Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Two theories of origin of the land-plant sporophyte: Which is left standing?

  • 16 Citations

Abstract

Questions concerning the two competing theories of the development of alternating generations in land plants, the homologous theory and the antithetic theory, have never been fully resolved. In the majority of recent accounts there appears to have been increasing de facto support (if one considers the ontogenetic processes and phylogenetic consequences discussed) for the antithetic theory. However, this preference is usually not plainly stated (as such) in these discussions, and some support has also continued for the homologous theory. The crux of both theories (homologous and antithetic) centers upon how the sporophyte may have originated in the life cycle. One problem with the homologous theory is that it is not made explicit how the development of a dependent sporophyte could have occurred in the life cycle (when the precedent organisms are considered to have had free-living, putatively similar, gametophytes and sporophytes). The antithetic theory, by contrast, offers a definite ontogenetic mechanism or process (retention of the zygote on the gametophyte, delay of zygotic meiosis, with zygotic mitoses occurring first) by which a dependent sporophyte might have originated and persisted, in the context of a life cycle formerly lacking a sporophyte generation. Also, a review of a variety of evidence (morphological, cytological, biochemical, etc.) would appear to lend more support to the antithetic theory than to the homologous theory. In discussing types of algae now known to be most clearly related to land plants (i.e., charophytes, particularly advanced forms), the type of life cycle exhibited by these particular algae (haplontic, with zygotic meiosis; no sporophyte present) suggests that only an antithetic origin of the sporophyte in land plants is actually feasible.

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

Literature Cited

  1. Al-Houty, F. A. A. &P. J. Syrett. 1984. The occurrence of urease/urea amidolyase and glycolate oxidase/ dehydrogenase inKlebsormidium spp. and members of the Ulotrichales. Brit. Phycol. J. 19: 1–10.

  2. Arber, A. R. 1950. The natural philosophy of plant form. Cambridge Univ. Press, Cambridge.

  3. Beech, P. L., K. Heimann &M. Melkonian. 1991. Development of the flagellar apparatus during the cell cycle in unicellular algae. Protoplasma 164: 23–37.

  4. Blackwell, W. H. &M. J. Powell. 1995. Where have all the algae gone, or, how many kingdoms are there? Amer. Biol. Teacher 57: 160–167.

  5. —. 1999. Reconciling kingdoms with codes of nomenclature: Is it necessary? Syst. Biol. 48: 406–412.

  6. —. 2000. A review of group fililation of stramenopiles, additional approaches to the question. Evol. Theory & Rev. 12(3): 49–88.

  7. Bold, H. C. 1948. The occurrence of chlorophyll in the sporophyte ofRicciocarpus natans. Amer. J. Bot. 35: 440–443.

  8. —. 1957. Morphology of plants. Harper & Brothers, New York.

  9. — &M. J. Wynne. 1978. Introduction to the algae: Structure and reproduction. Prentice-Hall, Englewood Cliffs, NJ.

  10. ——. 1985. Introduction to the algae: Structure and reproduction. Ed. 2. Prentice-Hall, Upper Saddle River, NJ.

  11. —,C. J. Alexopoulos &T. Delevoryas. 1980. Morphology of plants and fungi. Ed. 4. Harper & Row, New York.

  12. ———. 1987. Morphology of plants and fungi. Ed. 5. Harper & Row, New York.

  13. Bower, F. O. 1908. The origin of a land flora. Macmillan, London.

  14. —. 1935. Primitive land plants. Macmillan, London.

  15. Bremer, K. 1985. Summary of green plant phylogeny and classification. Cladistics 1: 369–385.

  16. —. 1986. Systematics of the green algae (Irvine, D.E.G. & John, D.M. (Eds.), a review. Cladistics 2: 378–381.

  17. — &H. E. Wanntorp. 1981a. A cladistic classification of green plants. Nord. J. Bot. 1: 1–3.

  18. ——. 1981b. The cladistic approach to plant classification. Pp. 87–94in V. Funk & D. R. Brooks (eds.), Advances in cladistics: Proceedings of the first meeting of the Willi Hennig Society. New York Botanical Garden, Bronx.

  19. —,C. J. Humphries, B. D. Mishler &S. P. Churchill. 1987. On cladistic relationships in green plants. Taxon 36: 339–349.

