Male Sterility1 is required for tapetal development and pollen wall biosynthesis

Plant Cell

Volumn 19, Issue 11, 2007, Pages 3530-3548

  Yang, Caiyun ^a   Vizcay Barrena, Gema ^a   Conner, Katie ^a   Wilson, Zoe A ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MICROARRAYS; MOLECULAR BIOLOGY; PLANT CELL CULTURE; TRANSCRIPTION FACTORS;

ARABIDOPSIS THALIANA; GREEN FLUORESCENT PROTEIN (GFP); MALE STERILITY1; POLLEN FORMATION;

GENES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 37849039575     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.054981     Document Type: Article

References (66)

1. Aarts, M.G., Hodge, R., Kalantidis, K., Florack, D., Wilson, Z.A., Mulligan, B.J., Stiekema, W.J., Scott, R., and Pereira, A. (1997). The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J. 12: 615-623.
2. Aarts, M.G.M., Dirkse, W.G., Stiekema, W.J., and Pereira, A. (1993). Transposon tagging of a male sterility gene in Arabidopsis. Nature 363: 715-717.
3. Albrecht, C., Russinova, E., Hecht, V., Baaijens, E., and de Vries, S. (2005). The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17: 3337-3349.
4. Alexander, M.P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technol. 44: 117-122.
5. Ariizumi, T., Hatakeyama, K., Hinata, K., Inatsugi, R., Nishida, I., Sato, S., Kato, T., Tabata, S., and Toriyama, K. (2004). Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J. 39: 170-181.
6. Ariizumi, T., Hatakeyama, K., Hinata, K., Sato, S., Kato, T., Tabata, S., and Toriyama, K. (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.
7. Ariizumi, T., Hatakeyama, K., Hinata, K., Sato, S., Kato, T., Tabata, S., and Toriyama, K. (2005). The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation. Sex. Plant Reprod. 18: 1-7.
8. Asaland, R., Gibson, T.J., and Stewart, A.F. (1995). The PHD finger: Implications for chromatin-mediated transcriptional regulation. Trends Biotechnol. 20: 56-59.
9. Bhatt, A.M., Canales, C., and Dickinson, H.G. (2001). Plant meiosis: The means to 1N. Trends Plant Sci. 6: 114-121.
10. Bolstad, B.M., Irizarry, R.A., Astrand, M., and Speed, T.P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
11. Canales, C., Bhatt, A.M., Scott, R., and Dickinson, H. (2002). EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12: 1718-1727.
12. Chasan, R. (1992). Breaching the callose wall. Plant Cell 4: 745-746.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C.E., and Schroeder, J.I. (2005). Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17: 3350-3361.
15. Dawson, J., Wilson, Z.A., Aarts, M.G.M., Braithwaite, A.F., Briarty, L.G., and Mulligan, B.J. (1993). Microspore and pollen development in six male-sterile mutants of Arabidopsis thaliana. Can. J. Bot. 71: 629-638.
16. Dong, X., Hong, Z., Sivaramakrishnan, M., Mahfouz, M., and Verma, D.P. (2005). Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J. 42: 315-328.
17. Goldberg, R., Beals, T., and Sanders, P. (1993). Anther development: Basic principles and practical applications. Plant Cell 5: 1217-1229.
18. Hoeberichts, F.A., and Woltering, E.J. (2003). Multiple mediators of plant programmed cell death: Interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25: 47-57.
19. Honys, D., and Twell, D. (2004). Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5: R85.
20. Hooker, T.S., Millar, A.A., and Kunst, L. (2002). Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol. 129: 1568-1580.
21. Hsieh, K., and Huang, A.H. (2004). Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiol. 136: 3427-3434.
22. Hsieh, K., and Huang, A.H. (2007). Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19: 582-596.
23. Ito, T., Nagata, N., Yoshiba, Y., Ohme-Takagi, M., Hong, M., and Shinozaki, K. (2007). Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19: 3549-3562.
24. Ito, T., and Shinozaki, K. (2002). The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol. 43: 1285-1292.
25. Jung, K.H., Han, M.J., Lee, Y.S., Kim, Y.W., Hwang, I., Kim, M.J., Kim, Y.K., Nahm, B.H., and An, G. (2005). Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17: 2705-2722.
26. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
27. Kepinski, S., and Leyser, O. (2002). Ubiquitination and auxin signaling: A degrading story. Plant Cell 14(Suppl): S81-S95.
28. Kim, H.U., Hsieh, K., Ratnayake, C., and Huang, A.H. (2002). A novel group of oleosins is present inside the pollen of Arabidopsis. J. Biol. Chem. 277: 22677-22684.
29. Lacoux, J., Gutierrez, L., Dantin, F., Beaudoin, B., Roger, D., and Laine, E. (2003). Antisense transgenesis of tobacco with a flax pectin methylesterase affects pollen ornamentation. Protoplasma 222: 205-209.
30. Lam, E., and del Pozo, O. (2000). Caspase-like protease involvement in the control of plant cell death. Plant Mol. Biol. 44: 417-428.
