop Science, vol. 39, no. 3, pp. 825–831, 1999. View at Scopus
  70. K. E. Koch, “Carbohydrate-modulated gene expression in plants,” Annual Review of Plant Physiology and Plant Molecular Biology, vol. 47, no. 1, pp. 509–540, 1996. View at Scopus
  71. E. Triboi and A.-M. Triboi-Blondel, “Productivity and grain or seed composition: a new approach to an old problem—invited paper,” European Journal of Agronomy, vol. 16, no. 3, pp. 163–186, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. S.-K. Lee, S.-K. Hwang, M. Han, et al., “Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.),” Plant Molecular Biology, vol. 65, no. 4, pp. 531–546, 2007. View at Publisher · View at Google Scholar · View at Scopus