  20. Brown, W. H. 1935. The plant kingdom: A textbook of general botany. Ginn & Company, Boston.

  21. Burns, G W. 1974. The plant kingdom. Macmillan, New York.

  22. Campbell, D. H. 1940. The evolution of land plants (Embryophyta). Stanford Univ. Press, Palo Alto, CA.

  23. Campbell, N. A., J. B. Reece &L. G. Mitchell. 1999. Biology. Ed. 5. Benjamin Cummings, CA.

  24. Cavalier-Smith, T. 1981. Eukaryote kingdoms, seven or nine? BioSystems 14: 461–481.

  25. Church, A. H. 1919. Thalassiophyta and the subaerial transmigration. Botanical Memoirs, 3. Oxford Univ. Press, Oxford.

  26. Croft, A. 1952. A newTrochiliscus (Charophyta) from the Downtownian of Podolia. Bull. Brit. Mus. (Nat. Hist), Geol. 1: 187–220.

  27. Cronquist, A. 1961. Introductory botany. Harper & Row, New York.

  28. Delevoryas, T. 1977. Plant diversification. Ed. 2. Holt, Rinehart & Winston, New York.

  29. Ditmer, H. J. 1964. Phylogeny and form in the plant kingdom. Van Nostrand, Toronto.

  30. Dodge, J. D. 1973. The fine structure of algal cells. Academic Press, London.

  31. Eames, A. J. 1936. Morphology of vascular plants: Lower groups (Psilophytales to Filicales). McGraw-Hill, New York.

  32. Foster, A. S. &E. M. Gifford. 1959. Comparative morphology of vascular plants. W. H. Freeman, San Francisco.

  33. Frederick, S. E., P. J. Gruber &N. E. Tolbert. 1973. The occurrence of glycolate dehydrogenase and glycolate oxidase in green plants: An evolutionary survey. Pl Physiol. (Lancaster) 52: 318–323.

  34. Fritsch, F. E. 1916. The algal ancestry of higher plants. New Phytol. 15: 233–250.

  35. —. 1935. The structure and reproduction of the algae. Vol. 1. Cambridge Univ. Press, Cambridge.

  36. Gifford, E. M. &A. S. Foster. 1989. Morphology and evolution of vascular plants. Ed. 3. W. H. Freeman, New York.

  37. Goebel, K. 1930. Organographie der Pflanzen. Ed. 3. G. Fischer, Jena, Germany.

  38. Graham, L. E. 1982. The occurrence, evolution, and phylogenetic significance of parenchyma inColeochaete Breb. (Chlorophyta). Amer. J. Bot. 69: 447–454.

  39. —. 1984.Coleochaete and the origin of land plants. Amer. J. Bot. 71: 603–608.

  40. —. 1985. The origin of the life cycle of land plants. Amer. Scientist 73: 178–186.

  41. —. 1993. Origin of land plants. Wiley & Sons, New York.

  42. — &L. W. Wilcox. 1983. The occurrence and phylogenetic significance of putative placental transfer cells in the green algaColeochaete. Amer. J. Bot. 70, 113–120.

  43. ——. 2000. Algae. Prentice Hall, Upper Saddle River, NJ.

  44. Gray, J. 1985. The microfossil record of early land plants: Advances in understanding of early terrestrialization. Pp. 167–195in W. G. Chaloner & J. D. Lawson (eds.), Evolution and environment in the late Silurian and early Devonian. Phil. Trans. Roy. Soc. London, B, 309.

  45. Green, P. B. 1962. Cell expansion. Pp. 625–632in R. A. Lewin (ed.), Physiology and biochemistry of algae. Academic Press, New York & London.

  46. Groover, R. D. &H. C. Bold. 1969. The taxonomy and comparative physiology of the Chlorosarcinales, and certain other edaphic algae. Phycological Studies, 8. Univ. of Texas, Austin.

  47. Haberlandt, G. 1914. Physiological plant anatomy. M. Drummond, trans. Macmillan, London.

  48. Haupt, A. W. 1953. Plant morphology. McGraw-Hill, New York.

  49. Hofmeister, W. 1851. Vergleichende Untersuchgungen. Friedrich Hofmeister, Leipzig, Germany.

  50. Jeffrey, C. 1962. The origin and differentiation of the archegoniate land-plants. Bot. Not. 115: 446–454.

  51. Kaplan, D. R. 2001. The science of plant morphology: Definition, history, and role in modern biology. Amer. J. Bot. 88: 1711–1741.

