Some Aspects of Reproductive Biology of the Gametophyte Generation of Homosporous Ferns

  • Satish Chander Verma
Chapter

Abstract

In the homosporous ferns, the ‘haploid’ gametophyte phase (generation) is exosporic, small, short -lived and, more importantly, is completely independent of the ‘diploid’ sporophyte generation. Hence, it is as much subject to divergence and natural selection as the dominant sporophyte generation. Further, the potentially homothallic nature of their prothalli has triggered inquiry to reveal adaptations of the gametophyte generation that tend to determine the relative probabilities of inter- and intragametophytic mating as against the presumptive notion of frequent/habitual gametophytic self-fertilization in the natural populations of homosporous ferns that leads to total homozygosity, reducing a population’s evolutionary flexibility. Reproductive biology of the gametophyte generation of about fifty species of leptosporangiate ferns from the Himalaya has been examined here in respect of (l) form and sexuality, (2) sequence, location and duration of gametangia on the eventually monoecious prothalli, (3) sexual structure of cultured gametophyte populations, and (4) the ability of isolated gametophytes to become bisexual and undergo self-fertilization (= isolate potential), besides correlations, if any, among gametophyte generation time, polyploidy, habit and habitat. The importance of ascertaining the ontogenic sequence of gametangia on meristic prothalli together-with duration of the formation of antheridia during the so-called “hermaphroditic” phase is stressed. Three parameters of the laboratory-raised gametophyte populations, namely, population index, fecundity index, and mating index, as proposed, may be useful to quantify the data for attempting comparative assessments of mating system both within and between species. Contrary to the general belief of predominant intragametophytic selfing amongst the homosporous ferns, the observations reveal a variety of strategies which may promote, disproportionately favour, or even ensure intergametophytic mating, and that the life cycle of homosporous ferns cannot be stereotyped.

Keywords

Reproductive Biology Mating Index Population Index Pteridium Aquilinum Juvenile Sporophyte 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Andersson, I. 1923. The genetics of variegation in a fern. J. Genet. 13: 1–11.Google Scholar
  2. Atkinson, L. R. and A. G. Stokey. 1964. Comparative morphology of the gametophyte of the homosporous ferns. Phytomorphology 14: 51–70.Google Scholar
  3. Banks, J. 1994. Sex-determining genes in the homosporous fern Ceratopteris. Development 120: 1949–1958.PubMedGoogle Scholar
  4. Banks, J. 1997a. Sex determination in the fern Ceratopteris. Trends Plant Sci. 2: 175–180.CrossRefGoogle Scholar
  5. Banks, J. 1997b. The Transformer genes of the fern Ceratopteris simultaneously promote meristem and archegonia development and repress antheridial development in the developing gametophyte. Genetics 147: 1885–1897.PubMedGoogle Scholar
  6. Banks, J. 1999. Gametophyte development in ferns. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 163–186.Google Scholar
  7. Banks, J., L. Hickok, and M. Webb. 1993. The programming of sexual phenotype in the homosporous fern, Ceratopteris richardii. Int. J. Plant Sci. 154: 522–534.Google Scholar
