Skip to main content
SpringerLink
Log in

Androgenesis Revisited

  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

Androgenesis can be defined as the set of biological processes leading to an individual genetically coming exclusively from a male nucleus. Androgenesis was traditionally considered as the spontaneous, in vivo development of a male-derived haploid embryo from a fertilized egg where the female nucleus is eliminated. However, at present it is also possible to generate androgenic haploids/doubled haploids through in vitro microspore embryogenesis and by in vitro meiocyte-derived callogenesis. These three androgenic alternatives clearly differ in the inducible stage, but lead to the same final haploid or doubled haploid product. Whereas microspore embryogenesis is widely studied and applied, the other two routes are much less known. In this paper, the evidence accounting for the existence of these three alternative pathways is revised, as well as the mechanisms potentially involved in their induction. Their differences and similarities are discussed from a biological perspective, leading to the notion that they might represent an ancient survival mechanism triggered by similar factors.

Resumen

La androgénesis se define como el conjunto de vías biológicas que dan lugar a un individuo cuyo fondo genético proviene exclusivamente de un núcleo de origen masculino. Tradicionalmente, el concepto de androgénesis estaba restringido al desarrollo espontáneo, in vivo, de un embrión haploide o doble haploide a partir de una célula huevo fecundada en la que el material genético de origen femenino era inactivado o eliminado. Sin embargo, hoy en día sabemos que existen otras vías para conseguir haploides o doble haploides androgénicos, mediante embriogénesis de microsporas y mediante la formación de callos derivados de meiocitos. Estas tres alternativas androgénicas difieren claramente en la etapa en la que es posible la inducción, pero dan lugar al mismo producto haploide o doble haploide final. Mientras que la embriogénesis de microsporas es un fenómeno ampliamente estudiado y de clara aplicación práctica, las otras dos rutas son mucho menos conocidas. En este trabajo se revisan las evidencias existentes al respecto de estas tres alternativas androgénicas, así como los mecanismos potencialmente implicados en su inducción. También se discuten sus diferencias y semejanzas, desde un punto de vista biológico, para llegar a la hipótesis de que estas rutas podrían representar un mecanismo atávico de supervivencia activado por factores similares.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Literature Cited

  • Aionesei, T., A. Touraev & E. Heberle-Bors. 2005. Pathways to microspore embryogenesis. Pp 11–34. In: C. E. Palmer, W. A. Keller, & K. J. Kasha (eds). Haploids in crop improvement II, vol.56. Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • Andersen, S. B. 2005. Haploids in the improvement of woody species. Pp 243–257. In: C. E. Palmer, W. A. Keller, & K. J. Kasha (eds). Haploids in crop improvement II, vol. 56. Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • Ari, E., S. Buyukalaca, K. Abak & S. Cetiner. 2007. Callus initiation for indirect pollen embryogenesis in Anemone coronaria. Proceedings of the 22nd International Eucarpia Symposium Section Ornamentals: Breeding for Beauty, Pt II 743: 87–90.

    CAS  Google Scholar 

  • Bal, U. & K. Abak. 2007. Haploidy in tomato (Lycopersicon esculentum Mill.): A critical review. Euphytica 158: 1–9.

    Google Scholar 

  • Baldursson, S., P. Krogstrup, J. V. Norgaard & S. B. Andersen. 1993. Microspore embryogenesis in anther culture of 3 species of Populus and regeneration of dihaploid plants of Populus trichocarpa. Canadian Journal of Forest Research-Revue Canadienne de Recherche Forestiere 23: 1821–1825.

    Google Scholar 

  • Beckert, M. 1998. Genetic analysis of in vitro androgenetic response in maize. Pp 24–37. In: Y. Chupeau, M. Caboche, & Y. Henry (eds). Androgenesis and haploid plants. Springer-Verlag, Berlin, Heidelberg.

    Google Scholar 

  • Belicuas, P. R., C. T. Guimaraes, L. V. Paiva, J. M. Duarte, W. R. Maluf & E. Paiva. 2007. Androgenetic haploids and SSR markers as tools for the development of tropical maize hybrids. Euphytica 156: 95–102.

    CAS  Google Scholar 

  • Belmonte, M. F., S. J. Ambrose, A. R. S. Ross, S. R. Abrams & C. Stasolla. 2006. Improved development of microspore-derived embryo cultures of Brassica napus cv Topas following changes in glutathione metabolism. Physiologia Plantarum 127: 690–700.

    CAS  Google Scholar 

  • Binarova, P., G. Hause, V. Cenklova, J. H. G. Cordewener & M. M. van Lookeren-Campagne. 1997. A short severe heat shock is required to induce embryogenesis in late bicellular pollen of Brassica napus L. Sexual Plant Reproduction 10: 200–208.

    Google Scholar 

  • Bohanec, B. 2009. Doubled haploids via gynogenesis. Pp 35–46. In: A. Touraev, B. P. Forster, & S. M. Jain (eds). Advances in haploid production in higher plants. Springer, Dordrecht.

    Google Scholar 

  • Borderies, G., M. le Bechec, M. Rossignol, C. Lafitte, E. Le Deunff, M. Beckert, C. Dumas & E. Matthys-Rochon. 2004. Characterization of proteins secreted during maize microspore culture: Arabinogalactan proteins (AGPs) stimulate embryo development. European Journal of Cell Biology 83: 205–212.

