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Diagram showing the alternation of generations between a diploid sporophyte (bottom) and a haploid gametophyte (top)
Diagram showing the alternation of generations between a diploid sporophyte (bottom) and a haploid gametophyte (top)

Alternation of generations (also known as metagenesis or heterogenesis)[1] is the predominant type of life cycle in plants and algae. It consists of a multicellular haploid sexual phase, the gametophyte, which has a single set of chromosomes alternating with a multicellular diploid asexual phase, the sporophyte which has two sets of chromosomes.

A mature sporophyte produces haploid spores by meiosis, a process which reduces the number of chromosomes to half, from two sets to one. The resulting haploid spores germinate and grow into multicellular haploid gametophytes. At maturity, a gametophyte produces gametes by mitosis, the normal process of cell division in eukaryotes, which maintains the original number of chromosomes. Two haploid gametes (originating from different organisms of the same species or from the same organism) fuse to produce a diploid zygote, which divides repeatedly by mitosis, developing into a multicellular diploid sporophyte. This cycle, from gametophyte to sporophyte (or equally from sporophyte to gametophyte), is the way in which all land plants and most algae undergo sexual reproduction.

The relationship between the sporophyte and gametophyte phases varies among different groups of plants. In the majority of algae, the sporophyte and gametophyte are separate independent organisms, which may or may not have a similar appearance. In liverworts, mosses and hornworts, the sporophyte is less well developed than the gametophyte and is largely dependent on it. Although moss and hornwort sporophytes can photosynthesise, they require additional photosynthate from the gametophyte to sustain growth and spore development and depend on it for supply of water, mineral nutrients and nitrogen.[2][3] By contrast, in all modern vascular plants the gametophyte is less well developed than the sporophyte, although their Devonian ancestors had gametophytes and sporophytes of approximately equivalent complexity.[4] In ferns the gametophyte is a small flattened autotrophic prothallus on which the young sporophyte is briefly dependent for its nutrition. In flowering plants, the reduction of the gametophyte is much more extreme; it consists of just a few cells which grow entirely inside the sporophyte.

Animals develop differently. They directly produce haploid gametes. No haploid spores capable of dividing are produced, so generally there is no multicellular haploid phase. (Some insects have a sex-determining system whereby haploid males are produced from unfertilized eggs; however females produced from fertilized eggs are diploid.)

Life cycles of plants and algae with alternating haploid and diploid multicellular stages are referred to as diplohaplontic (the equivalent terms haplodiplontic, diplobiontic and dibiontic are also in use, as is describing such an organism as having a diphasic ontogeny[5]). Life cycles, such as those of animals, in which there is only a diploid multicellular stage are referred to as diplontic. Life cycles in which there is only a haploid multicellular stage are referred to as haplontic.

Definition

Alternation of generations is defined as the alternation of multicellular diploid and haploid forms in the organism's life cycle, regardless of whether these forms are free-living.[6] In some species, such as the alga Ulva lactuca, the diploid and haploid forms are indeed both free-living independent organisms, essentially identical in appearance and therefore said to be isomorphic. The free-swimming, haploid gametes form a diploid zygote which germinates into a multicellular diploid sporophyte. The sporophyte produces free-swimming haploid spores by meiosis that germinate into haploid gametophytes.[7]

However, in some other groups, either the sporophyte or the gametophyte is very much reduced and is incapable of free living. For example, in all bryophytes the gametophyte generation is dominant and the sporophyte is dependent on it. By contrast, in all modern vascular land plants the gametophytes are strongly reduced, although the fossil evidence indicates that they were derived from isomorphic ancestors.[4] In seed plants, the female gametophyte develops totally within the sporophyte, which protects and nurtures it and the embryonic sporophyte that it produces. The pollen grains, which are the male gametophytes, are reduced to only a few cells (just three cells in many cases). Here the notion of two generations is less obvious; as Bateman & Dimichele say "[s]porophyte and gametophyte effectively function as a single organism".[8] The alternative term 'alternation of phases' may then be more appropriate.[9]

History

Debates about alternation of generations in the early twentieth century can be confusing because various ways of classifying "generations" co-exist (sexual vs. asexual, gametophyte vs. sporophyte, haploid vs. diploid, etc.).[10]

Initially, Chamisso and Steenstrup described the succession of differently organized generations (sexual and asexual) in animals as "alternation of generations", while studying the development of tunicates, cnidarians and trematode animals.[10] This phenomenon is also known as heterogamy. Presently, the term "alternation of generations" is almost exclusively associated with the life cycles of plants, specifically with the alternation of haploid gametophytes and diploid sporophytes.[10]