  8. Bell, P. R. 1990. Life cycle of European pteridophytes. Pp. 29–37. In: Rita, J. (ed.) Taxonomia Biogeografiay Conservacion de pteridofitos. Soc. Hist. Nat. Bal., Ime Palma de Mallorca.Google Scholar
  9. Chiou, W. L., and D. R. Farrar. 1997. Antheridiogen production and response in polypodiaceous species. Amer. J. Bot. 84: 633–640.Google Scholar
  10. Cousens, M. I. 1979. Gametophyte ontogeny, sex expression, and genetic load as measures of population divergence in Blechnum spicant. Am. J. Bot. 66: 116–132.Google Scholar
  11. Cousens, M. I., D. G. Lacey, and E. M. Kelly. 1985. Life-history studies of ferns: A consideration of perspective. Proc. Roy. Soc. Edinb. 86B: 371–380.Google Scholar
  12. DöPP, W. 1959. Über eine hemmende und eine fodernde Substanz bei der Antheridienbildung in den Prothallien von Pteridium aquilinum. Ber. Dt. Bot. Ges. 72: 11–24.Google Scholar
  13. Dyer, A. F. (ed.). 1979a. The Experimental Biology of Ferns. Academic Press: London, New York.Google Scholar
  14. Dyer, A. F. 1979b. The culture of fern gametophytes for experimental investigation. Pp. 254–305. In: Dyer, A. F. (ed.) The Experimental Biology of Ferns. Academic Press, London, New York.Google Scholar
  15. Dyer, A. F., and C. N. Page. (eds.). 1985. Biology of Pteridophytes. (Proc. Symp. Edinb. Sept.12–16, 1983 ). Proc. Roy. Soc. Edinb. 86B: 1–474.Google Scholar
  16. Furuya, A. M. 1983. Photomorphogenesis in ferns. Encyclopedia. Plant Physiol. (n.s.) 16: 569–600.Google Scholar
  17. Hasebe, M., T. Omori, M. Nakazawa, T. Sano, M. Kato, and K. Isatuski. 1994. rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proc. Natl. Acad. Sci. Usa 91: 5730–5734.Google Scholar
  18. Haufler, C. H. 1985. Pteridophyte evolutionary biology: the electrophoretic approach. Proc. Roy. Soc. Edinb. 86B: 315–323.Google Scholar
  19. Haufler, C. H. 1987. Electrophresis is modifying our concepts of evolution in homosporous pteridophytes. Amer. J. Bot. 74: 953–966.Google Scholar
  20. Haufler, C. H. and D. E. Soltis. 1984. Obligate outcrossing in a homosporous fern: Field confirmation of a laboratory prediction. Amer. J. Bot. 71: 878–881.Google Scholar
  21. Haufler, C. H. and C. B. Welling. 1994. Antheridiogen, dark spore germination, and outcrossing mechanisms in Bommeria (Adiantaceae). Amer. J. Bot. 81: 616–621.Google Scholar
  22. Hedrick, P. W. 1987. Population genetics of intragametophytic selfing. Evolution 41: 137–144.CrossRefGoogle Scholar
  23. Hill, R. H. 1971. Comparative habitat requirements for spore germination and prothallial growth in three ferns from southern Michigan. Amer. Fern J. 61: 171–182.Google Scholar
  24. Holbrook-Walker, S. G. and R. M. Lloyd. 1973. Reproductive biology and gametophyte morphology of the Hawaiian fern genus Sadleria (Blechnaceae) relative to habitat diversity and propensity for colonization. Bot. J. Linn. Soc. London 67: 157–174.Google Scholar
  25. Holsinger, K. E. 1987. Gametophytic self-fertilization in homosporous plants: Development, evaluation, and application of a statistical method for evaluating its importance. Amer. J. Bot. 74: 1173–1183.Google Scholar
  26. Khare, P. B., and S. K. Roy. 1977. Genetic aspect of capacity of Cheilanthes tenuifolia (Burm.) Sw. ( Pteridophyta, Polypodiaceae). Genetica 47: 183–185.Google Scholar
