Beyond promiscuity: From sexuality to apomixis in flowering plants

  • A. A. Estrada-Luna
  • W. Huanca-Mamani
  • G. Acosta-García
  • G. León-Martínez
  • A. Becerra-Flora
  • R. Pérez-Ruíz
  • Ph. Vielle-Calzada


Little is known about the genetic basis and molecular mechanisms regulating female gametogenesis in flowering plants. In many species sexuality is replaced by apomixis, a method of asexual reproduction that circumvents female meiosis and fertilization, and culminates in the formation of clonal seeds. Using a new generation of transposon based insertional mutagenesis strategies and their resulting molecular tools, we are investigating how female meiotically derived cells (megaspores) acquire their identity. We are also determining their function and interactions, and attempting the induction of apomixis initiation in the ovule of Arabidopsis. This basic knowledge will contribute to establish the transfer of apomixis into sexual crops, a major challenge faced by plant biotechnology. The introduction of apomixis as a reproductive alternative could represent a unique opportunity to simplify breeding schemes and genetically perpetuate any desired heterozygous genotype, including hybrids.

Key words

apomixis female gametophyte enhancer detection gene trapping Arabidopsis 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Asker, S. E.; Jerling, L. Apomixis in plants. Boca Raton, FL: CRC Press; 1992.Google Scholar
  2. Beadle, G. W.; McClintock, B.. A genetic disturbance of meiosis in Zea mays. Science 68:433: 1928.CrossRefPubMedGoogle Scholar
  3. Bell, P. R. Incompatibility in flowering plants: adaptation of an ancient response. Plant Cell 7:5–16; 1995.PubMedCrossRefGoogle Scholar
  4. Bellen, H. J.; O'Kane, C. J.; Wilson, C.; Grossniklaus, U.; Pearson, R. K.; Gehring, W. J.; P-element mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 3:1288–1300; 1989.PubMedGoogle Scholar
  5. Bicknell, R. A. Isolation of a diploid, apomictic plant of Hieracium aurantiacum. Sex. Plant Reprod. 10:168–172; 1997.CrossRefGoogle Scholar
  6. Bretagnolle, F.; Thompson, J. D. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129:1–22; 1995.CrossRefGoogle Scholar
  7. Carman, J. G. Asynchronous expression of duplicate genes in angiosperms may cause apomixes, bispory, tetraspory and polyembryony. J. Linnean Soc. 61:51–94; 1997.CrossRefGoogle Scholar
  8. Carman, J. G.; Crane, C. F.; Rieralizarazu O. Comparative histology of cell walls during meiotic and apomeiotic megasporogenesis in two hexaploid Australasian Elymus species. Crop. Sci. 31(6):1527–1532; 1991.CrossRefGoogle Scholar
  9. Conteau, F.; Belzile, F.; Horlow, C.; Grandjean, O.; Vezon, D.; Doutriaux, M. P. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmel mutant of Arabidopsis. Plant Cell 11(9):1623–1634; 1999.CrossRefGoogle Scholar
  10. D'Amato, F. Polyploidy in cell differentiation. Caryologis 42:183–211; 1989.Google Scholar
  11. De Haan, A.; Maceira, N. O.; Lumaret, R.; Delay, J. Production of 2n gametes in diploid subspecies of Dactylis glomerata L. 2. Occurrence and frequency of 2n eggs. Ann. Bot. 69:345–350; 1992.Google Scholar
  12. Golubovkaya, I. N. Effect of several meiotic mutants on female meiosis in maize. Dev. Genet. 13:411–424; 1992.CrossRefGoogle Scholar
  13. Golubovskaya, I. N.; Avalkin, N. A.; Sheridan, W. F. New insights into the role of the maize ameiotic 1 locus. Genetics 147:1339–1350; 1997.PubMedGoogle Scholar
  14. Golubovskaya, I. N.; Grebennikova, Z. K.; Avalkina, N. A.; Sheridan, W. F. The role of the ameiotic 1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135:1115–1166; 1993.Google Scholar
  15. Golubovskaya, I. N.; Sitnikova, D. V. Three meiotic mutations disturbing chromosome segregation at the first meiotic division in corn. Genetica 16:656–666; 1980.Google Scholar