Wilhelm Hofmeister demonstrated the morphological alternation of generations in plants,[11] between a spore-bearing generation (sporophyte) and a gamete-bearing generation (gametophyte).[12][13] By that time, a debate emerged focusing on the origin of the asexual generation of land plants (i.e., the sporophyte) and is conventionally characterized as a conflict between theories of antithetic (Čelakovský, 1874) and homologous (Pringsheim, 1876) alternation of generations.[10] Čelakovský coined the words sporophyte and gametophyte.[citation needed]

Eduard Strasburger (1874) discovered the alternation between diploid and haploid nuclear phases,[10] also called cytological alternation of nuclear phases.[14] Although most often coinciding, morphological alternation and nuclear phases alternation are sometimes independent of one another, e.g., in many red algae, the same nuclear phase may correspond to two diverse morphological generations.[14] In some ferns which lost sexual reproduction, there is no change in nuclear phase, but the alternation of generations is maintained.[15]

Alternation of generations in plants

Fundamental elements

The diagram above shows the fundamental elements of the alternation of generations in plants. The many variations found in different groups of plants are described by use of these concepts later in the article. Starting from the right of the diagram, the processes involved are as follows:[16]

The 'alternation of generations' in the life cycle is thus between a diploid (2n) generation of sporophytes and a haploid (n) generation of gametophytes.

Gametophyte of the fern Onoclea sensibilis (the flat thallus at the bottom of the picture) with a descendant sporophyte beginning to grow from it (the small frond at the top of the picture).
Gametophyte of the fern Onoclea sensibilis (the flat thallus at the bottom of the picture) with a descendant sporophyte beginning to grow from it (the small frond at the top of the picture).

The situation is quite different from that in animals, where the fundamental process is that a diploid (2n) individual directly produces haploid (n) gametes by meiosis. In animals, spores (i.e. haploid cells which are able to undergo mitosis) are not produced, so there is no asexual multi-cellular generation. Some insects have haploid males that develop from unfertilized eggs, but the females are all diploid.

Variations

The diagram shown above is a good representation of the life cycle of some multi-cellular algae (e.g. the genus Cladophora) which have sporophytes and gametophytes of almost identical appearance and which do not have different kinds of spores or gametes.[17]

However, there are many possible variations on the fundamental elements of a life cycle which has alternation of generations. Each variation may occur separately or in combination, resulting in a bewildering variety of life cycles. The terms used by botanists in describing these life cycles can be equally bewildering. As Bateman and Dimichele say "[...] the alternation of generations has become a terminological morass; often, one term represents several concepts or one concept is represented by several terms."[18]

Possible variations are:

There are some correlations between these variations, but they are just that, correlations, and not absolute. For example, in flowering plants, microspores ultimately produce microgametes (sperm) and megaspores ultimately produce megagametes (eggs). However, in ferns and their allies there are groups with undifferentiated spores but differentiated gametophytes. For example, the fern Ceratopteris thalictrioides has spores of only one kind, which vary continuously in size. Smaller spores tend to germinate into gametophytes which produce only sperm-producing antheridia.[27]

A complex life cycle

Graphic referred in text.
Graphic referred in text.

The diagram shows the alternation of generations in a species which is heteromorphic, sporophytic, oogametic, dioicous, heterosporic and dioecious. A seed plant example might be a willow tree (most species of the genus Salix are dioecious).[28] Starting in the centre of the diagram, the processes involved are:

Life cycles of different plant groups

The term "plants" is taken here to mean the Archaeplastida, i.e. the glaucophytes, red and green algae and land plants.

Alternation of generations occurs in almost all multicellular red and green algae, both freshwater forms (such as Cladophora) and seaweeds (such as Ulva). In most, the generations are homomorphic (isomorphic) and free-living. Some species of red algae have a complex triphasic alternation of generations, in which there is a gametophyte phase and two distinct sporophyte phases. For further information, see Red algae: Reproduction.

Land plants all have heteromorphic (anisomorphic) alternation of generations, in which the sporophyte and gametophyte are distinctly different. All bryophytes, i.e. liverworts, mosses and hornworts, have the gametophyte generation as the most conspicuous. As an illustration, consider a monoicous moss. Antheridia and archegonia develop on the mature plant (the gametophyte). In the presence of water, the biflagellate sperm from the antheridia swim to the archegonia and fertilisation occurs, leading to the production of a diploid sporophyte. The sporophyte grows up from the archegonium. Its body comprises a long stalk topped by a capsule within which spore-producing cells undergo meiosis to form haploid spores. Most mosses rely on the wind to disperse these spores, although Splachnum sphaericum is entomophilous, recruiting insects to disperse its spores. For further information, see Liverwort: Life cycle, Moss: Life cycle, Hornwort: Life cycle.