  27. Klekowski, E. J., JR. 1969. Reproductive biology of the Pteridophyta, II. Theoretical considerations. Bot. J. Linn. Soc.London 62: 347 –359.Google Scholar
  28. Klekowski, E. J., JR. 1972a. Evidence against self-incompatibility in the homosporous fern, Pteridium aquilinum. Evolution, 26: 66–73.CrossRefGoogle Scholar
  29. Klekowski, E. J., JR. 1972b. Genetical featuresof ferns as contrasted to seed plants. Ann. Mo. Bot. Gard. 59: 138–151.Google Scholar
  30. Klekowski, E. J., JR. 1973. Sexual and subsexual systems in the homosporous ferns: A new hypothesis. Amer. J. Bot. 60: 535–544.Google Scholar
  31. Klekowski, E. J., JR. 1976. Homoeologous chromosome pairing in ferns. Pp. 175–184. In: Jones K. and P. E. Brandham, (eds.) Current Chromosome Research. Elsevier/North Holland Biomedical Press, Amsterdam.Google Scholar
  32. Klekowski, E. J., JR. 1979. The genetics and reproductive biology of ferns. Pp. 133–170. In: Dyer, A. F. (ed.) The Experimental Biology of Ferns. Academic Press, London, New York.Google Scholar
  33. Klekowski, E. J., JR. and H. G. Baker. 1966. Evolutionary significance of polyploidy in the Pteridophyta. Science 153: 305–307.PubMedCrossRefGoogle Scholar
  34. Kumar, K. 2001. Reproductive biology of pteridophytes. Pp. 175–214. In: Johri, B. M. and P. S. Srivastava (eds.) Reproductive Biology of Plants. Narosa Publishing House, New Delhi.CrossRefGoogle Scholar
  35. Lloyd, D. G. 1979. Some reproductive factors affecting the selection of self-fertilization in plants. Amer. Naturalist, 113: 67–79.Google Scholar
  36. Lloyd, R. M. 1974a. Mating systems and genetic load in pioneer and non-pioneer Hawaiian Pteridophyta. Bot. J. Linn. Soc. London 69: 23–35.Google Scholar
  37. Lloyd, R. M. 1974b. Reproductive biology and evolution in the Pteridophyta. Ann. Mo. Bot. Gard. 61: 318–331.Google Scholar
  38. Lloyd, R. M. 1988. Experimental studies on the probability of selfing by protandrous gametophytes. Amer. Fern J. 78: 117–121.Google Scholar
  39. LöVE, A., D. LöVE, and R. E. G. Pichi-Sermolli. 1977. Cytotaxonomical Atlas of the Pteridophyta. J. Cramer, Vaduz.Google Scholar
  40. Masuyama, S. 1972. The sequence of sex expression in the prothallia of Adiantum pedatum L. and A. capillus-veneris L. J. Jap. Bot. 47: 97–106.Google Scholar
  41. Masuyama, S. 1975a. The sequence of the gametangium formation in homosporous fern gametophytesGoogle Scholar
  42. I. Patterns and their possible effect of the fertilization with special reference to the gametophytes of Athyrium. Sci. Reports Tokyo Kyoiku Daigaku, Sec. B, 16: 47–69.Google Scholar
  43. Masuyama, S. 1975b. The sequence of the gametangium formation in homosporous fern gametophytes II. Types and their taxonomic distribution. Sci Reports Tokyo Kyoiku Daigaku Sec. B, 16: 71–86.Google Scholar
  44. Masuyama, S. 1979. Reproductive biology of the fern Phegopteris decursive -pinnata. I. The dissimilar mating systems of diploids and tetraploids. Bot. Mag. Tokyo 92: 275–289.Google Scholar
  45. Masuyama, S. 1986. Reproductive biology of the fern Phegopteris decursive -pinnata. II.Genetic analysis of self-sterility in diploids. Bot. Mag. Tokyo 99: 107–121.Google Scholar
  46. Mehra, P. N. 1949. Some observations on the prothallus of Diplazium esculentum (Retz.) Sw. J. Indian Bot. Soc. 28: 28–35.Google Scholar
