Programmed cell death may act as a surveillance mechanism to safeguard male gametophyte development in Arabidopsis

Jian Zhang, Chong Teng, Yan Liang()

PDF(408 KB)
PDF(408 KB)
Protein Cell ›› 2011, Vol. 2 ›› Issue (10) : 837-844. DOI: 10.1007/s13238-011-1102-6
RESEARCH ARTICLE
RESEARCH ARTICLE

Programmed cell death may act as a surveillance mechanism to safeguard male gametophyte development in Arabidopsis

  • Jian Zhang, Chong Teng, Yan Liang()
Author information +
History +

Abstract

Programmed cell death (PCD) plays an important role in plant growth and development as well as in stress responses. During male gametophyte development, it has been proposed that PCD may act as a cellular surveillance mechanism to ensure successful progression of male gametogenesis, and this suicide protective machinery is repressed under favorable growth conditions. However, the regulatory mechanism of male gametophyte-specific PCD remains unknown. Here, we report the use of a TdT-mediated dUTP nick-end labeling-based strategy for genetic screening of Arabidopsis mutants that present PCD phenotype during male gametophyte development. By using this approach, we identified 12 mutants, designated as pcd in male gametogenesis (pig). pig mutants are defective at various stages of male gametophyte development, among which nine pig mutants show a microspore-specific PCD phenotype occurring mainly around pollen mitosis I or the bicellular stage. The PIG1 gene was identified by map-based cloning, and was found to be identical to ATAXIA TELANGIECTASIA MUTATED (ATM), a highly conserved gene in eukaryotes and a key regulator of the DNA damage response. Our results suggest that PCD may act as a general mechanism to safeguard the entire process of male gametophyte development.

Keywords

programmed cell death / male gametophyte / PIG / TdT-mediated dUTP nick-end labeling / ATM

Cite this article

Download citation ▾
Jian Zhang, Chong Teng, Yan Liang. Programmed cell death may act as a surveillance mechanism to safeguard male gametophyte development in Arabidopsis. Prot Cell, 2011, 2(10): 837‒844 https://doi.org/10.1007/s13238-011-1102-6

References

[1] Alexander, M.P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technol 44, 117–122 4181665.
[2] Bakeeva, L.E., Dzyubinskaya, E.V., and Samuilov, V.D. (2005). Programmed cell death in plants: ultrastructural changes in pea guard cells. Biochemistry (Mosc) 70, 972–979 16266266.
[3] Barlow, C., Liyanage, M., Moens, P.B., Deng, C.X., Ried, T., and Wynshaw-Boris, A. (1997). Partial rescue of the prophase I defects of Atm-deficient mice by p53 and p21 null alleles. Nat Genet 17, 462–466 9398851.
[4] Boder, E., and Sedgwick, R.P. (1958). Ataxia-telangiectasia; a familial syndrome of progressive cerebellar ataxia, oculocutaneous telangiectasia and frequent pulmonary infection. Pediatrics 21, 526–554 13542097.
[5] Bursch, W., Ellinger, A., Gerner, C., Fr?hwein, U., and Schulte-Hermann, R. (2000). Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 926, 1–12 11193023.
[6] Carpenter, A.T. (1979). Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma 75, 259–292 119618.
[7] Centerwall, W.R., and Miller, M.M. (1958). Ataxia, telangiectasia, and sinopulmonary infections; a syndrome of slowly progressive deterioration in childhood. AMA J Dis Child 95, 385–396 13507873.
[8] Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and Tissier, A. (2003). AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15, 119–132 12509526.
[9] Gartner, A., Milstein, S., Ahmed, S., Hodgkin, J., and Hengartner, M.O. (2000). A conserved checkpoint pathway mediates DNA damage—induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5, 435–443 10882129.
[10] Gavrieli, Y., Sherman, Y., and Ben-Sasson, S.A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119, 493–501 1400587.
[11] Howden, R., Park, S.K., Moore, J.M., Orme, J., Grossniklaus, U., and Twell, D. (1998). Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149, 621–631 9611178.
[12] Kato, R., and Ogawa, H. (1994). An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res 22, 3104–3112 8065923.
[13] Kuriyama, H., and Fukuda, H. (2002). Developmental programmed cell death in plants. Curr Opin Plant Biol 5, 568–573 12393021.
[14] Lalanne, E., and Twell, D. (2002). Genetic control of male germ unit organization in Arabidopsis. Plant Physiol 129, 865–875 12068125.
[15] Li, N., Zhang, D.S., Liu, H.S., Yin, C.S., Li, X.X., Liang, W.Q., Yuan, Z., Xu, B., Chu, H.W., Wang, J., (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999–3014 17138695.
[16] Lockshin, R.A. (1969). Programmed cell death. Activation of lysis by a mechanism involving the synthesis of protein. J Insect Physiol 15, 1505–1516 5348113.
[17] Lockshin, R.A., and Zakeri, Z. (2004). When cells die II: a comprehensive evaluation of apoptosis and programmed cell death. Hoboken , N.J.: Wiley-Liss.
[18] Lydall, D., Nikolsky, Y., Bishop, D.K., and Weinert, T. (1996). A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383, 840–843 8893012.
[19] Ma, H. (2005). Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56, 393–434 15862102.
[20] McCormick, S. (1993). Male gametophyte development. Plant Cell 5, 1265–1275 12271026.
[21] McCormick, S. (2004). Control of male gametophyte development. Plant Cell 16, S142–S153 15037731.
[22] Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15, 473–497 .
[23] Norbury, C.J., and Zhivotovsky, B. (2004). DNA damage-induced apoptosis. Oncogene 23, 2797–2808 15077143.
[24] Papini, A., Mosti, S., and Brighigna, L. (1999). Programmed-cell-death events during tapetum development of angiosperms. Protoplasma 207, 213–221 .
[25] Pennell, R.I., and Lamb, C. (1997). Programmed cell death in plants. Plant Cell 9, 1157–1168 12237381.
[26] 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 12354970.
[27] Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.-C., Lee, P.Y., Truong, M.T., Beals, T.P., and Goldberg, R.B. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11, 297–322 .
[28] Shi, D.Q., Liu, J., Xiang, Y.H., Ye, D., Sundaresan, V., and Yang, W.C. (2005). SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17, 2340–2354 15980260.
[29] Teng, C., Dong, H., Shi, L., Deng, Y., Mu, J., Zhang, J., Yang, X., and Zuo, J. (2008). Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol 146, 1322–1332 18218968.
[30] Varnier, A.L., Mazeyrat-Gourbeyre, F., Sangwan, R.S., and Clément, C. (2005). Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation. J Struct Biol 152, 118–128 16256370.
[31] 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 16908508.
[32] Williams, J.R., Little, J.B., and Shipley, W.U. (1974). Association of mammalian cell death with a specific endonucleolytic degradation of DNA. Nature 252, 754–755 4474604.
[33] Wyllie, A.H. (1980). Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555–556 6245367.
[34] Yang, X., Makaroff, C.A., and Ma, H. (2003). The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15, 1281–1295 12782723.
[35] Zuo, J., Niu, Q.W., and Chua, N.H. (2000). Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24, 265–273 11069700.
AI Summary AI Mindmap
PDF(408 KB)

Accesses

Citations

Detail

Sections
Recommended

/