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Gibberellic Acid and Ethylene Control Male Sex Determination and Development of Anemia phyllitidis Gametophytes

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Abstract

Development and male sex determination in homosporous fern ­gametophytes is controlled by antheridiogens, gibberellin derivatives, which are secreted by hermaphrodites or female and promote the development of males from sexually undetermined gametophytes. In Anemia phyllitidis, antheridiogenesis is a complex process and can be prematurely induced by gibberellic acid (GA3) which imitates the action of antheridic acid, the main antheridiogen of that fern. GA3 in young gametophytes induces many specific cytomorphological and metabolical features during “induction” and “expression” phases of male sex determination which allowed to describe the useful “three-zonal” model. Influence of GA3 on dispersion of nuclear chromatin, induction of cell division cycle, sugar metabolism, and cell wall structural reorganization leads to transverse cell growth and asymmetrical division of antheridial mother cells and to antheridia formation. These processes are modulated by ethylene playing the role of a secondary messenger. Disorganization of communication between cells in gametophytes can cause death of individual cells as well as whole gametophytes.

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References

  • Bleecker, A. B., and Kende, H. 2000. Ethylene: a gaseous signal molecule in plants. Ann. Rev. Cell Dev. 16:1–18.

    Article  CAS  Google Scholar 

  • Calvo, A. P., Nicolas, C., Lorenzo, O., Nicolas, G., and Rodríguez, G. 2004. Evidence for positive regulation by gibberellins and ethylene of ACC oxidase expression and activity during transition from dormancy to germination in Fagus sylvatica L. seeds. J. Plant Growth Regul. 23:44–53.

    Article  CAS  Google Scholar 

  • Chiou, W. L., and Farrar, R. 1997. Antheridiogen production and response in Polypodiaceae species. Am. J. Bot. 84:633–640.

    Article  Google Scholar 

  • Collett, C. E., Harberd, N., and Leyser, O. 2000. Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol. 124:553–561.

    Article  CAS  PubMed  Google Scholar 

  • Cooke, T. J., and Paolillo, D. J. Jr. 1980. The control of the orientation of cell divisions in fern gametophytes. Am. J. Bot. 67:1320–1333.

    Article  Google Scholar 

  • Corey, E. J., and Myers, A.G. 1985. Total synthesis of (±)-antheridium-inducing factor (AAn, 2) of the fern Anemia phyllitidis. Clarification of stereochemistry. J. Am. Chem. Soc. 107:5574–5576.

    Article  CAS  Google Scholar 

  • Corey, E. J., Myers, A.G., Takahashi, N., Yamane, H., and Schraudolf, H. 1986. Constitution of antheridium-inducing factor of Anemia phyllitidis. Tetrahedron Lett. 27:5083–5084.

    Article  CAS  Google Scholar 

  • Fisher, R. W., and Miller, J. H. 1978. Growth regulation by ethylene in fern gametophytes. V. Ethylene and the early events of spore germination. Am. J. Bot. 65:334–339.

    Article  CAS  Google Scholar 

  • Fisher, R. W., and Shropshire, W. Jr. 1979. Reversal by light of ethylene-induced inhibition of spore germination in the sensitive fern Onocela sensibilis. Plant Physiol. 63:984–988.

    Article  CAS  PubMed  Google Scholar 

  • Haufler, C. H., and Soltis, D. E. 1986.Genetic evidence suggests that homosporous ferns with high chromosome numbers are diploid. Proc. Natl. Acad. Sci. USA 83:4389–4393.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Y. M., Chou, H. M., and Chiou, W. L. 2004. Density affects growth and sexual expression of Osmunda cinnamomea (Osmundaceae: Pteridophyta). Ann. Bot. 94:229–232.

    Article  PubMed  Google Scholar 

  • Harthill, J. E., Meek, S. E. M., Morrice, N., Peggie, M. W., Borch, J., Wong, B. H. C., and MacKintosh, C. 2006. Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J. 47:211–223.

    Article  CAS  PubMed  Google Scholar 

  • Kaneta, T., Kakimoto, T., and Shiboaka, H. 1997. Gibberellin A3 causes a decrease in the accumulation of mRNA for ACC oxidase and in the activity of the enzyme in azuki bean (Vigna angularis) epicotyl. Plant Cell Physiol. 38:1135–1141.