  16. Grimanelli D.; Leblane, O.; Espinosa, E.; Perotti, R.; De Leon D. G.; Savidan, Y. Mapping diplosporous apomixes in tetrapoid Tripsacum, one gene or several genes. Heredity 80:40–47; 1998.PubMedCrossRefGoogle Scholar
  17. Grossniklaus, U.; Bellen, H. J.; Wilson, C.; Gehring, W. J. P-element mediated enhancer detection applied to the study of oogenesis in Drosophila. Development 107:189–200; 1989.PubMedGoogle Scholar
  18. Grossniklaus, U.; Pearson, R. K.; Gehring, W. J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 6:1030–1051; 1992.PubMedGoogle Scholar
  19. Grossniklaus, U.; Schneitz, K. The molecular and genetic basis of ovule and megagametophyte development. Sem. Cell Dev. Biol. 9:227–238; 1998.CrossRefGoogle Scholar
  20. Gustafsson, Å. Apomixis in angiosperms II. Lunds Univ. Årsskr N F II 43:71–179; 1947.Google Scholar
  21. Harlau, J. R.; de Wet, J. M. J. Pathways of genetic transfer from Tripsacum to Zea mays. Proc. Natl Acad. Sci. USA 74:3494–3497; 1977CrossRefGoogle Scholar
  22. Hermsen, J. G. T. Mechanisms and genetic implications of 2n-gamete formation Iowa State. J. Res. 58:421–434; 1984.Google Scholar
  23. Jongedijk, E. Desynapsis and FDR 2N-megaspore formation in diploid potato: potentials and limitations for breeding and for the induction of diplosporic apomixis. PhD Dissertation, University of Wageningen; 1991:111 pp.Google Scholar
  24. Kimber, G.; Riley, H. Haploid angiosperms. Bot. Rev. 29:480–531; 1963.Google Scholar
  25. Knox, R. B. Apomixis: seasonal and population differences in a grass. Science 157:325–326; 1967.PubMedCrossRefGoogle Scholar
  26. Koltunow, A. M. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437; 1993.PubMedCrossRefGoogle Scholar
  27. Koltunow, A. M.; Soltys, N.; Nobumasa, N.; McClure, S. Anther, ovule, and nucellar embryo development in Citrus sinensis cv Valencia. Can. J. Bot. 73:1567–1582; 1995.Google Scholar
  28. Leblanc, O.; Mazzucato, A. Screening procedures to identify and quantify apomixis. In: Savidan, Y.; Carman, J. G.; Dresselhaus, T., eds., The flowering apomixis: from mechanisms to genetic engineering. Mexico, D.F.: CIMMYT, IRD, European Commission DG VI (FAIR); 2001:121–136.Google Scholar
  29. Leblane, O.; Peel, M. D.; Carman, J. G.; Savidan, Y. Megasporogenesis and megagametogenesis in several Tripsacum species (Poaceae). Am. J. Bot. 82:57–63; 1995.CrossRefGoogle Scholar
  30. Ligrone, R.; Duckett, J. G.; Renzaglia, K. S. The gametophytic-sporophytic junction in land plants. Adv. Bot. Res. 19:231–317; 1993.CrossRefGoogle Scholar
  31. Lin, Y.-G.; Mitzukawa, N.; Oosumi, T.; Whittier, R. F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8:457–463; 1995.CrossRefGoogle Scholar
  32. Maheswari, P. An introduction to the embryology of angiosperms. New York: McGraw-Hill Book Co., Inc.: 1950:453 pp.Google Scholar
  33. Maizonnier, D. Production de tetraploïdes et de trisomiques naturels chez le Pétunia. Ann. d'Amel. Plantes 26:305–318; 1976.Google Scholar
  34. Miller, O. L. Cytological studies of asynaptic maize. Genetics 48:1445–1466; 1963.PubMedGoogle Scholar
  35. Naumova, T. N.; Willemse, M. T. M. Ultrastructural characterization of apospory in Panicum maximum. Sex. Plant Reprod. 8:197–204; 1995.CrossRefGoogle Scholar
  36. Nogler, G. A. Gametophytic apomixis. In: Johri, B. M., ed. Embryology of angiosperms. New York: Springer Verlag: 1984:475–518.Google Scholar
  37. O'Kane, C. J.; Gehring, W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl Acad. Sci USA 85:9123–9127; 1987.CrossRefGoogle Scholar
  38. Parrott, W. A.; Smith, R. R. Production of 2n pollen in red clover. Crop Sci. 24:469–472; 1986.CrossRefGoogle Scholar