  52. Karol, K. G., R. M. McCourt, M. T. Cimino &C. F. Delwiche. 2001. The closest living relatives of land plants. Science 294: 2351–2353.

  53. Katana, A., J. Kwiatowski, K. Spalik &B. Zakrys. 2001. Phylogenetic position ofKoliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. J. Phycol. 37: 443–451.

  54. Kranz, H. D., D. Miks, M. L. Siegler, I. Capesius, C. W. Sensen &V. A. R. Huss. 1995. The origin of land plants: Phylogenetic relationship among charophytes, bryophytes, and vascular plants inferred from complete small-subunit ribosomal RNA sequences. J. Molec. Evol. 41: 74–84.

  55. Lee, R. E. 1999. Phycology. Ed. 3. Cambridge Univ. Press, Cambridge.

  56. Mandai, D. K. &S. Ray. 2001. Karyotype analysis and cytotaxonomic study in the genusNitella (Charophyceae). Phytomorphology 51: 27–32.

  57. Manhart, J. R. &J. D. Palmer. 1990. The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants. Nature 345: 268–270.

  58. Marchant, H. J. &J. D. Pickett-Heaps. 1973. Mitosis and cytokinesis inColeochaete scutata. J. Phycol. 9: 461–471.

  59. Mattox, K. R. &K. D. Stewart. 1984. Classification of the green algae: A concept based on comparative cytology. Pp. 29–72in D. E. G. Irvine & D. M. John (eds.), Systematics of the green algae. Academic Press, London & Orlando.

  60. McCourt, R. M. 1995. Green algal phylogeny. Trends Ecol. Evol. 10: 159–163.

  61. Melkonian, M. 1982. Structural and evolutionary aspects of the flagellar apparatus in green algae and land plants. Taxon 31: 255–265.

  62. Minkoff, E. C. 1983. Evolutionary biology. Addison Wesley, Reading, MA.

  63. Mishler, B. D. &S. P. Churchill. 1984. A cladistic approach to the phylogeny of the “bryophytes.” Brittonia 36: 406–424.

  64. ——. 1985. Transition to a land flora: Phylogenetic relationships of the green algae and bryophytes. Cladistics 1: 305–328.

  65. Nakayama, T., B. Marin, H. D. Kranz, B. Surek, I. Inouye &M. Melkonian. 1998. The basal position of scaly green flagellates among the green algae (Chlorophyta) is revealed by analyses of nuclearencoded SSU rRNA sequences. Protist 149: 367–380.

  66. Niklas, K. J. 1992. Plant biomechanics: An engineering approach to plant form and function. Univ. of Chicago Press, Chicago & London.

  67. —. 1994. Plant allometry: The scaling of form and process. Univ. of Chicago Press, Chicago & London.

  68. —. 1997. The evolutionary biology of plants. Univ. of Chicago Press, Chicago & London.

  69. Okuda, K. &R. M. Brown Jr. 1992. A new putative cellulose-synthesizing complex ofColeochaete scutata. Protoplasma 168: 51–63.

  70. Pickett-Heaps, J. D. 1975. Green algae: Structure, reproduction and evolution in selected genera. Sinauer Associates, Sunderland, MA.

  71. —. 1976. Cell division in eukaryotic algae. BioScience 26: 445–450.

  72. Prescott, G W. 1968. The algae: A review. Houghton-Mifflin, Boston.

  73. Pringsheim, N. 1878. Ueber Sprossung der Moosfruchte und den Generationswechsel der Thallophyten. Jahrb. Wiss. Bot. 11: 1–46.

  74. Pritchard, H. N. &P. T. Bradt. 1984. Biology of nonvascular plants. Times Mirror/Mosby, Saint Louis.

  75. Purves, W. K., G H. Orians, H. C. Heller &D. Savada. 1998. Life: The science of biology. Ed. 5. Sinauer, Sunderland, MA.

  76. Remy, W. &H. Hass. 1986. Das Ur—Landpflanzen-Konzept—unter besonderer Berucksichtigung der Organization Altdevonisher Gametophyten. Argum. Palaeobot. 7: 173–214.