    CAS  PubMed  Google Scholar 

  • Kaźmierczak, A. 1998. Studies on morphology and metabolism of prothalli during GA3-induced formation of antheridia in Anemia phyllitidis. Acta Physiol. Plant. 20:277–283.

    Article  Google Scholar 

  • Kaźmierczak, A. 2003a. Induction of cell division and cell expansion at the beginning of GA3-induced precocious antheridia formation in Anemia phyllitidis gametophytes. Plant Sci. 165:933–939.

    Article  Google Scholar 

  • Kaźmierczak, A. 2003b. The ethylene is a positive regulator for GA3-induced male sex in Anemia phyllitidis gametophytes. Plant Cell Rep. 22:295–302.

    Article  PubMed  Google Scholar 

  • Kaźmierczak, A. 2004. Aminooxyacetic acid inhibits antheridiogenesis and development of Anemia phyllitidis gametophytes. Plant Cell Rep. 23:203–210.

    Article  PubMed  Google Scholar 

  • Kaźmierczak, A. 2005. Methionine and cobalt ions control of development of fern gametophytes. Acta Physiol. Plant. 27:447–454.

    Article  Google Scholar 

  • Kaźmierczak, A. 2006. Role of gibberellic acid and ethylene in controlling the sex determination in gametophytes of the homosporous fern Anemia phyllitidis. In Conservation-related Problems of Pteridophytes in Poland, Botanical Guidebooks 29, eds. H. Piekos-Mirkowa and E. Zentkeler, pp. 119–132. Kraków, Poland: Polish Academy of Science, W. Szafer Institute of Botany.

    Google Scholar 

  • Kaźmierczak, A. 2007. Ethylene is a modulator of gibberellic acid induced antheridiogenesis in Anemia phyllitidis gametophytes. Biol. Plant 51:683–689.

    Article  Google Scholar 

  • Kaźmierczak, A. 2008. Cell number, cell growth, antheridiogenesis, and callose amount is reduced and atrophy induced by deoxyglucose in Anemia phyllitidis gametophytes. Plant Cell Rep. 27:813–821.

    Article  PubMed  Google Scholar 

  • Kaźmierczak, A. 2010. Endoreplication in Anemia phyllitidis coincides with the development of gametophytes and male sex. Physiol. Plant 138:321–328.

    Article  PubMed  Google Scholar 

  • Kaźmierczak, A., and Kaźmierczak, J. 2007. The level of 1-aminocyclopropane-1-carboxylic acid is increased in Anemia phyllitidis gametophytes during GA3-induced antheridia formation. Acta Physiol. Plant. 29:211–216.

    Article  Google Scholar 

  • Kaźmierczak, A., and Kaźmierczak, J. 2009. Contrasting effects of ethylene perception and synthesis inhibitors on GA3-induced antheridiogenesis and the level of 1-aminocyclopropane-1-carboxylic acid in Anemia phyllitidis gametophytes. Environ. Exp. Botany 66:172–177.

    Article  Google Scholar 

  • Kaźmierczak, A., and Maszewski, J. 1997. Inhibition of GA3-induced antheridiogenesis in Anemia phyllitidis by peptidic extracts from male sex organs of Chara. Acta Physiol. Plant 19:269–276.

    Article  Google Scholar 

  • Kaźmierczak, A., and Maszewski, J. 1998. Antheridial chromatin condensation factor from male sex organs of Chara tomentosa. Cell Biol. Int. 22:227–236.

    Article  PubMed  Google Scholar 

  • Lucas, W. J., and Lee, J. Y. 2004. Plasmodesmata as a supracellular control network in plants. Nat. Rev. Mol. Cell. Biol. 5:712–726.

    Article  CAS  PubMed  Google Scholar 

  • Mander, L. N. 2003. Twenty years of gibberellin research. Natl. Prod. Rep. 20:49–69.

    Article  CAS  Google Scholar 

  • Marshall, W. F. 2002. Order and disorder in the nucleus. Curr. Biol. 12:R185–R192.

    Article  CAS  PubMed  Google Scholar 

  • Martin, C., Bhatt, K., and Baumann, K. 2001. Shaping in plant cells. Curr. Opin. Plant Biol. 4:540–549.