  47. Mehra, P. N. and A. Gupta. 1986. Gametophytes of Himalayan Ferns. Printed by P. Kapur, C-61, Mayapuri Industrial Area Phase II New Delhi.Google Scholar
  48. Miller, J. H. 1968. Fern gametophytes as experimental material. Bot. Rev. 34: 361–440.Google Scholar
  49. Momose, S. 1958. The antheridial area of the foliate type prothallium in ferns. Jap. J. Bot. 33: 33–37. Momose, S. 1967. Prothallia of the Japanese Ferns. Tokyo Univ. Press, Tokyo.Google Scholar
  50. Momose, S. 1968. Prothallia of the ferns from Thailand. Tonan Ajia Kenkyu (The Southeast Asian Studies) 6: 73–167.Google Scholar
  51. Mottier, D. M. 1931. Development of sex organs of fern prothallia under prolonged cultivation. Bot. Gaz. 92: 218–233.Google Scholar
  52. NÄF, U. 1979. Antheridiogens and antheridial development. Pp. 435–470. In: Dyer, A. F. (ed.) Experimental Biology of Ferns. Academic Press, London, New York.Google Scholar
  53. Nayar, B. K. and S. Kaur. 1971. Gametophytes of homosporous ferns. Bot. Rev. 37: 295–396.Google Scholar
  54. Peck, J. H., C. J. Peck, and D. R. Farrar. 1990. Comparative life history studies and the distribution of pteridophyte populations. Amer. Fern J. 80: 126–142.Google Scholar
  55. Raghavan, V. 1989. Developmental Biology of Fern Gametophytes. Cambridge Univ. Press, Cambridge.Google Scholar
  56. Ranker, T. A., C. E. C. Gemmil, P. G. Trapp, A. Hambleton, and K. HA. 1996. Population genetics and reproductive biology of lava flow colonizing species of Hawaiian Sadleria (Blechnaceae). Pp. 581–598. In: Camus, J. M., M. Gibby, and R. J. Johns (eds.) Pteridology in Perspective. Roy. Bot. Gardens, Kew.Google Scholar
  57. Rashid, A.1970. In vitro studies on sex expression in Lygodium flexuosum. Phytomorphology 20: 255–261.Google Scholar
  58. Rubin, G. and D. J. Paolillo, JR. 1983. Sexual development of Onoclea sensibilis on agar and soil media without the addition of antheridiogen. Amer. J. Bot. 70: 811–815.Google Scholar
  59. Schedlbauer, M. D. 1976. Fern gametophyte development: Controls of dimorphism in Ceratopteris thalictroides. Amer. J. Bot. 63: 1080–1087.Google Scholar
  60. Schedlbauer, M. D. and E. J. Klekowski, JR. 1972. Antheridiogen activity in the fern Ceratopteris thalictroides (L.) Brogn. Bot. J. Linn. Soc. London 65: 399–413.Google Scholar
  61. Schneller, J. J. 1981. Evidence for intergenetic incompatibility in ferns. Pl. Sys. Evol. 137: 45–56. Schneller, J. J. 1988. Remarks on reproductive biology of homosporous ferns. Pl. Sys. Evol. 161: 91–94.Google Scholar
  62. Scott, R. J. and L. Hickok. 1987. Genetic analysis of antheridiogen sensitivity in Ceratopteris richardii. Amer. J. Bot. 74: 1872–1877.Google Scholar
  63. Sheffield, E. 1994. Alternation of generations in ferns: Mechanisms and significance. Biol. Rev. Cambridge Philos. Soc. 69: 331–343.Google Scholar
  64. Sheffield, E. 1996. From pteridophyte spore to sporophyte in the natural environment. Pp. 541–549. In: Camus, J. M., M. Gibby, and R. J. Johns (eds.) Pteridology in Perspective. Roy. Bot. Gardens, Kew.Google Scholar
  65. Sheffield, E., P. G. Wolf, C. H. Haufler, and T. Ranker. 1989. A Re-evaluation of plants referred to as Pteridium herediae (Colmeiro) Löve & Kjellqvist. Bot. J. Linn. Soc.London 99: 377–386.Google Scholar
  66. Soltis, D. E. and P. S. Soltis. 1987a. Breeding system of the fern Dryopteris expansa: evidence for mixed mating. Amer. J. Bot. 74: 504–509.Google Scholar