  77. — &R. Remy. 1980. Devonian gametophytes with anatomically preserved gametangia. Science 208: 295–296.

  78. Renzaglia, K. S. &K. C. Vaughn. 2000. Anatomy, development and classification of hornworts. Pp. 1–20in A. H. Shaw & B. Goffinet (eds.), Bryophyte biology. Cambridge Univ. Press, Cambridge.

  79. Ruse, M. 1988. Philosophy of biology today. State Univ. Press of New York, Albany.

  80. Sattler, R. 1986. Biophilosophy: Analytic and holistic perspectives. Springer-Verlag, Berlin.

  81. —. 1998. On the origin of symmetry, branching and phyllotaxis in land plants. Pp. 775–793in R. V. Jean & D. Barabe (eds.), Symmetry in plants. World Scientific, Singapore.

  82. Scagel, R. F., R. J. Bandoni, J. R. Maze, G E. Rouse, W. B. Schofield &J. R. Stein. 1984. Plants: An evolutionary survey. Wadsworth, Belmont, CA.

  83. Schofield, W. B. 1985. Introduction to bryology. Macmillan, New York.

  84. Silva, P. C., K. R. Mattox &W. H. Blackwell. 1972. The generic nameHormidium as applied to green algae. Taxon 21: 639–345.

  85. Sluiman, H. J. 1985. A cladistic evaluation of the lower and higher green plants. Plant Syst. Evol. 149: 217–232.

  86. Smith, G M. 1938. Cryptogamic botany. Vol. 2. McGraw-Hill, New York & London.

  87. —. 1950. The fresh-water algae of the United States. Ed. 2. McGraw-Hill, New York.

  88. Solomon, E. P., L. R. Berg &D. W. Martin. 2002. Biology. Ed. 6. Brooks/Cole, South Melbourne, Australia.

  89. South, G R. &A. Whittick. 1987. Introduction to phycology. Blackwell Scientific, Oxford.

  90. Sporne, K. R. 1965. The morphology of gymnosperms: The structure and evolution of primitive seed-plants. Hutchinson, London.

  91. Stewart, K. D. &K. R. Mattox. 1975. Comparative cytology, evolution and classification of the green algae with some consideration of the origin of other organisms with chlorophylls a & b. Bot. Rev. (Lancaster) 41: 104–135.

  92. Stuessy, T. F. 1990. Plant taxonomy: The systematic evaluation of comparative data. Columbia Univ. Press, New York.

  93. Syrett, P. J. &F. A. A. Al-Houty. 1984. The phylogenetic significance of the occurrence of urease/urea amidolyase and glycolate oxidase/glycolate dehydrogenase in green algae. Brit. Phycol. J. 19: 11–21.

  94. Taylor, T. N. &E. L. Taylor. 1993. The biology and evolution of fossil plants. Prentice Hall, Englewood Cliffs, NJ.

  95. Theriot, E. 1988. A review of Sluiman’s cladistic classification of green plants with particular reference to flagella data and to land plant origins. Taxon 37: 913–919.

  96. Tippo, O. &W. L. Stern. 1977. Humanistic botany. W. W. Norton, New York.

  97. Vanden Hoek, C., D. G. Mann &H. M. Jahns. 1995. Algae: An introduction to phycology. Cambridge Univ. Press, Cambridge.

  98. Wardlaw, C. W. 1952. Phylogeny and morphogenesis: Contemporary aspects of botanical science. Macmillan, London.

  99. —. 1955. Embryogenesis in plants. Methuen, London.

  100. —. 1968. Essays on form in plants. Manchester Univ. Press, Manchester.

  101. Wolfe, S. L. 1983. Introduction to cell biology. Wadsworth, Belmont, CA.

  102. Zimmerman, W. 1930. Phylogenie der Pflanzen. G. Fischer, Jena, Germany.

  103. —. 1952. Main results of the telome theory. Palaeobotanist 1: 456–470.

Download references

Author information

Correspondence to Will H. Blackwell.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Blackwell, W.H. Two theories of origin of the land-plant sporophyte: Which is left standing?. Bot. Rev 69, 125 (2003). https://doi.org/10.1663/0006-8101(2003)069[0125:TTOOOT]2.0.CO;2

Download citation

Keywords

  • Green Alga
  • Botanical Review
  • Land Plant
  • Motile Cell
  • Homologous Theory