    PubMed  CAS  Google Scholar 

  • Bouharmont, J. 1977. Cytology of microspores and calli after anther culture in Hordeum vulgare. Caryologia 30: 351–360.

    Google Scholar 

  • Boutilier, K., M. Fiers, C. M. Liu & A. H. M. Van der Geest. 2005. Biochemical and molecular aspects of haploid embryogenesis. Pp 73–95. In: C. E. Palmer, W. A. Keller, & K. J. Kasha (eds). Haploids in crop improvement II, vol. 56. Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • Burk, L. G. 1962. Haploids in genetically marked progenies of tobacco. Journal of Heredity 53: 222–225.

    Google Scholar 

  • Campos, F. F. & D. T. J. Morgan. 1958. Haploid pepper from a sperm. Journal of Heredity 49: 135–137.

    Google Scholar 

  • Chase, S. S. 1963. Androgenesis—Its use for transfer of maize cytoplasm. Journal of Heredity 54: 152–158.

    Google Scholar 

  • ———. 1969. Monoploids and monoploid—derivatives of maize (Zea mays L.). Botanical Review 35: 117–167.

    Google Scholar 

  • Chen, C. C., K. J. Kasha & A. Marsolais. 1984. Segmentation patterns and mechanisms of genome multiplication in cultured microspores of barley. Canadian Journal of Genetics and Cytology 26: 475–483.

    Google Scholar 

  • Chen, L. J., X. Y. Zhu, L. Gu & B. Wu. 2005. Efficient callus induction and plant regeneration from anther of Chinese narcissus (Narcissus tazetta L. var. chinensis Roem). Plant Cell Reports 24: 401–407.

    PubMed  CAS  Google Scholar 

  • Chupeau, Y., M. Caboche & Y. Henry. 1998. Androgenesis and haploid plants. Springer-Verlag, Berlin, Heidelberg.

    Google Scholar 

  • Clausen, R. E. & W. E. Lammerts. 1929. Interspecific hybridisation in Nicotiana. X. Haploid and diploid merogony. The American Naturalist. 43: 279–282.

    Google Scholar 

  • Cordewener, J. H. G., G. Hause, E. Görgen, R. Busink, B. Hause, H. J. M. Dons, A. A. M. van Lammeren, M. M. van Lookeren-Campagne & P. Pechan. 1995. Changes in synthesis and localization of members of the 70-kDa class of heat-shock proteins accompany the induction of embryogenesis in Brassica napus L. microspores. Planta 196: 747–755.

    CAS  Google Scholar 

  • Corduan, G. & C. Spix. 1975. Haploid callus and regeneration of plants from anthers of Digitalis purpurea L. Planta 124: 1–11.

    Google Scholar 

  • Coronado, M. J., P. Gonzalez-Melendi, J. M. Segui, C. Ramirez, I. Barany, P. S. Testillano & M. C. Risueno. 2002. MAPKs entry into the nucleus at specific interchromatin domains in plant differentiation and proliferation processes. Journal of Structural Biology 140: 200–213.

    PubMed  CAS  Google Scholar 

  • Corral-Martínez, P., F. Nuez & J. M. Seguí-Simarro. In press. In: D. Thangadurai (ed). Molecular agrobiology. Bentham Science Publishers, USA.

    Google Scholar 

  • Dao, N. T. & Z. B. Shamina. 1978. Cultivation of isolated tomato anthers. Soviet Plant Physiology 25: 120–126.

    Google Scholar 

  • de Fossard, R. A. 1974a. Methods for producing haploids. Pp 145–150. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • ———. 1974b. Terminology in “Haploid” research. Pp 403–410. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • De Maine, M. J. 2003. Potato haploid technologies. Pp 241–247. In: M. Maluszynski, K. J. Kasha, B. P. Forster, & I. Szarejko (eds). Doubled haploid production in crop plants. A manual. Kluwer Academic Publishers, Dordretch, the Netherlands.

    Google Scholar 

  • Devaux, P. 2003. The Hordeum bulbosum (L.) method. Pp 15–19. In: M. Maluszynski, K. J. Kasha, B. P. Forster, & I. Szarejko (eds). Doubled haploid production in crop plants. A manual. Kluwer Academic Publishers, Dordretch, the Netherlands.

    Google Scholar 

  • Dumas de Vaulx, R. & D. Chambonnet. 1982. Culture in vitro d’anthères d’aubergine (Solanum melongena L.): Stimulation de la production de plantes au moyen de traitements à 35°C associés à de faibles teneurs en substances de croissance. Agronomie 2: 983–988.

    Google Scholar 

  • Dunwell, J. M. 2010. Haploids in flowering plants: origins and exploitation. Plant Biotechnology Journal 8:377–424.

    PubMed  CAS  Google Scholar 

  • Ecochard, R., G. Merkx & M. Matteoli. 1974. Parthenogenesis induced by specific radioinactivation of the male gametes. Pp 136. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Ehrensberger, R. 1948. Versuche zur auslösung von haploidie bei Blütenpflanzen. Biologisches Zentralblatt 67: 537–546.

    Google Scholar 

  • Evans, M. 2005. New nucleic acid molecule encoding indeterminate gametophyte 1, useful for producing male sterility and for generating androgenetic progeny in plant species. Carnegie Inst Washington, USA, Patent no. US2005198711-A1.

  • Evans, M. M. S. 2007. The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19: 46–62.

    PubMed  CAS  Google Scholar 

  • Evans, M. 2009. New isolated polypeptide or protein comprises the amino acid sequence of indeterminate gametophyte 1 (IG1) from Zea mays, useful for identifying and isolating an ortholog of ig1 in a non-Zea mays plant species. Carnegie Inst Washington, USA, Patent no. US2009151025-A1.

  • Evans, J. M. & N. P. Batty. 1994. Ethylene precursors and antagonists increase embryogenesis of Hordeum vulgare L anther culture. Plant Cell Reports 13: 676–678.

    CAS  Google Scholar 

  • Ferrie, A. M. R., D. J. Epp & W. A. Keller. 1995. Evaluation of Brassica rapa L. genotypes for microspore culture response and identification of a highly embryogenic line. Plant Cell Reports 14: 580–584.

    CAS  Google Scholar 

  • Forster, B. P., E. Heberle-Bors, K. J. Kasha & A. Touraev. 2007. The resurgence of haploids in higher plants. Trends in Plant Science 12: 368–375.

    PubMed  CAS  Google Scholar 

  • Gémes Juhász, A. & M. Jakse. 2005. Haploids in the improvement of miscellaneous crop species (Cucurbitaceae, Liliaceae, Asparagaceae, Chenopodiaceae, Araceae and Umbelliferae). Pp 259–276. In: C. E. Palmer, W. A. Keller, & K. J. Kasha (eds). Haploids in crop improvement II. Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • Gerassimova, H. 1936. Experimentally produced haploid plant in Crepis tectorum. Biologitcheski Journal 5: 895–900.

    Google Scholar 

  • Germana, M. 2006. Doubled haploid production in fruit crops. Plant Cell Tissue and Organ Culture 86: 131–146.

    Google Scholar 

  • Gerrish, E. E. 1956. Studies od the monoploid method of producing homozigous diploids in Zea mays. Ph.D. Thesis. University of Minnesota, Minneapolis.

  • Gonzalez-Medina, M. & J. Bouharmont. 1978. Experiments on anther culture in barley—Influence of culture methods on cell proliferation and organ differentiation. Euphytica 27: 553–559.

    Google Scholar 

  • Goodsell, S. F. 1961. Male sterility in corn by androgenesis. Crop Science 1: 227–228.

    Google Scholar 

  • Gresshoff, P. M. & C. H. Doy. 1972a. Development and differentiation of haploid Lycopersicon esculentum (tomato). Planta 107: 161–170.

    Google Scholar 

  • ——— & ———. 1972b. Haploid Arabidopsis thaliana callus and plants from anther culture. Australian Journal of Biological Sciences 25: 259.

    Google Scholar 

  • ——— & ———. 1974. Derivation of a haploid cell line from Vitis vinifera and importance of stage of meiotic development of anthers for haploid culture of this and other genera. Zeitschrift Fur Pflanzenphysiologie 73: 132–141.

    Google Scholar 

  • Guha, S. & S. C. Maheshwari. 1964. In vitro production of embryos from anthers of Datura. Nature 204: 497.

    Google Scholar 

  • Gulshan, T. M. V. & D. R. Sharma. 1981. Studies on anther cultures of tomato—Lycopersicon esculentum Mill. Biologia Plantarum 23: 414–420.

    Google Scholar 

  • Guo, F. L., B. Q. Huang, Y. Z. Han & S. Y. Zee. 2004. Fertilization in maize indeterminate gametophyte1 mutant. Protoplasma 223: 111–120.

    PubMed  Google Scholar 

  • Han, D. S., Y. Niimi & M. Nakano. 2000. Formation of calli from isolated microspore cultures of Asiatic hybrid lily ‘Connecticut King’. Journal of the Japanese Society for Horticultural Science 69: 52–56.

    CAS  Google Scholar 

  • Hayes, P., A. Corey & J. DeNoma. 2003. Doubled haploid production in barley using the Hordeum bulbosum (L.) technique. Pp 5–14. In: M. Maluszynski, K. J. Kasha, B. P. Forster, & I. Szarejko (eds). Doubled haploid production in crop plants. A manual. Kluwer Academic Publishers, Dordretch, the Netherlands.

    Google Scholar 

  • Hays, D. B., R. W. Wilen, C. Sheng, M. M. Moloney & R. P. Pharis. 1999. Embryo-specific gene expression in microspore-derived embryos of Brassica napus. An interaction between abscisic acid and jasmonic acid. Plant Physiology 119: 1065–1072.

    PubMed  Google Scholar 

  • ———, D. M. Reid, E. C. Yeung & R. P. Pharis. 2000. Role of ethylene in cotyledon development of microspore-derived embryos of Brassica napus. Journal of Experimental Botany 51: 1851–1859.

    PubMed  CAS  Google Scholar 

  • ———, R. M. Mandel & R. P. Pharis. 2001. Hormones in zygotic and microspore embryos of Brassica napus. Plant Growth Regulation 35: 47–58.

    CAS  Google Scholar 

  • ———, E. C. Yeung & R. P. Pharis. 2002. The role of gibberellins in embryo axis development. Journal of Experimental Botany 53: 1747–1751.

    PubMed  CAS  Google Scholar 

  • Holm, P. B., S. Knudsen, P. Mouritzen, D. Negri, F. L. Olsen & C. Roue. 1994. Regeneration of fertile barley plants from mechanically isolated protoplasts of the fertilized egg cell. Plant Cell 6: 531–543.

    PubMed  CAS  Google Scholar 

  • Honys, D. & D. Twell. 2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology 5: R85.

    PubMed  Google Scholar 

  • Hosp, J., S. D. F. Maraschin, A. Touraev & K. Boutilier. 2007a. Functional genomics of microspore embryogenesis. Euphytica 158: 275–285.

    Google Scholar 

  • ———, A. Tashpulatov, U. Roessner, E. Barsova, H. Katholnigg, R. Steinborn, B. Melikant, S. Lukyanov, E. Heberle-Bors & A. Touraev. 2007b. Transcriptional and metabolic profiles of stress-induced, embryogenic tobacco microspores. Plant Molecular Biology 63: 137–149.

    PubMed  CAS  Google Scholar 

  • Huang, B. Q. & W. F. Sheridan. 1996. Embryo sac development in the maize indeterminate gametophyte1 mutant: Abnormal nuclear behavior and defective microtubule organization. Plant Cell 8: 1391–1407.

    PubMed  CAS  Google Scholar 

  • Illies, Z. M. 1974. Induction of haploid parthenogenesis in Populus tremula by male gametes incativated with toluidine blue. Pp 136. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Ivanov, M. A. 1938. Experimental production of haploids in Nicotiana rustica L. Genetica 20: 295–386.

    Google Scholar 

  • Janick, J. & H. G. Hughes. 1974. Production of strawberry tetrahaploids from intergeneric crosses. Pp 137. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Joosen, R., J. Cordewener, E. D. J. Supena, O. Vorst, M. Lammers, C. Maliepaard, T. Zeilmaker, B. Miki, T. America, J. Custers & K. Boutilier. 2007. Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiology 144: 155–172.

    PubMed  CAS  Google Scholar 

  • Kasha, K. J. & K. N. Kao. 1970. High frequency haploid production in barley (Hordeum vulgare L.). Nature 225: 874–876.

    PubMed  CAS  Google Scholar 

  • Kehr, A. E. 1951. Monoploidy in Nicotiana. Journal of Heredity 42: 107–112.

    PubMed  CAS  Google Scholar 

  • Kermicle, J. L. 1969. Androgenesis conditioned by a mutation in maize. Science 166: 1422–1424.

    PubMed  CAS  Google Scholar 

  • ———. 1971. Pleiotropic effects on seed development of the indeterminate gametophyte gene in maize. American Journal of Botany 58: 1–7.

    Google Scholar 

  • ———. 1974. Origin of androgenetic haploids and diploids induced by the indeterminate gametophyte (ig) mutation in maize. Pp 137. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • ———. 1994. Indeterminate gametophyte (ig): Biology and use. Pp 388–393. In: M. Freeling & V. Walbot (eds). The maize handbook. Springer-Verlag, New York.

    Google Scholar 

  • Kim, M., J. Kim, M. Yoon, D.-I. Choi & K.-M. Lee. 2004. Origin of multicellular pollen and pollen embryos in cultured anthers of pepper (Capsicum annuum). Plant Cell, Tissue and Organ Culture 77: 63–72.

    CAS  Google Scholar 

  • ———, I.-C. Jang, J.-A. Kim, E.-J. Park, M. Yoon & Y. Lee. 2008. Embryogenesis and plant regeneration of hot pepper (Capsicum annuum L.) through isolated microspore culture. Plant Cell Reports 27: 425–434.

    PubMed  CAS  Google Scholar 

  • Kindiger, B. & S. Hamann. 1993. Generation of haploids in maize—A modification of the indeterminate gametophyte (ig) system. Crop Science 33: 342–344.

    Article  Google Scholar 

  • Kiviharju, E., M. Puolimatka, M. Saastamoinen, S. Hovinen & E. Pehu. 1998. The effect of genotype on anther culture response of cultivated and wild oats. Agricultural and Food Science in Finland 7: 409–422.

    Google Scholar 

  • Komen, H. & G. H. Thorgaard. 2007. Androgenesis, gynogenesis and the production of clones in fishes: A review. Aquaculture 269: 150–173.

    Google Scholar 

  • Komma, D. J. & S. A. Endow. 1995. Haploidy and androgenesis in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 92: 11884–11888.

    PubMed  CAS  Google Scholar 

  • Kostoff, D. 1929. An androgenic Nicotiana haploid. Zeitschrift fur Zellforschung 9: 640–642.

    Google Scholar 

  • ———. 1942. The problem of haploidy (Cytogenetic studies in Nicotiana haploids and their bearing on some other cytogenetic problems). Bibliographia Genetica 13: 1–148.

    Google Scholar 

  • Koul, A. K. & J. L. Karihaloo. 1977. In vivo embryoids from anthers of Narcissus biflorus Curt. Euphytica 26: 97–102.

    Google Scholar 

  • Kumlehn, J., H. Lorz & E. Kranz. 1998. Differentiation of isolated wheat zygotes into embryos and normal plants. Planta 205: 327–333.

    CAS  Google Scholar 

  • Lacadena, J. R. 1974. Spontaneous and induced parthenogenesis and androgenesis. Pp 13–32. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Letarte, J., E. Simion, M. Miner & K. J. Kasha. 2006. Arabinogalactans and arabinogalactan-proteins induce embryogenesis in wheat (Triticum aestivum L.) microspore culture. Plant Cell Reports 24: 691–698.

    PubMed  CAS  Google Scholar 

  • Levenko, B. A., V. A. Kunakh & G. N. Yurkova. 1977. Studies on callus tissue from anthers.1. Tomato. Phytomorphology 27: 377–383.

    Google Scholar 

  • Li, J. Q., Y. Q. Wang, L. H. Lin, L. J. Zhou, N. Luo, Q. X. Deng, J. R. Xian, C. X. Hou & Y. Qiu. 2008. Embryogenesis and plant regeneration from anther culture in loquat (Eriobotrya japonica L.). Scientia Horticulturae 115: 329–336.

    CAS  Google Scholar 

  • Lin, B. Y. 1978. Structural modifications of female gametophyte associated with indeterminate-gametophyte (ig) mutant in maize. Canadian Journal of Genetics and Cytology 20: 249–257.

    Google Scholar 

  • ———. 1981. Megagametogenetic alterations associated with the indeterminate gametophyte (ig) mutation in maize. Revista Brasileira de Biologia 41: 557–563.

    Google Scholar 

  • ———. 1984. Ploidy barrier to endosperm development in maize. Genetics 107: 103–115.

    PubMed  CAS  Google Scholar 

  • Liu, J., X. Xu & X. Deng. 2005. Intergeneric somatic hybridization and its application to crop genetic improvement. Plant Cell, Tissue and Organ Culture 82: 19–44.

    CAS  Google Scholar 

  • Ma, R., Y. D. Guo & S. Pulli. 2004. Comparison of anther and microspore culture in the embryogenesis and regeneration of rye (Secale cereale). Plant Cell Tissue and Organ Culture 76: 147–157.

    Google Scholar 

  • Magnard, J. L., E. Le Deunff, J. Domenech, P. M. Rogowsky, P. S. Testillano, M. Rougier, M. C. Risueño, P. Vergne & C. Dumas. 2000. Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Molecular Biology 44: 559–574.

    PubMed  CAS  Google Scholar 

  • Malik, M. R., F. Wang, J. M. Dirpaul, N. Zhou, P. L. Polowick, A. M. R. Ferrie & J. E. Krochko. 2007. Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiology 144: 134–154.

    PubMed  CAS  Google Scholar 

  • ———, ———, J. Dirpaul, N. Zhou, J. Hammerlindl, W. Keller, S. R. Abrams, A. M. R. Ferrie & J. E. Krochko. 2008. Isolation of an embryogenic line from non-embryogenic Brassica napus cv. Westar through microspore embryogenesis. Journal of Experimental Botany 59: 2857–2873.

    PubMed  CAS  Google Scholar 

  • Mallikarjuna, N., D. Jadhav, H. Clarke, C. Coyne & F. Muehlbauer. 2005. Induction of androgenesis as a consequence of wide crossing in chickpea. International Chickpea and Pigeonpea Newsletter 12: 12–15.

    Google Scholar 

  • Maluszynski, M., K. J. Kasha, B. P. Forster & I. Szarejko. 2003a. Doubled haploid production in crop plants. A manual. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • ———, ——— & I. Szarejko. 2003b. Published doubled haploid protocols in plant species. Pp 309–335. In: M. Maluszynski, K. J. Kasha, B. P. Forster, & I. Szarejko (eds). Doubled haploid production in crop plants. A manual. Kluwer Academic Publishers, Dordretch, the Netherlands.

    Google Scholar 

  • Mantovani, B. & V. Scali. 1992. Hybridogenesis and androgenesis in the stick insect Bacillus rossius grandii benazzi (Insecta, Phasmatoidea). Evolution 46: 783–796.

    Google Scholar 

  • Maraschin, S. F., W. de Priester, H. P. Spaink & M. Wang. 2005. Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. Journal of Experimental Botany 56: 1711–1726.

    PubMed  CAS  Google Scholar 

  • Maraschin, S. D. F., M. Caspers, E. Potokina, F. Wulfert, A. Graner, H. P. Spaink & M. Wang. 2006. CDNA array analysis of stress-induced gene expression in barley androgenesis. Physiologia Plantarum 127: 535–550.

    CAS  Google Scholar 

  • Massonneau, A., M. J. Coronado, A. Audran, A. Bagniewska, R. Mol, P. S. Testillano, G. Goralski, C. Dumas, M. C. Risueño & E. Matthys-Rochon. 2005. Multicellular structures developing during maize microspore culture express endosperm and embryo-specific genes and show different embryogenic potentialities. European Journal of Cell Biology 84: 663–675.

    PubMed  CAS  Google Scholar 

  • McKone, M. J. & S. L. Halpern. 2003. The evolution of androgenesis. American Naturalist 161: 641–656.

    PubMed  Google Scholar 

  • Miyoshi, K. 1996. Callus induction and plantlet formation through culture of isolated microspores of eggplant (Solanum melongena L). Plant Cell Reports 15: 391–395.

    CAS  Google Scholar 

  • Muñoz-Amatriain, M., J. T. Svensson, A. M. Castillo, L. Cistue, T. J. Close & M. P. Valles. 2006. Transcriptome analysis of barley anthers: Effect of mannitol treatment on microspore embryogenesis. Physiologia Plantarum 127: 551–560.

    Google Scholar 

  • Myint, A. & R. A. de Fossard. 1974. Induction of haploid callus from rice anthers and regeneration of plants. Pp 139. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Naess, S. K., H. J. Swartz & G. R. Bauchan. 1998. Ploidy reduction in blackberry. Euphytica 99: 57–73.

    Google Scholar 

  • Nontaswatsri, C., S. Ruamrungsri & S. Fukai. 2008. Callus induction and plant regeneration of Dianthus chinensis L. and Dianthus barbatus L. via Anther Culture. Proceedings of the International Workshop on Ornamental Plants 788: 109–114.

    CAS  Google Scholar 

  • Paire, A., P. Devaux, C. Lafitte, C. Dumas & E. Matthys-Rochon. 2003. Proteins produced by barley microspores and their derived androgenic structures promote in vitro zygotic maize embryo formation. Plant Cell Tissue and Organ Culture 73: 167–176.

    CAS  Google Scholar 

  • Palmer, C. E., W. A. Keller & K. J. Kasha. 2005. Haploids in crop improvement II. Springer-Verlag, Berlin.

    Google Scholar 

  • Pandey, K. K. 1973. Theory and practice of induced androgenesis. New Phytologist 72: 1129–1140.

    Google Scholar 

  • Pauls, K. P., J. Chan, G. Woronuk, D. Schulze & J. Brazolot. 2006. When microspores decide to become embryos—cellular and molecular changes. Canadian Journal of Botany-Revue Canadienne De Botanique 84: 668–678.

    CAS  Google Scholar 

  • Picard, E., J. De Buyser & J. Bozza. 1974. Production of haploid plants by anther culture of wheat. Pp 143. In: K. J. Kasha (ed). Haploids in higher plants: Advances and potential. University of Guelph, Guelph, Canada.

    Google Scholar 

  • Piccirilli, M. & S. Arcioni. 1991. Haploid plants regenerated via anther culture in wild barley (Hordeum spontaneum c-kock). Plant Cell Reports 10: 273–276.

    Google Scholar 

  • Pulido, A., A. Hernando, F. Bakos, E. Mendez, M. Devic, B. Barnabas & A. Olmedilla. 2006. Hordeins are expressed in microspore-derived embryos and also during male gametophytic and very early stages of seed development. Journal of Experimental Botany 57: 2837–2846.

    PubMed  CAS  Google Scholar 

  • Raghavan, V. 1986. Polen embryogenesis. Pp 152–189. In: P. W. Barlow, P. V. Green, & C. C. Wylie (eds). Embryogenesis in angiosperms, a developmental and experimental study. Cambridge University Press, London.

    Google Scholar 

  • Ramanna, M. S. & J. G. T. Hermsen. 1974. Embryoid formation in anthers of some interspecific hybrids in Solanum. Euphytica 23: 423–427.

    Google Scholar 

  • Ramesar-Fortner, N. S. & E. C. Yeung. 2006. Physiological influences in the development and function of the shoot apical meristem of microspore-derived embryos of Brassica napus ‘Topas’. Canadian Journal of Botany-Revue Canadienne De Botanique 84: 371–383.

    CAS  Google Scholar 

  • Razdan, M. K. 2003. Introduction to plant tissue culture. Science Publishers, Inc., Enfield, New Hampshire, USA.

    Google Scholar 

  • Reynolds, T. L. 1997. Pollen embryogenesis. Plant Molecular Biology 33: 1–10.

    PubMed  CAS  Google Scholar 

  • ——— & R. L. Crawford. 1996. Changes in abundance of an abscisic acid-responsive, early cysteine-labeled metallothionein transcript during pollen embryogenesis in bread wheat (Triticum aestivum). Plant Molecular Biology 32: 823–829.

    PubMed  CAS  Google Scholar 

  • Rieger, R. A., A. Michaelis & M. M. Green. 1968. A glossary of genetics and cytogenetics. Springer-Verlag, New York.

    Google Scholar 

  • Rudolf, K., B. Bohanec & M. Hansen. 1999. Microspore culture of white cabbage, Brassica oleracea var. capitata L.: Genetic improvement of non-responsive cultivars and effect of genome doubling agents. Plant Breeding 118: 237–241.

    CAS  Google Scholar 

  • Seaney, R. R. 1955. Studies on monoploidy in maize. Ph.D. Thesis. Cornell University, Ithaca, New York.

  • Seguí-Simarro, J. M. & F. Nuez. 2005. Meiotic metaphase I to telophase II is the most responsive stage of microspore development for induction of androgenesis in tomato (Solanum Lycopersicum). Acta Physiologiae Plantarum 27: 675–685.

    Google Scholar 

  • ——— & ———. 2006. Androgenesis induction from tomato anther cultures: Callus characterization. Pp 855–861. In: M. G. Fári, I. Holb, & G. D. Bisztray (eds). Acta Horticulturae, no. 725. ISHS, Debrecen, Hungary.

    Google Scholar 

  • ——— & ———. 2007. Embryogenesis induction, callogenesis, and plant regeneration by in vitro culture of tomato isolated microspores and whole anthers. Journal of Experimental Botany 58: 1119–1132.

    PubMed  Google Scholar 

  • ——— & ———. 2008a. How microspores transform into haploid embryos: changes associated with embryogenesis induction and microspore-derived embryogenesis. Physiologia Plantarum 134: 1–12.

    PubMed  Google Scholar 

  • ——— & ———. 2008b. Pathways to doubled haploidy: chromosome doubling during androgenesis. Cytogenetic and Genome Research 120: 358–369.

    PubMed  Google Scholar 

  • ———, P. S. Testillano & M. C. Risueño. 2003. Hsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus L. cv Topas. Journal of Structural Biology 142: 379–391.

    PubMed  Google Scholar 

  • ———, ——— & ———. 2005. MAP kinases are developmentally regulated during stress-induced microspore embryogenesis in Brassica napus L. Histochemistry and Cell Biology 123: 541–551.

    PubMed  Google Scholar 

  • Shariatpanahi, M. E., U. Bal, E. Heberle-Bors & A. Touraev. 2006. Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiologia Plantarum 127: 519–534.

    CAS  Google Scholar 

  • Shivanna, K. R. & B. M. Johri. 1985. The angiosperm pollen. Structure and function. Wiley Eastern Limited, New Delhi, India.

    Google Scholar 

  • Shtereva, L. A., N. A. Zagorska, B. D. Dimitrov, M. M. Kruleva & H. K. Oanh. 1998. Induced androgenesis in tomato (Lycopersicon esculentum Mill). II. Factors affecting induction of androgenesis. Plant Cell Reports 18: 312–317.

    CAS  Google Scholar 

  • Silva, A. S., J. M. Q. Luz, T. M. Rodrigues, S. V. Marques, R. V. Marques & M. Pasqual. 2009. Coffea arabica L. anther callus and pro-embryoid induction by different growth regulators. Bioscience Journal 25: 19–27.

    Google Scholar 

  • Simmonds, D. H. & W. A. Keller. 1999. Significance of preprophase bands of microtubules in the induction of microspore embryogenesis of Brassica napus. Planta 208: 383–391.

    CAS  Google Scholar 

  • Smykal, P. 2000. Pollen embryogenesis—the stress mediated switch from gametophytic to sporophytic development. Current status and future prospects. Biologia Plantarum. 43: 481–489.

    CAS  Google Scholar 

  • Song, H., Q. F. Lou, X. D. Luo, J. N. Wolukau, W. P. Diao, C. T. Qian & J. F. Chen. 2007. Regeneration of doubled haploid plants by androgenesis of cucumber (Cucumis sativus L.). Plant Cell Tissue and Organ Culture 90: 245–254.

    CAS  Google Scholar 

  • Srivastava, P. & R. Chaturvedi. 2008. In vitro androgenesis in tree species: An update and prospect for further research. Biotechnology Advances 26: 482–491.

    PubMed  CAS  Google Scholar 

  • Stasolla, C., M. F. Belmonte, T. Muhammad, E. Mohamed, K. Khalil, R. Joosen, C. Maliepaard, A. G. Sharpe, B. Gjetvaj & K. Boutilier. 2008. Buthionine sulfoximine (BSO)-mediated improvement in cultured embryo quality in vitro entails changes in ascorbate metabolism, meristem development and embryo maturation. Planta 228: 255–272.

    PubMed  CAS  Google Scholar 

  • Summers, W. L., J. Jaramillo & T. Bailey. 1992. Microspore developmental stage and anther length influence the induction of tomato anther callus. Hortscience 27: 838–840.

    Google Scholar 

  • Supena, E. D. J., W. Muswita, S. Suharsono & J. B. M. Custers. 2006a. Evaluation of crucial factors for implementing shed-microspore culture of Indonesian hot pepper (Capsicum annuum L.) cultivars. Scientia Horticulturae 107: 226–232.

    Google Scholar 

  • ———, S. Suharsono, E. Jacobsen & J. B. M. Custers. 2006b. Successful development of a shed-microspore culture protocol for doubled haploid production in Indonesian hot pepper (Capsicum annuum L.). Plant Cell Reports 25: 1–10.

    PubMed  CAS  Google Scholar 

  • ———, B. Winarto, T. Riksen, E. Dubas, A. van Lammeren, R. Offringa, K. Boutilier & J. Custers. 2008. Regeneration of zygotic-like microspore-derived embryos suggests an important role for the suspensor in early embryo patterning. Journal of Experimental Botany 59: 803–814.

    PubMed  CAS  Google Scholar 

  • Tai, G. C. C. 2005. Haploids in the improvement of solanaceous species. Pp 173–190. In: C. E. Palmer, W. A. Keller, & K. J. Kasha (eds). Haploids in crop improvement II, vol. 56. Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • Tang, X. C., Y. Q. He, Y. Wang & M. X. Sun. 2006. The role of arabinogalactan proteins binding to Yariv reagents in the initiation, cell developmental fate, and maintenance of microspore embryogenesis in Brassica napus L. cv. Topas. Journal of Experimental Botany 57: 2639–2650.

    PubMed  CAS  Google Scholar 

  • Touraev, A., M. Pfosser & E. Heberle-Bors. 2001. The microspore: A haploid multipurpose cell. Advances in Botanical Research 35: 53–109.

    Google Scholar 

  • ———, B. P. Forster & S. M. Jain. 2009. Advances in haploid production in higher plants. Springer, New York.

    Google Scholar 

  • Tsuwamoto, R., H. Fukuoka & Y. Takahata. 2007. Identification and characterization of genes expressed in early embryogenesis from microspores of Brassica napus. Planta 225: 641–652.

    PubMed  CAS  Google Scholar 

  • Tulecke, W. 1965. Haploid versus Diploidy in the reproduction of cell type. Pp 217–241. In: M. Locke (ed). Reproduction: Molecular, subcellular and cellular. Academic Press, New York.

    Google Scholar 

  • Twell, D. & R. Howden. 1998. Mechanisms of asymmetric division and cell fate determination in developing pollen. Pp 69–103. In: Y. Chupeau, M. Caboche, & Y. Henry (eds). Androgenesis and haploid plants. INRA-Springer-Verlag, Berlin Heidelberg.

    Google Scholar 

  • van Bergen, S., M. J. Kottenhagen, R. M. van der Meulen & M. Wang. 1999. The role of abscisic acid in induction of androgenesis: A comparative study between Hordeum vulgare L-cvs. Igri and Digger. Journal of Plant Growth Regulation 18: 135–143.

    PubMed  Google Scholar 

  • Varghese, T. M. & Y. Gulshan. 1986. Production of embryoids and calli from isolated microspores of tomato (Lycopersicon esculentum Mill.) in liquid media. Biologia Plantarum 28: 126–129.

    Google Scholar 

  • Vasil, I. K. & T. A. Thorpe. 1994. Plant cell and tissue culture. Kluwer Academic Publishers, Dordretch, The Netherlands.

    Google Scholar 

  • Wang, M., S. van Bergen & B. Van Duijn. 2000. Insights into a key developmental switch and its importance for efficient plant breeding. Plant Physiology 124: 523–530.

    PubMed  CAS  Google Scholar 

  • Wedzony, M., B. P. Forster, I. Zur, E. Golemiec, M. Szechynska-Hebda, E. Dubas & G. Gotebiowska. 2009. Progress in doubled haploid technology in higher plants. Pp 1–33. In: A. Touraev, B. P. Forster, & S. M. Jain (eds). Advances in haploid production in higher plants. Springer, Dordrecht.

    Google Scholar 

  • Yang, J. S., M. B. Endo & I. Inada. 2005. Anther and microspore culture of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitam.). Journal of the Japanese Society for Horticultural Science 74: 78–86.

    CAS  Google Scholar 

  • Zagorska, N. A., A. Shtereva, B. D. Dimitrov & M. M. Kruleva. 1998. Induced androgenesis in tomato (Lycopersicon esculentum Mill.)—I. Influence of genotype on androgenetic ability. Plant Cell Reports 17: 968–973.

    CAS  Google Scholar 

  • ———, L. A. Shtereva, M. M. Kruleva, V. G. Sotirova, D. L. Baralieva & B. D. Dimitrov. 2004. Induced androgenesis in tomato (Lycopersicon esculentum Mill.). III. Characterization of the regenerants. Plant Cell Reports 22: 449–456.

    PubMed  CAS  Google Scholar 

  • Zaki, M. A. M. & H. G. Dickinson. 1991. Microspore-derived embryos in Brassica: The significance of division symmetry in pollen mitosis I to embryogenic development. Sexual Plant Reproduction 4: 48–55.

    Google Scholar 

  • Zamir, D., R. A. Jones & N. Kedar. 1980. Anther culture of male sterile tomato (Lycopersicon esculentum Mill.) mutants. Plant Science Letters 17: 353–361.

    Google Scholar 

  • Zarsky, V., D. Garrido, N. Eller, J. Tupy, O. Vicente, F. Schöffl & E. Heberle-Bors. 1995. The expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation. Plant Cell and Environment 18: 139–147.

    CAS  Google Scholar 

  • Zenkteler, M. & W. Nitzsche. 1984. Wide hybridization experiments in cereals. Theoretical and Applied Genetics 68: 311–315.

    Google Scholar 

  • Zhao, F. C., D. Nilanthi, Y. S. Yang & H. Wu. 2006. Anther culture and haploid plant regeneration in purple coneflower (Echinacea purpurea L.). Plant Cell Tissue and Organ Culture 86: 55–62.

    Google Scholar 

Download references

Acknowledgements

This work was supported by grant ‘AGL2006-06678’ from the Spanish Ministry of Education and Science.

Author information

Authors and Affiliations

  1. Instituto para la Conservación y Mejora de la Agrodiversidad Valenciana (COMAV), Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación (CPI), Edificio 8E - Escalera I. Camino de vera, s/n, 46022, Valencia, Spain

    José M. Seguí-Simarro

Authors
  1. José M. Seguí-Simarro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José M. Seguí-Simarro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seguí-Simarro, J.M. Androgenesis Revisited. Bot. Rev. 76, 377–404 (2010). https://doi.org/10.1007/s12229-010-9056-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12229-010-9056-6

Keywords

Search

Navigation