  67. Soltis, D. E. and P. S. Soltis. 1987b. Polyploidy and breeding systems in homosporous Pteridophyta: A reevaluation. Amer. Naturalist 130: 219–232.Google Scholar
  68. Soltis, D. E. and P. S. Soltis. 1989. Polyploidy, breeding systems and genetic differentiation in homosporous pteridophytes. Pp. 241–258. In: Soltis, D. E. and P. S. Soltis (eds.) Isozymes in Plant Biology. Dioscorides, Portland (Usa)CrossRefGoogle Scholar
  69. Soltis, D. E. and P. S. Soltis. 1993. Molecular data and the dynamic nature of polyploidy. Crit. Rev. Pl. Sci. 12: 243–273.Google Scholar
  70. Soltis, D. E. and P. S. Soltis. 1999. Polyploidy: Recurrent formation and genome evolution. Trends Ecol. Evol. 14: 348–352.Google Scholar
  71. Soltis, P. S. and D. E. Soltis. 1990. Genetic variation within and among populations of ferns. Amer. Fern J. 80: 161–172.Google Scholar
  72. Soltis, P. S., D. E. Soltis, and K. E. Holsinger. 1988. Estimates of intragametophytic selfing and inter-populational gene flow in homosporous ferns. Amer. J. Bot. 75: 1765–1770.Google Scholar
  73. Stebbins, G. L. 1950. Variation and Evolution in Plants. Columbia Univ. Press, New York.Google Scholar
  74. Stebbins, G. L. 1957. Self-fertilization and population variability in higher plants. Amer. Naturalist 91: 337–354.Google Scholar
  75. Stewart, W. and G. Rothwell. 1993. Paleobotany and the Evolution of Plants, 2nd ed., Cambridge Univ. Press, Cambridge.Google Scholar
  76. Takebayashi, N. and L. Peter Morrell. 2001. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macro-evolutionary approach. Amer. J. Bot. 88: 1143–1150.Google Scholar
  77. Verma, S. C. 1969. Genetics of gametophytic variation and mating system in Adiantum capillus-veneris L. Pp. 18–19. In: Johri, B. M., R. N. Kapil, and A. Rashid (eds.) Seminar on Morphology, Anatomy and Embryology of Plants (Dec. 23–28, 1969). Dept. Botany, Univ. Delhi, Delhi, India.Google Scholar
  78. Verma, S. C. 1985a. The gametophyte in relation to colonizing habit in Himalayan ferns: Relevance to reproductive biology. Proc. Roy. Soc. Edinb. 86B: 470–471.Google Scholar
  79. Verma, S. C. 1985b. Some considerations on the reproductive biology of homosporous ferns with particular reference to the colonizing species from the Himalaya. Pp. 92–98. In: Govil, C. M., and V. Kumar (eds.) Trends in Plant Research. Bishen Singh M. Pal Singh, Dehra Dun, India.Google Scholar
  80. Verma, S. C. 1989. Overt and covert mechanisms of intergametophytic mating in homosporous ferns. Pp. 285–300. In: Trivedi, M. L. B. S. Gill, and S. S. Saini (eds.) Plant Science Research in India. Today and Tomorrow’s Printers and Publishers. New Delhi.Google Scholar
  81. Verma, S. C. 2000a. Evolutionary biology of homosporous ferns: An enigma. Indian Fern J. 17: 36–49. Verma, S.C. 2000b. An appraisal of some issues in the evolutionary cytogenetics of homosporous ferns. Bionature 20: 55–74.Google Scholar
  82. Verma, S.C. 2001. Genetic implications of diversity in gametophyte biology and isolate potential of homosporous ferns. Phytomorphology 51: 33–39.Google Scholar
  83. Verma, S. C. and V. Bala. 1979. Comparative study of mating systems in some diploid and polyploid species of homosporous ferns. Pp. 237–243. In: Bir, S. S. (ed.) Recent Researches in Plant Sciences. Kalyani Publishers, New Delhi.Google Scholar
