Skip to main content
NCBI home page
Protein & Cell logoLink to Protein & Cell
. 2011 Nov 6;2(10):837–844. doi: 10.1007/s13238-011-1102-6

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

Jian Zhang 1, Chong Teng 1, Yan Liang 1,✉
PMCID: PMC4875295  PMID: 22058038

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 labelingbased 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.

Electronic Supplementary Material

Supplementary material is available for this article at 10.1007/s13238-011-1102-6 and is accessible for authorized users.

Keywords: programmed cell death, male gametophyte, PIG, TdT-mediated dUTP nick-end labeling, ATM

Electronic supplementary material

13238_2011_1102_MOESM1_ESM.pdf (348.8KB, pdf)

Supplementary material, approximately 348 KB.

Footnotes

Electronic Supplementary Material

Supplementary material is available for this article at 10.1007/s13238-011-1102-6 and is accessible for authorized users.

References

  1. Alexander M.P. Differential staining of aborted and nonaborted pollen. Stain Technol. 1969;44:117–122. doi: 10.3109/10520296909063335. [DOI] [PubMed] [Google Scholar]
  2. Bakeeva L.E., Dzyubinskaya E.V., Samuilov V.D. Programmed cell death in plants: ultrastructural changes in pea guard cells. Biochemistry (Mosc) 2005;70:972–979. doi: 10.1007/s10541-005-0211-3. [DOI] [PubMed] [Google Scholar]
  3. Barlow C., Liyanage M., Moens P.B., Deng C.X., Ried T., Wynshaw-Boris A. Partial rescue of the prophase I defects of Atm-deficient mice by p53 and p21 null alleles. Nat Genet. 1997;17:462–466. doi: 10.1038/ng1297-462. [DOI] [PubMed] [Google Scholar]
  4. Boder E., Sedgwick R.P. Ataxia-telangiectasia; a familial syndrome of progressive cerebellar ataxia, oculocutaneous telangiectasia and frequent pulmonary infection. Pediatrics. 1958;21:526–554. [PubMed] [Google Scholar]
  5. Bursch W., Ellinger A., Gerner C., Fröhwein U., Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci. 2000;926:1–12. doi: 10.1111/j.1749-6632.2000.tb05594.x. [DOI] [PubMed] [Google Scholar]
  6. Carpenter A.T. Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma. 1979;75:259–292. doi: 10.1007/BF00293472. [DOI] [PubMed] [Google Scholar]
  7. Centerwall W.R., Miller M.M. Ataxia, telangiectasia, and sinopulmonary infections; a syndrome of slowly progressive deterioration in childhood. AMA J Dis Child. 1958;95:385–396. doi: 10.1001/archpedi.1958.02060050387007. [DOI] [PubMed] [Google Scholar]
  8. Garcia V., Bruchet H., Camescasse D., Granier F., Bouchez D., Tissier A. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell. 2003;15:119–132. doi: 10.1105/tpc.006577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gartner A., Milstein S., Ahmed S., Hodgkin J., Hengartner M. O. A conserved checkpoint pathway mediates DNA damage—induced apoptosis and cell cycle arrest in C. elegans. Mol Cell. 2000;5:435–443. doi: 10.1016/S1097-2765(00)80438-4. [DOI] [PubMed] [Google Scholar]
  10. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992;119:493–501. doi: 10.1083/jcb.119.3.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Howden R., Park S.K., Moore J.M., Orme J., Grossniklaus U., Twell D. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics. 1998;149:621–631. doi: 10.1093/genetics/149.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kato R., Ogawa H. An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 1994;22:3104–3112. doi: 10.1093/nar/22.15.3104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kuriyama H., Fukuda H. Developmental programmed cell death in plants. Curr Opin Plant Biol. 2002;5:568–573. doi: 10.1016/S1369-5266(02)00305-9. [DOI] [PubMed] [Google Scholar]
