The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato

Plant Journal

Volumn 57, Issue 1, 2009, Pages 1-13

  Nashilevitz, Shai ^a,b   Melamed Bessudo, Cathy ^a   Aharoni, Asaph ^a   Kossmann, Jens ^c   Wolf, Shmuel ^b   Levy, Avraham A ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Carbohydrate metabolism; Male sterility; Starch degradation; Starch excess; Transposon tagging

Indexed keywords

PHOSPHOTRANSFERASE; STARCH; VEGETABLE PROTEIN;

ALLELE; ARTICLE; ENZYMOLOGY; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; PHOSPHORYLATION; PLANT LEAF; PLASTID; POLLEN; TOMATO; TRANSPOSON;

ALLELES; DNA TRANSPOSABLE ELEMENTS; FERTILITY; GENE EXPRESSION REGULATION, PLANT; GERMINATION; LYCOPERSICON ESCULENTUM; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PHOSPHORYLATION; PHOSPHOTRANSFERASES (PAIRED ACCEPTORS); PLANT LEAVES; PLANT PROTEINS; PLASTIDS; POLLEN; STARCH;

ARABIDOPSIS; LYCOPERSICON ESCULENTUM; SOLANUM TUBEROSUM;

EID: 58149138857     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03664.x     Document Type: Article

References (58)