    Article  CAS  PubMed  Google Scholar 

  • Metzger, J. M. 1995. Hormones and reproductive development. In Plant Hormones, ed. P. J. Davis, pp. 617–648. Dordrecht, Netherlands: Kluwer Academic Publishers.

    Google Scholar 

  • Miller, J. H. 1968. Fern gametophytes as experimental material. Bot. Rev. 34:361–440.

    Article  CAS  Google Scholar 

  • Miller, P. M., Sweet, H., and C., Miller, J. H. 1970. Growth regulation by ethylene in fern gametophytes. I. Effects on protonemal and rhizoidal growth and interaction with auxin. Am. J. Bot. 57:212–217.

    Google Scholar 

  • Mickel, J. T. 1982. The genus Anemia (Schizaeaceae) in Mexico. Brittonia 34:388–413.

    Article  Google Scholar 

  • Nakanishi, K., Endo, M., Näf, U., and Johnson, J. F. 1971. Structure of the antheridium-inducing factor of the fern Anemia phyllitidis. J. Am. Chem. Soc. 93:5579–5581.

    Article  CAS  Google Scholar 

  • Näf, U., Nakanishi, K., and Endo, M. 1975. On the physiology and chemistry of fern antheridiogens. Bot. Rev. 41:315–359.

    Article  Google Scholar 

  • Nick, P. 1999. Signals, motors, morphogenesis – the cytoskeleton in plant development. Plant Biol. 1:169–179.

    Article  CAS  Google Scholar 

  • Pichersky, E., Soltis, D., and Soltis, P. 1990. Defective chlorophyll a/b-binding protein genes in the genome of a homosporous fern. Proc. Natl. Acad. Sci. USA 87:195–199.

    Article  CAS  PubMed  Google Scholar 

  • Raghavan, V. 1989. Control differentiation of sex organs on gametophytes. In Developmental Biology of Fern Gametophytes. Cambridge: Cambridge University Press.

    Google Scholar 

  • Raghavan, V. 1993. Differential expression of nuclear and plastid genes induced by red light and gibberellic acid during germination of spores of the fern Anemia phyllitidis. Am. J. Bot. 80:385–390.

    Article  CAS  Google Scholar 

  • Reynolds, W. F., and Wolfe, S. L. 1984. Protamines in plant sperm. Exp. Cell Res.152:443–448.

    Article  CAS  PubMed  Google Scholar 

  • Rijnders, J. G. H. M., Yang, Y. Y., Kamiya, Y., Takahashi, N., Barendse, G. W. M., Bloom, C. W. P. M., and Voesenek L. A. C. J. 1997. Ethylene enhances gibberellin levels and petiole sensitivity in flooding-tolerant Rumex palustris but not in flooding-intolerant R. acetosa. Planta 203:20–25.

    CAS  Google Scholar 

  • Rohwer, F., and Bopp, M. 1984. Ethylene synthesis in moss protonema. J. Plant Physiol. 117:331–338.

    Google Scholar 

  • Rutter, M. R., and Raghavan, V. 1978. DNA synthesis and cell division during spore germination in Lygodium japonicum. Ann. Bot. 42:957–965.

    Google Scholar 

  • Schraudolf, H. 1964. Relative activity of the gibberellins in the antheridium induction in Anemia phyllitidis. Nature 201:98–99.

    Article  CAS  Google Scholar 

  • Schraudolf, H. 1966. Die Wirkung von Phytohormonen auf Keimung und Entwicklung von Farnprothallien II. Analyse der Wechselbeziehung Zwischen Gibberllinkonzentration, Antheridienbildung und physiologischem Alter der Prothalliumzellen in Anemia phyllitidis. Planta (Berl.) 68:335–352.

    Article  CAS  Google Scholar 

  • Schuettpelz, E., and Pryer, K. M. 2007. Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050.

    Article  Google Scholar 

  • Sugimoto-Shirasu, K., and Roberts, K. 2003. “Big it up”: endoreduplication and cell size control in plants. Curr. Opin. Plant Biol. 6:544–553.

    Article  CAS  PubMed  Google Scholar 

  • Tadeo, F. R., Gómez-Cadenas, A., Ben-Cheikh, W., Primo-Millo, E., and Talón, M. 1997. Gibberellin-ethylene interaction controls radial expansion in citrus roots. Planta 202:370–378.

