The arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl- coenzyme a synthase required for development of tapetum-specific organelles and fertility of pollen grains

Plant and Cell Physiology

Volumn 51, Issue 6, 2010, Pages 896-911

  Ishiguro, Sumie ^a   Nishimori, Yuka ^a,d   Yamada, Miho ^b   Saito, Hiroko ^a   Suzuki, Toshiya ^a   Nakagawa, Tsuyoshi ^c   Miyake, Hiroshi ^a   Okada, Kiyotaka ^b,e   Nakamura, Kenzo ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c SHIMANE UNIVERSITY   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

^e NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Arabidopsis thaliana; HMG CoA synthase; Male sterile; Mevalonate pathway; Pollen coat; Tapetal cells

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COENZYME A; 3-HYDROXY-3-METHYLGLUTARYL-COENZYME A; ACYL COENZYME A; ARABIDOPSIS PROTEIN; BACTERIAL DNA; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; CELL ORGANELLE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MUTATION; PLANT GENE; PLANT INFERTILITY; POLLEN; PROMOTER REGION; TRANSGENIC PLANT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACYL COENZYME A; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CLONING, MOLECULAR; DNA, BACTERIAL; GENE EXPRESSION PROFILING; GENES, PLANT; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS, INSERTIONAL; MUTATION; ORGANELLES; PLANT INFERTILITY; PLANTS, GENETICALLY MODIFIED; POLLEN; PROMOTER REGIONS, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77953592112     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq068     Document Type: Article

References (56)

