Alternation of generations

Alternation of generations (also known as alternation of phases or metagenesis) is a term primarily used in describing the life cycle of plants (taken here to mean the Archaeplastida). A multicellular sporophyte, which is diploid with 2N paired chromosomes (i.e. N pairs), alternates with a multicellular gametophyte, which is haploid with N unpaired chromosomes. A mature sporophyte produces spores by meiosis, a process which results in a reduction of the number of chromosomes by a half. Spores germinate and grow into a gametophyte. At maturity, the gametophyte produces gametes by mitosis, which does not alter the number of chromosomes. Two gametes (originating from different organisms of the same species or from the same organism) fuse to produce a zygote, which develops into a diploid sporophyte. This cycle, from sporophyte to sporophyte (or equally from gametophyte to gametophyte), is the way in which all land plants and many algae undergo sexual reproduction.

The relationship between the sporophyte and gametophyte varies among different groups of plants. In those algae which have alternation of generations, 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, being entirely dependent on it in the first two groups. By contrast, the fern gametophyte is less well developed than the sporophyte, forming a small flattened thallus. In flowering plants, the reduction of the gametophyte is even more extreme; it consists of just a few cells which grow entirely inside the sporophyte.

All animals develop differently. A mature animal is diploid and so is, in one sense, equivalent to a sporophyte. However, an animal directly produces haploid gametes by meiosis. No haploid spores capable of dividing are produced, so neither is a haploid gametophyte. There is no alternation between diploid and haploid forms.

Other organisms, such as fungi, can have life cycles in which different kinds of organism alternate. The term 'alternation of generations' has also been applied to these cases.^{[citation needed]}

Life cycles, such as those of plants, with alternating haploid and diploid phases can be referred to as diplohaplontic (the equivalent terms haplodiplontic, diplobiontic or dibiontic are also in use). Life cycles, such as those of animals, in which there is only a diploid phase are referred to as diplontic. (Life cycles in which there is only a haploid phase are referred to as haplontic.)

Definition

The discussion of 'alternation of generations' above treats the alternation of a multicellular diploid form with a multicellular haploid form as the defining characteristic, regardless of whether these forms are free-living or not.^[1] 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. The free-swimming gametes form a zygote which germinates into a diploid sporophyte; the free-swimming spores germinate into a haploid gametophyte.

However, in other species, either the sporophyte or the gametophyte is very much reduced and is incapable of free living. For example, in seed plants, the gametophyte generation develops totally within the sporophyte which protects and nurtures it, with the sole exception of pollen grains, which are the male gametophytes, but which have been reduced to only three cells. Here the notion of two generations is less obvious; as Bateman & Dimichele say "[s]porophyte and gametophyte effectively function as a single organism".^[2] The alternative term 'alternation of phases' may then be more appropriate.^[3]

Alternation of generations in plants

Fundamental elements

The diagram below shows the fundamental elements of the alternation of generations in plants. It is vital to have a good understanding of these fundamentals before considering the many variations found in different groups of plants. Starting from the right of the diagram, the processes involved are as follows:^[4]

• Two single-celled haploid gametes, each containing N unpaired chromosomes, fuse to form a single-celled diploid zygote, which now contains N pairs of chromosomes, i.e. 2N chromosomes in total.
• The single-celled diploid zygote germinates, dividing by the normal process (mitosis), which maintains the number of chromosomes at 2N. The result is a multi-cellular diploid organism, called the sporophyte (because at maturity it produces spores).
• When it reaches maturity, the sporophyte produces one or more sporangia (singular sporangium) which are the organs which produce diploid spore mother cells (sporocytes). These divide by a special process (meiosis) which reduces the number of chromosomes by a half. This results in four single-celled haploid spores, each containing N unpaired chromosomes.
• The single-celled haploid spore germinates, dividing by the normal process (mitosis), which maintains the number of chromosomes at N. The result is a multi-cellular haploid organism, called the gametophyte (because at maturity it produces gametes).
• When it reaches maturity, the gametophyte produces one or more gametangia (singular gametangium) which are the organs which produce haploid gametes. At least one kind of gamete possesses some mechanism for reaching another gamete in order to fuse with it.

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).

The situation is quite different in all animals, where the fundamental process is that a diploid (2N) individual directly produces haploid (N) gametes by meiosis. Spores (i.e. haploid cells which are able to undergo mitosis) are not produced, so neither is a haploid multi-cellular organism. The single-celled gametes are the only entities which are haploid.

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 very similar, if not identical, appearance, and which do not have different kinds of spores or gametes.^[5]

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."^[6]

Possible variations are:

• Relative importance of the sporophyte and the gametophyte.
  • Equal (homomorphy or isomorphy).
    Filamentous algae of the genus Cladophora, which are predominantly found in fresh water, have diploid sporophytes and haploid gametophytes which are externally indistinguishable.^[7] No living land plant has equally dominant sporophytes and gametophytes, although some theories of the evolution of alternation of generations suggest that ancestral land plants did.
  • Unequal (heteromorphy or anisomorphy).
    