    Article  CAS  Google Scholar 

  • Tanurdzic, M., and Banks, J. A. 2004. Sex-determining mechanisms in land plants. Plant Cell 16:S61–S71.

    Article  CAS  PubMed  Google Scholar 

  • Tittle, F. L. 1987. Auxin-stimulated ethylene production in fern gametophytes and sporophytes. Physiol. Plant 70:499–502.

    Article  CAS  Google Scholar 

  • Tilney, T. G., Cooke, T. J., Connelly, P. S., and Tilney, M. S. 1990. The distribution of plasmodesmata and its relationship to morphogenesis in fern gametophytes. Development 110:1209–1221.

    CAS  PubMed  Google Scholar 

  • Wang, K. L. C., Li, H., and Ecker, J. R. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151.

    CAS  PubMed  Google Scholar 

  • Warne, T. R., and Lloyd, R. M. 1986. Gametophytic density and sex expression in Ceratopteris. Can. J. Bot. 65:362–365.

    Article  Google Scholar 

  • Wolniak, S. M, Klink, V. P., Hart, P. E., and Tai, C. W. 2000. Control of development in the ­spermatozoids of lower plants. Grav. Space Biol. Bull. 13:85–93.

    CAS  Google Scholar 

  • Van Der Knaap, E., Kim, J. H., and Kende, H. 2000. A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol. 122:695–704.

    Article  PubMed  Google Scholar 

  • Voesenek, L. A. C. J., Benschop, J. J., Bou, J., Cox, M. C. H., Groeneveld, H. W., Millenaar, F. F., Vreeburg, R. A. M., and Peeters, A. J. M. 2003. Interactions between plant hormones regulate submergence-induced shoot elongation in the flooding-tolerant dicot Rumex palustris. Ann. Bot. 91:205–211.

    Article  CAS  PubMed  Google Scholar 

  • Vriezen, W. H., Zhou, Z., and van der Straeten, D. 2003. Regulation of submergence-induced enhancement shoot elongation in Oryza sativa L. Ann. Bot. 91:263–270.

    Article  CAS  PubMed  Google Scholar 

  • Yamane, H. 1998. Ferns antheridiogens. Int. Rev. Cytol. 184:1–31.

    Article  CAS  Google Scholar 

  • Yamauchi, T., Oyama, N., Yamane, N., Murofushi, N., Schraudolf, H., Pour, M., Furber, M., and Mander, L. N. 1996. Identification of antheridiogens in Lygodium círcinnatum and Lygodium flexuosum. Plant Physiol. 111:741–745.

    CAS  PubMed  Google Scholar 

  • Yamauchi, T., Oyama, N., Yamane, N., Murofushi, N., Schraudolf, H., Pour, M., Seto, H., and Mander, L. N. 1997. Biosynthesis of GA73 methyl ester in Lygodium ferns. Plant Physiol. 113:773–778.

    CAS  PubMed  Google Scholar 

  • Yamasaki, S., Fujii, N., and Takahashi, H. 2000. The ethylene-regulated expression of CS-ETR2 and CS-ERS genes in cucumber plants and their possible involvement with sex expression in flowers. Plant Cell Physiol. 41:608–616.

    CAS  PubMed  Google Scholar 

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Acknowledgments

I thank M. Fronczak for the help in preparing this manuscript in English.

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  1. Department of Cytophysiology, University of Łódź, ul. Pilarskiego 14, Łódź, 90-231, Poland

    Andrzej Kaźmierczak

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  1. Andrzej Kaźmierczak
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Correspondence to Andrzej Kaźmierczak .

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Editors and Affiliations

  1. Dept. Botany, University of Rajasthan, Jaipur, 302004, India

    Ashwani Kumar

  2. Depto. Biologia de Organismos y Sis, Unidad de Fisologia Vegetal, Universidad de Oviedo, Oviedo, 33005, Spain

    Helena Fernández

  3. , Dpt. Biología de Organismos y Sistemas, Universidad de Oviedo, c) Catedrático Rodrigo, Oviedo, 33071, Spain

    Maria Angeles Revilla

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Kaźmierczak, A. (2011). Gibberellic Acid and Ethylene Control Male Sex Determination and Development of Anemia phyllitidis Gametophytes. In: Kumar, A., Fernández, H., Revilla, M. (eds) Working with Ferns. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7162-3_5

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