In ferns and their allies, including clubmosses and horsetails, the conspicuous plant observed in the field is the diploid sporophyte. The haploid spores develop in sori on the underside of the fronds and are dispersed by the wind (or in some cases, by floating on water). If conditions are right, a spore will germinate and grow into a rather inconspicuous plant body called a prothallus. The haploid prothallus does not resemble the sporophyte, and as such ferns and their allies have a heteromorphic alternation of generations. The prothallus is short-lived, but carries out sexual reproduction, producing the diploid zygote that then grows out of the prothallus as the sporophyte. For further information, see Fern: Life cycle.

In the spermatophytes, the seed plants, the sporophyte is the dominant multicellular phase; the gametophytes are strongly reduced in size and very different in morphology. The entire gametophyte generation, with the sole exception of pollen grains (microgametophytes), is contained within the sporophyte. The life cycle of a dioecious flowering plant (angiosperm), the willow, has been outlined in some detail in an earlier section (A complex life cycle). The life cycle of a gymnosperm is similar. However, flowering plants have in addition a phenomenon called 'double fertilization'. Two sperm nuclei from a pollen grain (the microgametophyte), rather than a single sperm, enter the archegonium of the megagametophyte; one fuses with the egg nucleus to form the zygote, the other fuses with two other nuclei of the gametophyte to form 'endosperm', which nourishes the developing embryo. For further information, see Double fertilization.

Evolution of the dominant diploid phase

It has been proposed that the basis for the emergence of the diploid phase of the life cycle (sporophyte) as the dominant phase (e.g. as in vascular plants) is that diploidy allows masking of the expression of deleterious mutations through genetic complementation.[29][30] Thus if one of the parental genomes in the diploid cells contained mutations leading to defects in one or more gene products, these deficiencies could be compensated for by the other parental genome (which nevertheless may have its own defects in other genes). As the diploid phase was becoming predominant, the masking effect likely allowed genome size, and hence information content, to increase without the constraint of having to improve accuracy of DNA replication. The opportunity to increase information content at low cost was advantageous because it permitted new adaptations to be encoded. This view has been challenged, with evidence showing that selection is no more effective in the haploid than in the diploid phases of the lifecycle of mosses and angiosperms.[31]

Similar processes in other organisms

Rhizaria

Life cycle of Foraminifera showing alternation of generations.
Life cycle of Foraminifera showing alternation of generations.

Some organisms currently classified in the clade Rhizaria and thus not plants in the sense used here, exhibit alternation of generations. Most Foraminifera undergo a heteromorphic alternation of generations between haploid gamont and diploid agamont forms. The single-celled haploid organism is typically much larger than the diploid organism.

Fungi

Fungal mycelia are typically haploid. When mycelia of different mating types meet, they produce two multinucleate ball-shaped cells, which join via a "mating bridge". Nuclei move from one mycelium into the other, forming a heterokaryon (meaning "different nuclei"). This process is called plasmogamy. Actual fusion to form diploid nuclei is called karyogamy, and may not occur until sporangia are formed. Karogamy produces a diploid zygote, which is a short-lived sporophyte that soon undergoes meiosis to form haploid spores. When the spores germinate, they develop into new mycelia.

Slime moulds

The life cycle of slime moulds is very similar to that of fungi. Haploid spores germinate to form swarm cells or myxamoebae. These fuse in a process referred to as plasmogamy and karyogamy to form a diploid zygote. The zygote develops into a plasmodium, and the mature plasmodium produces, depending on the species, one to many fruiting bodies containing haploid spores.

Animals

Alternation between a multicellular diploid and a multicellular haploid generation is never encountered in animals.[32] In some animals, there is an alternation between parthenogenic and sexually reproductive phases (heterogamy). Both phases are diploid. This has sometimes been called "alternation of generations",[33] but is quite different. In some other animals, such as hymenopterans, males are haploid and females diploid, but this is always the case rather than there being an alternation between distinct generations.