    Gametophyte of Mnium hornum, a moss.
    • Dominant gametophyte (gametophytic).
      In liverworts, mosses and hornworts, the dominant form is the haploid gametophyte. The diploid sporophyte is not capable of an independent existence, gaining most of its nutrition from the parent gametophyte, and having no chlorophyll when mature.^[8]
      

      Sporophyte of Blechnum discolor, a fern.
    • Dominant sporophyte (sporophytic).
      In ferns, both the sporophyte and the gametophyte are capable of living independently, but the dominant form is the diploid sporophyte. The haploid gametophyte is much smaller and simpler in structure. In seed plants, the gametophyte is even more reduced (at the minimum to only three cells), gaining all its nutrition from the sporophyte. The extreme reduction in the size of the gametophyte and its retention within the sporophyte means that when applied to seed plants the term 'alternation of generations' is somewhat misleading: "[s]porophyte and gametophyte effectively function as a single organism".^[2] Some authors have preferred the term 'alternation of phases'.^[3]
• Differentiation of the gametes.
  • Both gametes the same (isogamy).
    Like other species of Cladophora, C. callicoma has flagellated gametes which are identical in appearance and ability to move.^[7]
  • Gametes of two distinct sizes (anisogamy).
    • Both of similar motility.
      Species of Ulva, the sea lettuce, have gametes which all have two flagella and so are motile. However they are of two sizes: larger 'female' gametes and smaller 'male' gametes.^[9]
    • One large and sessile, one small and motile (oogamy). The larger sessile megagametes are eggs (ova), and smaller motile microgametes are sperm (spermatazoa, spermatozoids). The degree of motility of the sperm may be very limited (as in the case of flowering plants) but all are able to move towards the sessile eggs. When (as is almost always the case) the sperm and eggs are produced in different kinds of gametangia, the sperm-producing ones are called antheridia (singular antheridium) and the egg-producing ones archegonia (singular archegonium).
      

      Gametophyte of Pellia epiphylla with sporophytes growing from the remains of archegonia.
      • Antheridia and archegonia occur on the same gametophyte, which is then called monoicous. (Many sources, including those concerned with bryophytes, use the term 'monoecious' for this situation and 'dioecious' for the opposite.^[10][11] Here 'monoecious' and 'dioecious' are used only for sporophytes.)
        The liverwort Pellia epiphylla has the gametophyte as the dominant generation. It is monoicous: the small reddish sperm-producing antheridia are scattered along the midrib while the egg-producing archegonia grow nearer the tips of divisions of the plant.^[12]
      • Antheridia and archegonia occur on different gametophytes, which are then called dioicous.
        The moss Mnium hornum has the gametophyte as the dominant generation. It is dioicous: male plants produce only antheridia in terminal rosettes, female plants produce only archegonia in the form of stalked capsules.^[13] Seed plants are also dioicous; however, the extreme reduction of the gametophyte, particularly the microgametophyte, means that the antheridia and archegonia are microscopic.
• Differentiation of the spores.
  • All spores the same size (homospory or isospory).
    Horsetails (species of Equisetum) have spores which are all of the same size.^[14]
  • Spores of two distinct sizes (heterospory or anisospory): larger megaspores and smaller microspores. When the two kinds of spore are produced in different kinds of sporangia, these are called megasporangia and microsporangia. A megaspore often (but not always) develops at the expense of the other three cells resulting from meiosis, which abort.
    • Megasporangia and microsporangia occur on the same sporophyte, which is then called monoecious.
      Most flowering plants fall into this category. Thus the flower of a lily contains six stamens (the microsporangia) which produce microspores which develop into pollen grains (the microgametophytes), and three fused carpels (the megasporangia) which produce megaspores which develop into ovules (the megagametophytes). In other plants, such as hazel, some flowers have only stamens, others only carpels, but the same plant (i.e. sporophyte) has both kinds of flower and so is monoecious.
      

      Flowers of European Holly, a dioecious species: male above, female below (leaves cut to show flowers more clearly)
    • Megasporangia and microsporangia occur on different sporophytes, which are then called dioecious.
      An individual tree of the European holly (Ilex aquifolium) produces either 'male' flowers which have only functional stamens (microsporangia) producing microspores which develop into pollen grains (microgametophytes) or 'female' flowers which have only functional carpels (megasporangia) producing megaspores which develop into ovules (megagametophytes).