  84. Verma, S. C. and H. K. Cheema. 1987. Evidence of self-compatibility in a population of bracken fern from Britain. Phytomorphology 37: 317–321.Google Scholar
  85. Verma, S. C. and S. Kapur. 1972. Genetic systems in homosporous ferns– II. Comparative study of breeding system in three adiantaceous ferns. Pp. 227–240. In: Murty, Y. S. (ed.) Biology of Land Plants. Sarita Prakashan, Meerut, India.Google Scholar
  86. Verma, S. C., A. Kaur, and P. Mani Selvan. 1999. Experimental studies on the gametophyte generation of homosporous ferns–II. Sexuality, gametangial sequence and mating system in Pityrogramma calomelanos and Gymnopteris vestita. Indian Fern J. 16: 55–71.Google Scholar
  87. Verma, S. C., A. Kaur, and P. Mani Selvan. 2000. Experimental studies on the gametophyte generation of homosporous ferns- Iii. Sexuality, gametangial sequence, and mating system in some species of Pteris. Indian Fern J. 17: 136–174.Google Scholar
  88. Verma, S. C., A. Kaur, and S. S. Sharma. 1987. Gametophyte ontogeny, sex expression, and mating system in Hypolepis punctata: A homosporous fern. Phytomorphology 37: 53–67.Google Scholar
  89. Verma, S. C., A. Kaur, and S. S. Sharma. 1988. Experimental studies on the gametophyte generation of homosporous ferns-I. Sexuality, gametangial sequence and mating system in two lindsaeoid ferns: Sphenomeris chinensis and Lindsaea odorata. Indian Fern J. 5: 5–27.Google Scholar
  90. Verma, S. C. and P. Mani Selvan. 2001. Intraspecific variation in spore-size of homosporous ferns and its implications on fern mating systems. Bionature 21: 1–9.Google Scholar
  91. Voeller, B. 1971. Developmental physiology of fern gametophytes: Relevance for biology. BioScience 21: 266–270.Google Scholar
  92. Von Aderkas, P. and E. G. Cutter. 1983. Gametophyte plasticity and its bearing on sex expression in Todea Barbara (L.) Moore. Bot. Gaz. 144: 525–532.Google Scholar
  93. Wagner, W. H. and F. S. Wagner. 1980. Polyploidy in pteridophytes. Pp. 199–214. In: Lewis, W.H. (ed.) Polyploidy: Biological Relevance. Plenum, New York.CrossRefGoogle Scholar
  94. Warne, T. R. and R. M. Lloyd. 1980. The role of spore germination and gametophyte development in habitat selection: Temperature responses in certain temperate and tropical ferns. Bull. Torrey Bot. Cl. 107: 57–64.Google Scholar
  95. Warne, T. R. and R. M. Lloyd. 1987. Gametophyte density and sex expression in Ceratopteris. Canad. J. Bot. 65: 362–365.Google Scholar
  96. Wen, C. K., R. Smith, and J. Banks. 1999. Anii: A sex pheromone induced gene in Ceratopteris gametophytes and its possible role in sex determination. Plant Cell 11: 1307–1318.Google Scholar
  97. Wilkie, D. 1956. Incompatibility in bracken. Heredity 10: 247–256.CrossRefGoogle Scholar
  98. Wilkie, D. 1963. Genetic analysis of variation in the bracken prothallus. J. Linn. Soc. London (Bot.) 58: 333–336.Google Scholar
  99. Willson, M. F. 1981. Sex expression in fern gametophytes: Some evolutionary possibilities. J. Theor. Biol. 93: 403–409.Google Scholar
  100. Yamane, H. 1998. Fern antheridiogens. Int. Rev. Cytol. 184: 1–32.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2003

Authors and Affiliations

  • Satish Chander Verma

There are no affiliations available

Personalised recommendations