1. Aarts, M.G.M., Keijzer, C.J., Stiekema, W.J. and Pereira, A. (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7: 2115-2127.
2. Ariizumi, T., Hatakeyama, K., Hinata, K., Sato, S., Kato, T., Tabata, S., et al. (2003) A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine. Plant Mol. Biol. 53: 107-116.
3. Chappell, J. (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 521-547.
4. Chen, X., Goodwin, S.M., Boroff, V.L., Liu, X. and Jenks, M.A. (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15: 1170-1185.
5. Cheung, A.Y., Chen, C.Y., Tao, L.Z., Andreyeva, T., Twell, D. and Wu, M.H. (2003) Regulation of pollen tube growth by Rac-like GTPases. J. Exp. Bot. 54: 73-81.
6. Dickinson, H.G. and Elleman, C.J. (1985) Structural changes in the pollen grain of Brassica oleracea during dehydration in the anther and development on the stigma as revealed by anhydrous fi xation techniques. Micron Microsc. Acta 16: 255-270.
7. Edlund, A.F., Swanson, R. and Preuss, D. (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16: S84-S97.
8. Fiebig, A., Mayfield, J.A., Miley, N.L., Chau, S., Fischer, R.L. and Preuss, D. (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12: 2001-2008.
9. Grienenberger, E., Besseau, S., Geoffroy, P., Debayle, D., Heintz, D., Lapierre, C., et al. (2009) A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J. 58: 246-259.
10. Hajdukiewicz, P., Svab, Z. and Maliga, P. (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994.
11. Hemmerlin, A., Hoeffler, J.F., Meyer, O., Tritsch, D., Kagan, I.A., Grosdemange-Billiard, C., et al. (2003) Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J. Biol. Chem. 278: 26666-26676.
12. Hernandez-Pinzon, I., Ross, J.H., Barnes, K.A., Damant, A.P. and Murphy, D.J. (1999) Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208: 588-598.
13. Hsieh, K. and Huang, A.H. (2005) Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J. 43: 889-899.
14. Hsieh, K. and Huang, A.H. (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived fl avonoids and alkanes for delivery to the pollen surface. Plant Cell 19: 582-596.
15. Hulskamp, M., Kopczak, S.D., Horejsi, T.F., Kihl, B.K. and Pruitt, R.E. (1995) Identifi cation of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J. 8: 703-714.
16. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I. and Okada, K. (2001) The DEFECTIVE IN ANTHER DEHISCIENCE 1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence and fl ower opening in Arabidopsis. Plant Cell 13: 2191-2209.
17. Kasahara, H., Hanada, A., Kuzuyama, T., Takagi, M., Kamiya, Y. and Yamaguchi, S. (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J. Biol. Chem. 277: 45188-45194.
18. Kim, H.U., Hsieh, K., Ratnayake, C. and Huang, A.H.C. (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J. Biol. Chem. 277: 22677-22684.
19. Kurata, T., Kawabata-Awai, C., Sakuradani, E., Shimizu, S., Okada, K. and Wada, T. (2003) The YORE-YORE gene regulates multiple aspects of epidermal cell differentiation in Arabidopsis. Plant J. 36: 55-66.
20. Laule, O., Furholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., et al. (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100: 6866-6871.
21. Lichtenthaler, H.K. (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 47-65.
22. Matsumoto, N. and Okada, K. (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 15: 3355-3364.
23. Mayfield, J.A., Fiebig, A., Johnstone, S.E. and Preuss, D. (2001) Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292: 2482-2485.
24. Mayfield, J.A. and Preuss, D. (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat. Cell Biol. 2: 128-130.
25. Millar, A.A., Clemens, S., Zachgo, S., Giblin, E.M., Taylor, D.C. and Kunst, L. (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11: 825-838.
26. Montamat, F., Guilloton, M., Karst, F. and Delrot, S. (1995) Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl-coenzyme A synthase. Gene 167: 197-201.
27. Morant, M., J rgensen, K., Schaller, H., Pinot, F., Müller, B. L., Werck-Reichhart, D., et al. (2007) CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19: 1473-1487.
28. Murphy, D.J. and Ross, J.H. (1998) Biosynthesis, targeting and processing of oleosin-like proteins, which are major pollen coat components in Brassica napus. Plant J. 13: 1-16.
29. Nagata, N., Suzuki, M., Yoshida, S. and Muranaka, T. (2002) Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the non-mevalonate pathway. Planta 216: 345-350.
30. Nakagawa, T., Nakamura, S., Tanaka, K., Kawamukai, M., Suzuki, T., Nakamura, K., et al. (2008) Development of R4 gateway binary vectors (R4pGWB) enabling high-throughput promoter swapping for plant research. Biosci. Biotechnol. Biochem. 72: 624-629.
31. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hino, T., Maeo, K., et al. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71: 2095-2100.
32. Owen, H.A. and Makaroff, C.A. (1995) Ultrastructure of microsporo-genesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185; 7-21.
33. Park, J.H., Halitschke, R., Kim, H.B., Baldwin, I.T., Feldmann, K.A. and Feyereisen, R. (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 31: 1-12.
34. Piffanelli, P. and Murphy, D.J. (1998) Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci. 3: 250-253.
35. Piffanelli, P., Ross, J.H. and Murphy, D.J. (1997) Intra-and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J. 11: 549-562.
36. Piffanelli, P., Ross, J.H.E. and Murphy, D.J. (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11: 65-80.
37. Platt, K.A., Huang, A.H.C. and Thomson, W.W. (1998) Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Wester during microsposogenesis. Int. J. Plant Sci. 159: 724-737.
38. Preuss, D., Lemieux, B., Yen, G. and Davis, R.W. (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev. 7: 974-985.
39. Preuss, D., Rhee, S.Y. and Davis, R.W. (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458-1460.
40. Rodriguez-Concepcion, M. and Boronat, A. (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130: 1079-1089.
41. Rodriguez-Concepcion, M., Fores, O., Martinez-Garcia, J.F., Gonzalez, V., Phillips, M.A., Ferrer, A., et al. (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16: 144-156.
42. Rohmer, M. (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep. 16: 565-574.
43. Rowland, O., Lee, R., Franke, R., Schreiber, L. and Kunst, L. (2007) The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett. 581: 3538-3544.
44. Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.C., Lee, P.Y., et al. (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant. Reprod. 11: 297-322.
45. Scott, R.J., Spielman, M. and Dickinson, H.G. (2004) Stamen structure and function. Plant Cell 16: S46-S60.
46. Sessions, A., Burke, E., Presting, G., Aux, G., McElver, J., Patton, D., et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
47. Shiba, H., Takayama, S., Iwano, M., Shimosato, H., Funato, M., Nakagawa, T., et al. (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specifi city in the self-incompatibility of Brassica species. Plant Physiol. 125: 2095-2103.
48. Suzuki, M., Kamide, Y., Nagata, N., Seki, H., Ohyama, K., Kato, H., et al. (2004) Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfi ng, early senescence and male sterility, and reduced sterol levels. Plant J. 37: 750-761.
49. Suzuki, M., Nakagawa, S., Kamide, Y., Kobayashi, K., Ohyama, K., Hashinokuchi, H., etal. (2009) Complete blockage of the mevalonate pathway results in male gametophyte lethality. J. Exp. Bot. 60: 2055-2064.
50. Ting, J.T.L., Wu, S.S.H., Ratnayake, C. and Huang, A.H.C. (1998) Constituents of the tapetosomes and elaioplasts in Brassica campestris tapetum and their degradation and retention during microsporogenesis. Plant J. 16: 541-551.
51. Twell, D., Yamaguchi, J. and McCormick, S. (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705-713.
52. von Malek, B., van der Graaff, E., Schneitz, K. and Keller, B. (2002) The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216: 187-192.
53. Wu, S.S.H., Moreau, R.A., Whitaker, B.D. and Huang, A.H.C. (1999) Steryl esters in the elaioplasts of the tapetum in developing Brassica anthers and their recovery on the pollen surface. Lipids 34: 517-523.
54. Wu, S.S.H., Platt, K.A., Ratnayake, C., Wang, T.W., Ting, J.T. and Huang, A.H.C. (1997) Isolation and characterization of neutral-lipid-containing organelles and globuli-fi lled plastids from Brassica napus tapetum. Proc. Natl Acad. Sci. USA 94: 12711-12716.
55. Zambryski, P., Joos, H., Genetello, C., Leemans, J., Montagu, M.V. and Schell, J. (1983) Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J. 2: 2143-2150.
56. Zinkl, G.M., Zwiebel, B.I., Grier, D.G. and Preuss, D. (1999) Pollen-stigma adhesion in Arabidopsis: a species-specifi c interaction mediated by lipophilic molecules in the pollen exine. Development 126: 5431-5440.