  39. Peel, M. D.; Carman, J. G.; Leblane, O. Megasporocyte callose in apomictic buffelgrass Kentucky bluegrass, Pennisetum squamulatum Fresen, Tripsacum L., and weeping lovegrass. Crop Sci. 37:717–723; 1997.CrossRefGoogle Scholar
  40. Rhoades, M. M. Genic control of chromosomal behavior. Maize Genet. Cooperative Newsletter 30:38–42; 1956.Google Scholar
  41. Rhoades, M. M.; Dempsey, E. Induction of chromosome doubling by the elongate gene in maize. Genetics 54:505–522; 1966.PubMedGoogle Scholar
  42. Savidan, Y. Apomixis: genetic and breeding. Plant Breed. Rev. 18:13–86; 2000.Google Scholar
  43. Sheridan, W. F.; Avalkina, N. A.; Shamrov, I.-I.; Batygina T. B.; Golubovskaya, I. N. The macl gene: Controlling the commitment to the meiotic pathway in maize. Genetics 142(3):1009–1020; 1996.PubMedGoogle Scholar
  44. Sheridan, W. F.; Golubeva, E. A.; Abrhamova, L. I.; Golubovskaya, I. The Macl mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–941; 1999.PubMedGoogle Scholar
  45. Siddiqui, I.; Ganesh, G.; Grossniklaus U.; Subbiah, V. The dyad gene is required for progression througth female meiosis in Arabidopsis. Development 127(1):197–207; 2000.Google Scholar
  46. Skarnes, W. C. Entrapment vectors: a new tool for mammalian genetics. Bio/Technology 8:827–831; 1990.PubMedCrossRefGoogle Scholar
  47. Staiger, C. J.; Cande, W. Z. Cytoskeletal analysis of maize meiotic mutants. In: Ormrod, J. C.; Francis, D., eds., Molecular and cell biology of the plant cell cycle. Dordrecht: Kluwer Academic Publishers; 1993: 157–171.Google Scholar
  48. Sumner, M. J.; van Cascele, L. Ovule development in Brassica campestris. A light microscope study. Can. J. Bot. 66:473–476; 1988.CrossRefGoogle Scholar
  49. Sundaresan, V.; Springer, P.; Volpe, T.; Haward, S.; Jones, J. D. G.; Dean, C. Ma, H.; Martienssen, R. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9:1797–1810; 1995.PubMedGoogle Scholar
  50. Veilleux, R. Diploid and polyploid gametes in crop plants: mechanisms of formation and utilization in plant breeding. Plant Breed. Rev. 3:252–288; 1985.Google Scholar
  51. Veronesi, F.; Mariani, A.; Bingham, E. T. Unreduced gametes in diploid Medicago and their importance in alfalfa breeding. Theor. Appl. Genet. 72:37–41; 1986.CrossRefGoogle Scholar
  52. Vielle-Calzada, J.-Ph.; Baskar, R.; Grossniklaus, U. Delayed activation of the paternal genome during seed development. Nature 404:91–94; 2000.PubMedCrossRefGoogle Scholar
  53. Vielle-Calzada, J.-Ph.; Crane, C. F.; Stelly, D. M. Apomixis: the asexual revolution. Science 274:1322–1323; 1996.CrossRefGoogle Scholar
  54. Werner, J. E.; Peloquin, S. J. Frequency and mechanisms of 2n egg formation in haploid tuberosum-wild species F1 hybrids. Am. Potato J. 64:641–654; 1987.Google Scholar
  55. Willemse, M. T. M.; Van Went, J. L. The female gametophyte. In: Johri, B. M., ed. Embryology of angiosperms. New York: Springer Verlag; 1984;159–196.Google Scholar
  56. Willson, C.; Pearson, R. K.; Bellen, H. J.; O'Kane, C. J.; Grossniklaus, U.; Gehring, W. J. P-element mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes. Genes Dev. 3:1301–1313; 1989.Google Scholar
  57. Yang, W. C.; Sundaresan, V. Genetics and gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. 3:53–57; 2000.PubMedCrossRefGoogle Scholar

Copyright information

© Society for In Vitro Biology 2002

Authors and Affiliations

  • A. A. Estrada-Luna
    • 1
  • W. Huanca-Mamani
    • 1
  • G. Acosta-García
    • 1
  • G. León-Martínez
    • 1
  • A. Becerra-Flora
    • 1
  • R. Pérez-Ruíz
    • 1
  • Ph. Vielle-Calzada
    • 1
  1. 1.CINVESTAV-Plant Biotechnology UnitLaboratory of Reproductive Development and ApomixisIrapuato Gto.México

Personalised recommendations