  14. Lalanne E., Twell D. Genetic control of male germ unit organization in Arabidopsis. Plant Physiol. 2002;129:865–875. doi: 10.1104/pp.003301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  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., et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell. 2006;18:2999–3014. doi: 10.1105/tpc.106.044107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lockshin R.A. Programmed cell death. Activation of lysis by a mechanism involving the synthesis of protein. J Insect Physiol. 1969;15:1505–1516. doi: 10.1016/0022-1910(69)90172-3. [DOI] [PubMed] [Google Scholar]
  17. Lockshin R.A., Zakeri Z. When cells die II: a comprehensive evaluation of apoptosis and programmed cell death. Hoboken, N.J.: Wiley-Liss; 2004. [Google Scholar]
  18. Lydall D., Nikolsky Y., Bishop D.K., Weinert T. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature. 1996;383:840–843. doi: 10.1038/383840a0. [DOI] [PubMed] [Google Scholar]
  19. Ma H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol. 2005;56:393–434. doi: 10.1146/annurev.arplant.55.031903.141717. [DOI] [PubMed] [Google Scholar]
  20. McCormick S. Male gametophyte development. Plant Cell. 1993;5:1265–1275. doi: 10.1105/tpc.5.10.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McCormick S. Control of male gametophyte development. Plant Cell. 2004;16:S142–S153. doi: 10.1105/tpc.016659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Murashige T., Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant. 1962;15:473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x. [DOI] [Google Scholar]
  23. Norbury C.J., Zhivotovsky B. DNA damage-induced apoptosis. Oncogene. 2004;23:2797–2808. doi: 10.1038/sj.onc.1207532. [DOI] [PubMed] [Google Scholar]
  24. Papini A., Mosti S., Brighigna L. Programmed-celldeath events during tapetum development of angiosperms. Protoplasma. 1999;207:213–221. doi: 10.1007/BF01283002. [DOI] [Google Scholar]
  25. Pennell R.I., Lamb C. Programmed cell death in plants. Plant Cell. 1997;9:1157–1168. doi: 10.1105/tpc.9.7.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Regan S.M., Moffatt B.A. Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. Plant Cell. 1990;2:877–889. doi: 10.1105/tpc.2.9.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sanders P.M., Bui A.Q., Weterings K., McIntire K.N., Hsu Y.-C., Lee P.Y., Truong M.T., Beals T.P., Goldberg R.B. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod. 1999;11:297–322. doi: 10.1007/s004970050158. [DOI] [Google Scholar]
  28. Shi D.Q., Liu J., Xiang Y.H., Ye D., Sundaresan V., Yang W.C. SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell. 2005;17:2340–2354. doi: 10.1105/tpc.105.033563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Teng C., Dong H., Shi L., Deng Y., Mu J., Zhang J., Yang X., Zuo J. Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol. 2008;146:1322–1332. doi: 10.1104/pp.107.113506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Varnier A.L., Mazeyrat-Gourbeyre F., Sangwan R.S., Clément C. 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. 2005;152:118–128. doi: 10.1016/j.jsb.2005.07.011. [DOI] [PubMed] [Google Scholar]
  31. Vizcay-Barrena G., Wilson Z.A. Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J Exp Bot. 2006;57:2709–2717. doi: 10.1093/jxb/erl032. [DOI] [PubMed] [Google Scholar]
  32. Williams J.R., Little J.B., Shipley W.U. Association of mammalian cell death with a specific endonucleolytic degradation of DNA. Nature. 1974;252:754–755. doi: 10.1038/252754a0. [DOI] [PubMed] [Google Scholar]
  33. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980;284:555–556. doi: 10.1038/284555a0. [DOI] [PubMed] [Google Scholar]
  34. Yang X., Makaroff C.A., Ma H. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell. 2003;15:1281–1295. doi: 10.1105/tpc.010447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zuo J., Niu Q.W., Chua N.H. Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 2000;24:265–273. doi: 10.1046/j.1365-313x.2000.00868.x. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

13238_2011_1102_MOESM1_ESM.pdf (348.8KB, pdf)

Supplementary material, approximately 348 KB.

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES