Abstract
Embryogenesis can be initiated directly from microspores or pollen grains. This is known as androgenesis and refers to the process of redirection of normal pollen development (gametophytic pathway) towards the embryo formation (sporophytic). This review mainly deals with the current knowledge of stress and developmental aspects of induction of androgenesis. The crucial role of stress inductive treatment together with changes in cell polarity are discussed in relation to other relevant biological systems. The intriguing speculations are made on the basis of these comparisons which may point out the direction of future investigations.
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Afele, J.C., Kannenberg, L.W., Keats, R., Sohota, S., Swanson, E.B.: Increased induction of microspore embryos following manipulation of donor plant environment and culture temperature in corn (Zea mays L.).-Plant Cell Tissue Organ Cult. 28: 87-90, 1992.
Alique, R., Akhavan-Niak, H., Russel, P.: A role for Hsp90 in cell cycle control: Weel tyrosine kinase activity requires interaction with Hsp90.-EMBO J. 13: 6099-6106, 1994.
Atkinson, B.G., Raizada, M., Bouchard, R.A., Frappier, J.R.H., Walden, D.B.: The independent stage-specific expression of the 18 kDa heat shock protein genes during microsporogenesis in Zea mays.-Develop. Genet. 14: 15-26, 1993.
Binarová, P., Hause, G., Cenklova, V., Cordewener, J.H.G., van Lookeren Campagne, M.M.: A short severe heat shock is required to induce embryogenesis in late bicellular pollen of Brassica napus L.-Sex. Plant Reprod. 10: 200-208, 1997.
Binarová, P., Straatman, K., Hause, B., Hause, G., van Lammeren, A.A.M.: Nuclear DNA-synthesis during the induction of embryogenesis in cultured microspores and pollen of Brassica napus L.-Theor. appl. Genet. 87: 9-16, 1993.
Bonet, F.J., Azbaid, L., Olmedilla, A.: Pollen embryogenesis: atavism or totipotency?-Protoplasma 202: 115-121, 1998.
Boutilier, K.A., Gines, M.J., DeMoor, J.M., Huang, B., Baczynski, C.L., Iyer, V.N., Miki, B.L.: Expression of the BnNAP subfamily of napin genes coincide with the induction of Brassica microspore embryogenesis.-Plant Mol. Biol. 26: 1711-1723, 1994.
Boutilier, K., Hattori, J., Oullet, T., van Blijderveen, M., van Lookeren Campagne, M.M., Miki, B.: Bnm3, an embryo-expressed AP2 domain transcription factor from Brassica napus.-In.: Abstracts of XVth International Congress on Sexual Plant Reproduction, Wageningen 1998.
Chen, Y.C., McCormick, S.: sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development.-Development 122: 3243-3253, 1996.
Chupeau, Y., Caboche, M., Henry, Y. (ed.): Androgenesis and Haploid Plants.-Springer, Berlin 1998
Cordewener, J., Jansen, H., Hause, G., Fiers, M., van Lookeren Campagne, M.: Bnp23, the plant homologue of mammalian p23, is induced during microspore embryogenesis in Brassica napus.-In: Abstracts of XVth International Congress on Sexual Plant Reproduction, Wageningen 1998.
Cordewener, J.H.G., Busink, R., Traas, J.A., Custers, J.B.M., Dons, H.J.M., van Lookeren Campagne, M.M.: Induction of microspore embryogenesis in Brassica napus L. is accompanied by specific changes in protein synthesis.-Planta 195: 50-56, 1994.
Cordewener, J.H.G., Hause, G., Gorgen, E., Bunsik, R., Hause, B., Dons, H.J.M., van Lammeren, A.A.M., van Lookeren Campagne, M.M., Pechan, P.M.: 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, 1995.
Custers, J.B.M., Cordewener, J.H.G., Nollen, Y., Dons, H.J.M., van Lookeren Campagne, M.M.: Temperature controls both gametophytic and sporophytic development in microspore cultures of Brassica napus.-Plant Cell Rep. 13: 267-271, 1994.
DeRocher, A.E., Vierling, E.: Developmental control of small heat shock protein expression during pea seed maturation. Plant J. 5: 93-102, 1994.
Eady, C., Lindsey, K., Twell, D.: The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation.-Plant Cell 7: 65-74, 1995.
Ferrie, A.M.R., Palmer, C.E., Keller, W.A.: Haploid Embryogenesis.-In: Thorpe, T.A. (ed.): In Vitro Embryogenesis in Plants. Pp. 309-344. Kluwer Academic Publishers, Dordrecht 1995.
Golschmidt, R.: Gen und Ausseneigenschaft (Untersuchungen an Drosophila).-Z. Indukt. Abstamm. Vererbungsl. 69: 38-69, 70–131, 1935.
Gonzalez-Melendi, P., Testillano, P.S., Ahmadian, P., Fadon, B., Vicente, O., Risueno, M.C.: In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum.-Protoplasma 187: 60-71, 1995.
Guha, S., Maheshwari, S.C.: In vitro production of embryos from anthers of Datura.-Nature 204: 497, 1964.
Gyorgyey, J., Gartner, A., Nemeth, K., Magyar, Z., Hirt, H., Heberle-Bors, E., Dudits, D.: Alfalfa heat shock genes are differentially expressed during somatic embryogenesis.-Plant mol. Biol. 16: 999-1007, 1991.
Harada, H., Kyo, M., Imamura, J.: Induction of embryogenesis and regulation of the developmental pathway in immature pollen of Nicotiana species.-Curr. Topics Develop. Biol. 20: 397-408, 1986.
Hause, G., Cordewener, J.H.G., Ehrmanova, M., Hause, B., Binarová, P., van Lookeren Campagne, M.M., van Lammeren, A.A.M.: Cell cycle dependent distribution of phosphorylated proteins in microspores and pollen of Brassica napus L., detected by the monoclonal antibody MPM-2.-Protoplasma 187: 117-126, 1995.
Hause, G., Hause, B., van Lammeren, A.A.M.: Microtubular and actin filament configurations during microspore and pollen development in Brassica napus cv. Topas.-Can. J. Bot. 70: 1369-1376, 1992.
Hause, G., Hause, G., Pechan, P., van Lammeren, A.A.M.: Cytoskeletal changes and induction of embryogenesis in microspore and pollen cultures of Brassica napus L.-Cell Biol. int. 17: 153-168, 1993.
Heberle-Bors, E.: In vitro haploid formation from pollen: a critical review.-Theor. appl. Genet. 71: 361-374, 1985.
Horwitz, R.H., Herskowitz, I.: Mechanisms of asymmetric cell division: Two Bs or not two Bs, that is the question.-Cell 68: 237-255, 1992.
Huang, B., Sunderland, N.: Temperature-stress pretreatment in barley anther culture.-Ann. Bot. 49: 77-88, 1982.
Jan, Y.N., Jan, L.Y.: Asymetric cell division.-Nature 392: 775-778, 1998.
Keller, W.A., Armstrong, K.C.: Stimulation of embryogenesis and haploid production in Brassica campestris anther cultures by elevated temperature treatments.-Theor. appl. Genet. 55: 65-67, 1979.
Kirk, D.L.: The genetic program for germ-soma differentiation in Volvox.-Annu. Rev. Genet. 31: 359-380, 1997.
Koul, A.K., Karihaloo, J.L.: In vivo embryoids from anthers of Narcissus bioflorus curt.-Euphytica 26: 97-102, 1977.
Kyo, M., Harada, H.: Control of the developmental pathway of tobacco pollen in vitro.-Planta 168: 427-432, 1986.
Kyo, M., Harada, H.: Specific phosphoproteins in the initial period of tobacco pollen embryogenesis.-Planta 182: 58-63, 1990.
Kyo, M., Ohkawa, T.: Investigation of subcellular localization of several phosphoproteins in embryogenic pollen grains of tobacco.-J. Plant Physiol. 137: 525-529, 1991.
Nasmyth, K., Jansen, R.P.: The cytoskeleton in mRNA localization and cell differentiation.-Curr. Opin. Cell Biol. 9: 396-400, 1997.
Němec, B.: [About the pollen grains of petaloid anthers of Hyacinthus orientalis L.]-Rozpr. Čes. Akad. 7(17): 1-18, 1898. [In Czech.]
Nitsch, C.: Pollen culture —a new technique for mass production of haploid and homozygous plants.-In: Kasha, K.J. (ed.): Haploids in Higher Plants. Advances and Potential. Pp. 123-135. University of Guelph, Guelph 1974.
Nitsch, C., Norrel, B.: Effect d'un choc thermique sur le pouvoir embryogène du pollen de Datura innoxia cultivédans l'anthère ou isoléde l'anthère.-Compt. rend. Acad. Sci. Paris, Sér. D 276: 303-306, 1973.
Park, S.K., Howden, R., Twell, D.: The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate.-Development 125: 3789-3799, 1998.
Pechan, P., Keller, W.A.: Induction of microspore embryogenesis in Brassica napus by gamma irradiation and ethanol stress.-In vitro cell. develop. Biol. 25: 1073-1074, 1989.
Pechan, P.M., Bartels, D., Brown, D.C.W., Schell, J.: Messenger-RNA and protein changes associated with induction of Brassica microspore embryogenesis.-Planta 184: 161-165, 1991.
Pechan, P.M., Keller, W.A.: Indentification of potentially embryogenic microspores in Brassica napus.-Physiol. Plant. 74: 377-384, 1988.
Petersen, N.S., Young, P.: Effects of heat shock on protein processing and turnover in developing Drosophila wings.-Develop. Genet. 10: 11-15, 1989.
Petersen, R., Lindquist, S.: Regulation of HSP 70 synthesis by messenger RNA degradation.-Cell Regul. 1: 135-149, 1989.
Petolino, J.F., Thomson, S.A.: Genetic analysis of anther culture response in maize.-Theor. appl. Genet. 74: 284-286, 1987.
Powell, W.: Environmental and genetical aspects of pollen embryogenesis.-In: Bajaj, V.P.S. (ed.): Haploids in Crop Improvement I. Biotechnology in Agriculture and Forestry. Vol. 12. Pp. 45-65. Springer-Verlag, Berlin 1990.
Raghawan, V.: Molecular Embryology of Flowering Plants.-Cambridge University Press, Cambridge 1997.
Ramanna, M.S.: The origin and in vivo development of embryoids in the anthers of Solanum hybrids.-Euphytica 23: 623-632, 1974.
Rashid, A., Reinert, J.: Factors affecting high-frequency embryo formation in ab initio pollen cultures of Nicotiana.-Protoplasma 116: 155-160, 1983.
Reynolds, T.L.: Pollen embryogenesis.-Plant mol. Biol. 33: 1-10, 1997.
Reynolds, T.L., Crawford, R.L.: Changes in abundance of an anbscisic acid-responsive, early cysteine-labelled metallothionein transcript during pollen embryogenesis in bread wheat (Triticum aestivum).-Plant mol. Biol. 32: 823-829, 1996.
Reynolds, T.L., Kitto, S.L.: Identification of embryoid-abundant genes that are temporally expressed during pollen embryogenesis in wheat anther cultures.-Plant Physiol. 100: 1744-1750, 1992.
Říhová, L., Čapková, V., Tupý, J.: Changes in glycoprotein patterns associated with male gametophyte development and with induction of pollen embryogenesis in Nicotiana tabacum.-J. Plant Physiol. 147: 573-581, 1996.
Scott, P., Lyne, R.L., ap Rees, T.: Metabolism of maltose and sucrose by microspores isolated from barley (Hordeum vulgare L.).-Planta 197: 435-441, 1995.
Shaw, S.L., Quatrano, R.S.: Polar localization of adihydropyridine receptor on living Fucus zygotes.-J. Cell Sci. 109: 335-342, 1996a.
Shaw, S.L., Quatrano, R.S.: The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes.-Development 122: 2623-2630, 1996b.
Smýkal, P.: Effect of high temperature on gene expression and develomental fate of plant cells.-PhD Thesis, Charles University, Prague 1999.
Sopory, S.K., Munshi, M.: Anther culture.-In: Jain, S.M., Sopory, S.K., Veilleux, R.E., (ed.): In Vitro Haploid Production in Higher Plants. Vol. 1. Pp. 145-176. Kluwer Academic Publishers, Dordrecht 1996.
Sterk, P., Booij, H., Schellekens, G.A., van Kammen, A., de Vries, S.C.: Cell-specific expression of the carrot EP2 lipid transfer protein gene.-Plant Cell 3: 907-921, 1991.
Sunderland, N., Collins, G.B., Dunwell, J.M.: The role of nuclear fusion in pollen embryogenesis of Datura innoxia. Mill.-Planta 117: 227-241, 1974.
Sunderland, N., Wicks, F.M.: Embryoid formation in pollen grains of Nicotiana tabacum.-J. exp. Bot. 22: 213-226, 1971.
Telmer, C.A., Newcomb, W., Simmons, D.H.: Microspore development in Brassica napus and the effect of high temperature on division in vivo and in vitro.-Protoplasma 172: 154-165, 1993.
Telmer, C.A., Newcomb, W., Simmonds, D.H.: Cellular changes during heat shock induction and embryo development of cultured microspores of Brassica napus cv. Topas.-Protoplasma 185: 106-112, 1995.
Telmer, C.A., Simmonds, D.H., Newcomb, W.: Determination of developmental stage to obtain high frequencies of embryogenic microspores in Brassica napus.-Physiol. Plant. 84: 417-424, 1992.
Testillano, P.S., Gonzales-Melendi, P., Ahmadian, P., Fadon, B., Risueno, M.C.: The immunolocalization of nuclear antigens during the pollen developmental program and the induction of pollen embryogenesis.-Exp. Cell Res. 221: 41-54, 1995.
Touraev, A., Ilham, A., Vicente, O., Heberle-Bors, E.: Stress-induced microspore embryogenesis in tobacco: an optimized system for molecular studies.-Plant Cell Rep. 15: 561-565, 1996a.
Touraev, A., Lezin, F., Heberle-Bors, E., Vicente, O.: Maintenance of gametophytic development after symmetrical division in tobacco microspore culture.-Sex. Plant Reprod. 8: 70-76, 1995.
Touraev, A., Pfosser, M., Vicente, O., Heberle-Bors, E.: Stress as the major signal controlling the developmental fate of tobacco microspores: towards a unified model of induction of microspore/pollen embryogenesis.-Planta 200: 144-152, 1996b.
Touraev, A., Vicente, O., Heberle-Bors, E.: Initiation of microspore embryogenesis by stress.-Trends Plant Sci. 2: 297-301, 1997.
Twell, D., Howden, R.: Mechanism of asymmetric division and cell fate determination in developing pollen.-In: Chupeau, Y., Caboche, M., Henry, Y. (ed.): Androgenesis and Haploid Plants. Pp. 67-103. Springer, Berlin 1998.
Vrinten, P.I., Nakamuar, T., Kasha, K.J.: Characterization of cDNAs expressed in the early stages of microspore embryogenesis in barley (Hordeum vulgare) L.-Plant mol. Biol. 41: 455-463, 1999.
Zaki, M.A.M., Dickinson, H.: Structural changes during the first divisions of embryos resulting from anther and free microspore culture in Brassica napus.-Protoplasma 156: 149-162, 1990.
Zaki, M.A.M., Dickinson, H.G.: Microspore-derived embryos in Brassica: the significance of division symmetry in pollen mitosis I to embryogenic development.-Sex. Plant Reprod. 4: 48-55, 1991.
Zaki, M.A.M., Dickinson, H.G.: Modification of cell development in vitro: the effect of colchicine on anther and isolated microspore culture in Brassica napus.-Plant Cell Tissue Organ Cult. 40: 255-270, 1995.
Žárský, V., Garrido, D., Eller, N., Tupý, J., Vicente, O., Schoffl, F., Heberle-Bors, E.: The expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation.-Plant Cell Environ. 18: 139-147, 1995.
Žárský, V., Garrido, D., Říhová, L., Tupý, J., Vicente, O., Heberle-Bors, E.: Derepression of the cell cycle by starvation is involved in the induction of tobacco pollen embryogenesis.-Sex. Plant Reprod. 5: 189-194, 1992.
Zhao, J.P., Simmonds, D.H., Newcomb, W.: Induction of embryogenesis with colchicine instead of heat in microspores of Brassica napus L. cv. Topas.-Planta 198: 433-439, 1996.
Zimmeramn, J.L., Cohill, P.R.: Heat shock and thermotolerance in plant and animal embryogenesis.-New Biol. 3: 641-650, 1991.
Zonia, L.E., Tupý, J.: Lithium treatment of Nicotiana tabacum microspores blocks polar nuclear migration, disrupts the partitioning of membrane-associated Ca, and induces symmetrical mitosis.-Sex. Plant Reprod. 8: 152-160, 1995.
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Smýkal, P. Pollen Embryogenesis - The Stress Mediated Switch from Gametophytic to Sporophytic Development. Current Status and Future Prospects. Biologia Plantarum 43, 481–489 (2000). https://doi.org/10.1023/A:1002835330799
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DOI: https://doi.org/10.1023/A:1002835330799