31. Li, N., et al. (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014.
32. Ma, H. (2005). Molecular genetic analysis of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56: 393-434.
33. 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.
34. Mayfield, J.A., and Preuss, D. (2000). Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat. Cell Biol. 2: 128-130.
35. McCormick, S. (2004). Control of male gametophyte development. Plant Cell 16 (suppl.): S142-S153.
36. Millar, A.A., and Gubler, F. (2005). The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705-721.
37. Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19: 270-280.
38. Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2005). The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17: 2993-3006.
39. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassay with tobacco pith cultures. Physiol. Plant. 15: 473-497.
40. Pacini, E., Franchi, G., and Hesse, M. (1985). The tapetum: Its form, function, and possible phylogeny in embryophyta. Plant Syst. Evol. 149: 155-185.
41. Paxson-Sowders, D.M., Dodrill, C.H., Owen, H.A., and Makaroff, C.A. (2001). DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol. 127: 1739-1749.
42. 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.
43. Quesada, V., Macknight, R., Dean, C., and Simpson, G.G. (2003). Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J. 22: 3142-3152.
44. Reddy, T.V., Kaur, J., Agashe, B., Sundaresan, V., and Siddiqi, I. (2003). The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development 130: 5975-5987.
45. Regan, S.M., and Moffatt, B.A. (1990). Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. Plant Cell 2: 877-889.
46. Rubinelli, P., Hu, Y., and Ma, H. (1998). Identification, sequence analysis and expression studies of novel anther-specific genes of Arabidopsis thaliana. Plant Mol. Biol. 37: 607-619.
47. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
48. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and Schneitz, K. (1999). Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 11664-11669.
49. Scott, R.J., Spielman, M., and Dickinson, H.G. (2004). Stamen structure and function. Plant Cell 16(Suppl 1): S46-S60.
50. Shi, X., et al. (2006). ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99.
51. Siloto, R.M., Findlay, K., Lopez-Villalobos, A., Yeung, E.C., Nykiforuk, C.L., and Moloney, M.M. (2006). The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell 18: 1961-1974.
52. Smyth, D.R., Bowman, J.L., and Meyerowitz, E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755-767.
53. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., and Levine, A. (1999). The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431-444.
54. Sorensen, A.M., Krober, S., Unte, U.S., Huijser, P., Dekker, K., and Saedler, H. (2003). The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33: 413-423.
55. Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., 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.
56. Tusher, V.G., Tibshirani, R., and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121.
57. Vizcay-Barrena, G., and Wilson, Z.A. (2006). Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J. Exp. Bot. 57: 2709-2717.
58. Wijeratne, A.J., Zhang, W., Sun, Y., Liu, W., Albert, R., Zheng, Z., Oppenheimer, D.G., Zhao, D., and Ma, H. (2007). Differential gene expression in Arabidopsis wild-type and mutant anthers: Insights into anther cell differentiation and regulatory networks. Plant J. 52: 14-29.
59. Wilson, Z.A., Morroll, S.M., Dawson, J., Swarup, R., and Tighe, P.J. (2001). The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 28: 27-39.
60. Wysocka, J., Swigut, T., Xiao, H., Milne, T.A., Kwon, S.Y., Landry, J., Kaue, M., Tackett, A.J., Chait, B.T., Badenhorst, P., Wu, C., and Allis, C.D. (2006). A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90.
61. Yang, S.L., Xie, L.F., Mao, H.Z., Puah, C.S., Yang, W.C., Jiang, L., Sundaresan, V., and Ye, D. (2003a). TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15: 2792-2804.
62. Yang, W.C., Ye, D., Xu, J., and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13: 2108-2117.
63. Yang, X., Makaroff, C.A., and Ma, H. (2003b). The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15: 1281-1295.
64. Zhang, W., Sun, Y.L., Timofejeva, L., Chen, C., Grossniklaus, U., and Ma, H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM (DYT1) encoding a putative bHLH transcription factor. Development 133: 3085-3095.
65. Zhao, D.Z., Wang, G.F., Speal, B., and Ma, H. (2002). The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16: 2021-2031.
66. Zheng, Z., Xia, Q., Dauk, M., Shen, W., Selvaraj, G., and Zou, J. (2003). Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell 15: 1872-1887.