See also

Notes and references

  1. ^ "alternation of generations | Definition & Examples". Encyclopedia Britannica. Retrieved 2021-02-25.
  2. ^ Thomas, R.J.; Stanton, D.S.; Longendorfer, D.H. & Farr, M.E. (1978), "Physiological evaluation of the nutritional autonomy of a hornwort sporophyte", Botanical Gazette, 139 (3): 306–311, doi:10.1086/337006, S2CID 84413961
  3. ^ Glime, J.M. (2007), Bryophyte Ecology: Vol. 1 Physiological Ecology (PDF), Michigan Technological University and the International Association of Bryologists, retrieved 2013-03-04
  4. ^ a b Kerp, H.; Trewin, N.H. & Hass, H. (2003), "New gametophytes from the Lower Devonian Rhynie Chert", Transactions of the Royal Society of Edinburgh: Earth Sciences, 94 (4): 411–428, doi:10.1017/S026359330000078X, S2CID 128629425
  5. ^ Kluge, Arnold G.; Strauss, Richard E. (1985). "Ontogeny and Systematics". Annual Review of Ecology and Systematics. 16: 247–268. doi:10.1146/annurev.es.16.110185.001335. ISSN 0066-4162. JSTOR 2097049.
  6. ^ Taylor, Kerp & Hass 2005
  7. ^ ""Plant Science 4 U". Retrieved 5 July 2016.
  8. ^ a b Bateman & Dimichele 1994, p. 403
  9. ^ a b Stewart & Rothwell 1993
  10. ^ a b c d e Haig, David (2008), "Homologous versus antithetic alternation of generations and the origin of sporophytes" (PDF), The Botanical Review, 74 (3): 395–418, doi:10.1007/s12229-008-9012-x, S2CID 207403936, retrieved 2014-08-17
  11. ^ Svedelius, Nils (1927), "Alternation of Generations in Relation to Reduction Division", Botanical Gazette, 83 (4): 362–384, doi:10.1086/333745, JSTOR 2470766, S2CID 84406292
  12. ^ Hofmeister, W. (1851), Vergleichende Untersuchungen der Keimung, Entfaltung und Fruchtbildildiung höherer Kryptogamen (Moose, Farne, Equisetaceen, Rhizocarpeen und Lycopodiaceen) und der Samenbildung der Coniferen (in German), Leipzig: F. Hofmeister, retrieved 2014-08-17. Translated as Currey, Frederick (1862), On the germination, development, and fructification of the higher Cryptogamia, and on the fructification of the Coniferæ, London: Robert Hardwicke, retrieved 2014-08-17
  13. ^ Feldmann, J. & Feldmann, G. (1942), "Recherches sur les Bonnemaisoniacées et leur alternance de generations" (PDF), Ann. Sci. Natl. Bot., Series 11 (in French), 3: 75–175, archived from the original (PDF) on 2014-08-19, retrieved 2013-10-07, p. 157
  14. ^ a b Feldmann, J. (1972), "Les problèmes actuels de l'alternance de génerations chez les Algues", Bulletin de la Société Botanique de France (in French), 119: 7–38, doi:10.1080/00378941.1972.10839073
  15. ^ Schopfer, P.; Mohr, H. (1995). "Physiology of Development". Plant physiology. Berlin: Springer. pp. 288–291. ISBN 978-3-540-58016-4.
  16. ^ Unless otherwise indicated, the material in the whole of this section is based on Foster & Gifford 1974, Sporne 1974a and Sporne 1974b.
  17. ^ Guiry & Guiry 2008
  18. ^ Bateman & Dimichele 1994, p. 347
  19. ^ a b Shyam 1980
  20. ^ Watson 1981, p. 2
  21. ^ Kirby 2001
  22. ^ Watson 1981, p. 33
  23. ^ Bell & Hemsley 2000, p. 104
  24. ^ Watson 1981, pp. 425–6
  25. ^ Watson 1981, pp. 287–8
  26. ^ Sporne 1974a, pp. 17–21.
  27. ^ a b Bateman & Dimichele 1994, pp. 350–1
  28. ^ Chisholm, Hugh, ed. (1911). "Willow" . Encyclopædia Britannica. Vol. 28 (11th ed.). Cambridge University Press. pp. 688–689.
  29. ^ Bernstein, H.; Byers, G.S. & Michod, R.E. (1981), "Evolution of sexual reproduction: Importance of DNA repair, complementation, and variation", The American Naturalist, 117 (4): 537–549, doi:10.1086/283734, S2CID 84568130
  30. ^ Michod, R.E. & Gayley, T.W. (1992), "Masking of mutations and the evolution of sex", The American Naturalist, 139 (4): 706–734, doi:10.1086/285354, S2CID 85407883
  31. ^ Szövényi, Péter; Ricca, Mariana; Hock, Zsófia; Shaw, Jonathan A.; Shimizu, Kentaro K. & Wagner, Andreas (2013), "Selection is no more efficient in haploid than in diploid life stages of an angiosperm and a moss", Molecular Biology and Evolution, 30 (8): 1929–39, doi:10.1093/molbev/mst095, PMID 23686659
  32. ^ Barnes et al. 2001, p. 321
  33. ^ Scott 1996, p. 35

Bibliography