1. Alexander, M.P. (1980) A versatile stain for pollen fungi, yeast and bacteria. Stain Technol. 55, 13 18.
2. Aloni, B., Peet, M., Pharr, M. Karni, L. (2001) The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiol. Plant, 112, 505 512.
3. Baunsgaard, L., Lutken, H., Mikkelsen, R., Glaring, M.A., Pham, T.T. Blennow, A. (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J. 41, 595 605.
4. Betz, A.U. (1997) Generation and analysis of conditional mutant mice. Res. Immunol. 148, 475 480.
5. Blennow, A., Bay-Smidt, A.M., Olsen, C.E. Moller, B.L. (2000) The distribution of covalently bound phosphate in the starch granule in relation to starch crystallinity. Int. J. Biol. Macromol. 27, 211 218.
6. Blennow, A., Nielsen, T.H., Baunsgaard, L., Mikkelsen, R. Engelsen, S.B. (2002) Starch phosphorylation: a new front line in starch research. Trends Plant Sci. 7, 445 450.
7. Caspar, T., Lin, T.P., Kakefuda, G., Benbow, L., Preiss, J. Somerville, C. (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol. 95, 1181 1188.
8. Chen, R., Zhao, X., Shao, Z., Wei, Z., Wang, Y., Zhu, L., Zhao, J., Sun, M., He, R. He, G. (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell, 19, 847 861.
9. Clement, C. Audran, J.C. (1999) Anther carbohydrates during in vivo and in vitro pollen development. In Anther and Pollen from Biology to Biotechnology (Clement, C., Pacini, E. Audran, J.C., eds). Berlin : Springer, pp. 69 90.
10. Datta, R., Chamusco, K.C. Chourey, P.S. (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol. 130, 1645 1656.
11. Dorion, S., Lalonde, S. Saini, H.S. (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol. 111, 137 145.
12. Edner, C., Li, J., Albrecht, T. et al. (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol. 145, 17 28.
13. van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A. Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288 290.
14. Eshed, Y. Zamir, D. (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield associated QTL. Genetics, 141, 1147 1162.
15. Eshed, Y., Baum, S.F. Bowman, J.L. (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell, 99, 199 209.
16. Franchi, G.G., Bellani, L., Nepi, M. Pacini, E. (1996) Types of carbohydrate reserves in pollen: localization, systematic distribution and ecophysiological significance. Flora, 191, 143 159.
17. Garcia, C.C. (2007) Pollen starch reserves in tomato relatives: ecophysiological implications. Grana, 46, 13 19.
18. Gass, N., Glagotskaia, T., Mellema, S., Stuurman, J., Barone, M., Mandel, T., Roessner-Tunali, U. Kuhlemeier, C. (2005) Pyruvate decarboxylase provides growing pollen tubes with a competitive advantage in petunia. Plant Cell, 17, 2355 2368.
19. Gentry, M.S., Dowen, R.H. III., Worby, C.A., Mattoo, S., Ecker, J.R. Dixon, J.E. (2007) The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J. Cell Biol. 178, 477 488.
20. Glaring, M.A., Zygadlo, A., Thorneycroft, D., Schulz, A., Smith, S.M., Blennow, A. Baunsgaard, L. (2007) An extra-plastidial {alpha}-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J. Exp. Bot. 58, 3949 3960.
21. Goetz, M., Godt, D.E., Guivarc'h, 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, 6522 6527.
22. Hoekstra, F.A., Crowe, J.H. Crowe, L.M. (1989) Differential desiccation sensitivity of corn and Pennisetum pollen linked to their sucrose contents. Plant Cell Environ. 12, 83 91.
23. Hoekstra, F.A., Crowe, J.H., van Roekel, T. Vermeer, E. (1992) Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species? Plant Cell Environ. 15, 601 606.
24. Jobling, S. (2004) Improving starch for food and industrial applications. Curr. Opin. Plant Biol. 7, 210 218.
25. Kaplan, F. Guy, C.L. (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J. 44, 730 743.
26. Koonjul, P.K., Minhas, J.S., Nunes, C., Sheoran, I.S. Saini, H.S. (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J. Exp. Bot. 56, 179 190.
27. Kötting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M. Ritte, G. (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137, 242 252.
28. Kuang, A. Musgrave, M.E. (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation in Arabidopsis thaliana. Protoplasma, 194, 81 90.
29. Lloyd, J.R., Kossmann, J. Ritte, G. (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci. 10, 130 137.
30. Lorberth, R., Ritte, G., Willmitzer, L. Kossmann, J. (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat. Biotechnol. 16, 473 477.
31. Meissner, R., Jacobson, Y., Melamed, S., Levyatuv, S., Shalev, G., Ashri, A., Elkind, Y. Levy, A.A. (1997) A new model system for tomato genetics. Plant J. 12, 1465 1472.
32. Meissner, R., Chague, V., Zhu, Q., Emmanuel, E., Elkind, Y. Levy, A.A. (2000) Technical advance: a high throughput system for transposon tagging and promoter trapping in tomato. Plant J. 22, 265 274.
33. Mikkelsen, R., Baunsgaard, L. Blennow, A. (2004) Functional characterization of alpha-glucan,water dikinase, the starch phosphorylating enzyme. Biochem. J. 377, 525 532.
34. Mikkelsen, R., Mutenda, K.E., Mant, A., Schurmann, P. Blennow, A. (2005) Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc. Natl Acad. Sci. USA, 102, 1785 1790.
35. Niewiadomski, P., Knappe, S., Geimer, S., Fischer, K., Schulz, B., Unte, U.S., Rosso, M.G., Ache, P., Flugge, U.I. Schneider, A. (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell, 17, 760 775.
36. Niittyla, T., Comparot-Moss, S., Lue, W.L. et al. (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J. Biol. Chem. 281, 11815 11818.
37. Pacini, E. (1996) Types and meaning of pollen carbohydrate reserves. Sex. Plant Reprod. 9, 362 366.
38. Pacini, E. Franchi, G.G. (1988) Amylogenesis and amylolysis during pollen grain development. In Sexual Reproduction in Higher Plants (Cresti, M., Gori, P. Pacini, E., eds). Berlin, Heidelberg, New York : Springer, pp. 181 186.
39. Pacini, E. Viegi, L. (1995) Total polysaccharide content of developing pollen in two angiosperm species. Grana, 34, 237 241.
40. Polowick, P.L. Sawhney, V.K. (1993) An ultrastructural study of pollen development in tomato (Lycopersicon esculentum). II. Pollen maturation. Can. J. Bot. 71, 1048 1055.
41. Pressman, E., Moshkovitch, H., Rosenfeld, K., Shaked, R., Gamliel, B. Aloni, B. (1998) Influence of low night temperatures on sweet pepper flower quality and the effect of repeated pollinations, with viable pollen, on fruit setting. J. Hortic. Sci. Biotechnol. 73, 131 136.
42. Pressman, E., Peet, M.M. Pharr, D.M. (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann. Bot. (Lond.), 90, 631 636.
43. Pressman, E., Harel, D., Zamski, E., Shaked, R., Althan, L., Rosenfeld, K. Firon, N. (2006) The effect of high temperatures on the expression and activity of sucrose-cleaving enzymes during tomato (Lycopersicon esculentum) anther development. J. Horti. Sci. Biotechnol. 81, 341 348.
44. Reimann, R., Ritte, G., Steup, M. Appenroth, K.J. (2002) Association of alpha-amylase and the R1 protein with starch granules precedes the initiation of net starch degradation in turions of Spirodela polyrhiza. Physiol. Plant, 114, 2 12.
45. Ritte, G., Lorberth, R. Steup, M. (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant J. 21, 387 391.
46. Ritte, G., Lloyd, J.R., Eckermann, N., Rottmann, A., Kossmann, J. Steup, M. (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc. Natl Acad. Sci. USA, 99, 7166 7171.
47. Ritte, G., Steup, M., Kossmann, J. Lloyd, J.R. (2003) Determination of the starch-phosphorylating enzyme activity in plant extracts. Planta, 216, 798 801.
48. Ritte, G., Scharf, A., Eckermann, N., Haebel, S. Steup, M. (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol. 135, 2068 2077.
49. Scott, L., LaFoe, D. Weil, C.F. (1996) Adjacent sequences influence DNA repair accompanying transposon excision in maize. Genetics, 142, 237 246.
50. Shaked, R., Rosenfeld, K. Pressman, E. (2004) The effect of low night temperatures on carbohydrates metabolism in developing pollen grains of pepper in relation to their number and functioning. Sci. Hortic. 102, 29 36.
51. Smith, A.M., Zeeman, S.C. Smith, S.M. (2005) Starch degradation. Annu. Rev. Plant Biol. 56, 73 98.
52. Speranza, A., Calzoni, G.L. Pacini, E. (1997) Occurrence of mono- or disaccharides and polysaccharide reserves in mature pollen grains. Sex. Plant Reprod. 10, 110 115.
53. Twell, D., Yamaguchi, J. McCormick, S. (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development, 109, 705 713.
54. Vikso-Nielsen, A., Hao-Jie Chen, P., Larsson, H., Blennow, A. Moller, B.L. (2002) Production of highly phosphorylated glycopolymers by expression of R1 in Escherichia coli. Carbohydr. Res. 337, 327 333.
55. Weigel, D., Ahn, J.H., Blazquez, M.A. et al. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003 1013.
56. Yu, T.S., Kofler, H., Hausler, R.E. et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell, 13, 1907 1918.
57. Zeeman, S.C., Northrop, F., Smith, A.M. Rees, T. (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 15, 357 365.
58. Zhu, Q.H., Ramm, K., Shivakkumar, R., Dennis, E.S. Upadhyaya, N.M. (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol. 135, 1514 1525.