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.^[14]

A complex life cycle

The diagram shows the alternation of generations in a species which is heteromorphic, sporophytic, oogametic, dioicous, heterosporic and dioecious. A seed plant example is a willow tree (genus Salix).^[15] Starting in the centre of the diagram, the processes involved are:

• An immobile egg, typically remaining in the archegonium, fuses with a mobile sperm, released from an antheridium. The resulting zygote is either 'male' or 'female'.
• A 'male' zygote develops by mitosis into a microsporophyte, which at maturity produces one or more microsporangia. Microspores develop within the microsporangium by meiosis.
  In a willow (like all seed plants) the zygote first develops into a seed within the ovule (megasporangium). Later the seed is shed and grows into a mature tree. A 'male' willow tree (a microsporophyte) produces flowers with only stamens, the anthers of which are the microsporangia.
• Microspores germinate producing microgametophytes; at maturity one or more antheridia are produced. Sperm develop within the antheridia.
  In a willow, microspores are not liberated from the anther (the microsporangium), but develop into pollen grains (microgametophytes) within it. The whole pollen grain is moved (typically by an insect) to an ovule (megagametophyte), where a sperm is produced which moves down a pollen tube to reach the egg.
• A 'female' zygote develops by mitosis into a megasporophyte, which at maturity produces one or more megasporangia. Megaspores develop within the megasporangium; typically one of the four spores produced by meiosis gains bulk at the expense of the remaining three, which disappear.
  'Female' willow trees (megasporophytes) produce flowers with only carpels (the megasporangia).
• Megaspores germinate producing megagametophytes; at maturity one or more archegonia are produced. Eggs develop within the archegonia.
  In a willow, megaspores develop into ovules (megagametophytes) within the carpels (megasporangia). An archegonium develops within the ovule and produces an egg. All of this happens within the carpel (the megasporangium). The whole of the gametophytic 'generation' remains within the protection of the sporophyte except for pollen grains (which have been reduced to just three cells).
  

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. For further information, see Liverwort: Life cycle, Moss: Life cycle, Hornwort: Life cycle.

• 

  Diagram of alternation of generations in liverworts.

• 

  Moss life cycle diagram

• 

  Hornwort life cycle diagram

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.

• 

  Diagram of alternation of generations in ferns.
• 

  A gametophyte (prothallus) of Dicksonia sp.
• 

  A sporophyte of Dicksonia antarctica.
• 

  The underside of a Dicksonia antarctica frond showing the sori, or spore-producing structures.

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.

• 

  Angiosperm life cycle

• 

  Tip of tulip stamen showing pollen (microgametophytes)

• 

  Plant ovules (megagametophytes): Gymnosperm ovule on left, angiosperm ovule (inside ovary) on right

• 

  Double fertilization

Other groups of organism

Some organisms currently classified in the Chromalveolata, and thus not plants in the sense used here, exhibit alternation of generations. Kelp are an example of a brown alga with a heteromorphic alternation of generations. Species from the genus Laminaria have a large sporophytic thallus that produces haploid spores which germinate to produce free-living microscopic male and female gametophytes. 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.

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.

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.

In some animals, there is an alternation between parthenogenic and sexually reproductive phases (heterogamy). Although in some ways similar to alternation of generations, the genetics of heterogamy is significantly different.^{[citation needed]}

See also

• Evolutionary history of plants#life cycles: Evolutionary origin of the alternation of phases

Notes and references

1. ^ Taylor, Kerp & Hass 2005
2. ^ ^{a b} Bateman & Dimichele 1994, p. 403
3. ^ ^{a b} Stewart & Rothwell 1993
4. ^ Unless otherwise indicated, the material in the whole of this section is based on Foster & Gifford 1974, Sporne 1974a and Sporne 1974b.
5. ^ Guiry & Guiry 2008
6. ^ Bateman & Dimichele 1994, p. 347
7. ^ ^{a b} Shyam 1980
8. ^ Watson 1981, p. 2
9. ^ Kirby 2001
10. ^ Watson 1981, p. 33
11. ^ Bell & Hemsley 2000, p. 104
12. ^ Watson 1981, pp. 425–6
13. ^ Watson 1981, pp. 287–8
14. ^ ^{a b} Bateman & Dimichele 1994, pp. 350–1
15. ^ "Willows", Encyclopædia Britannica, XIX (11th ed.), New York: Encyclopædia Britannica, 1911, http://en.wikisource.org/wiki/Page:EB1911_-_Volume_28.djvu/708, retrieved 2011-01-01 

Bibilography

• Bateman, R.M. & Dimichele, W.A. (1994), "Heterospory – the most iterative key innovation in the evolutionary history of the plant kingdom", Biological Reviews of the Cambridge Philosophical Society 69: 315–417, http://si-pddr.si.edu/dspace/bitstream/10088/7107/1/paleo_1994_BatemanDiMichele_Heterospory_BiolRev_small.pdf, retrieved 2010-12-30 
• Bell, P.R. & Hemsley, A.R. (2000), Green Plants: their Origin and Diversity (2nd ed.), Cambridge, etc.: Cambridge University Press, ISBN 978-0-521-64109-8 
• Foster, A.S. & Gifford, E.M. (1974), Comparative Morphology of Vascular Plants (2nd ed.), San Francisco: W.H. Freeman, ISBN 978-0-7167-0712-7 
• Guiry, M.D.; Guiry, G.M. (2008), "Cladophora", AlgaeBase (World-wide electronic publication, National University of Ireland, Galway), http://www.algaebase.org/search/genus/detail/?genus_id=37, retrieved 2011-07-21 
• Kirby, A. (2001), Ulva, the sea lettuce, Monterey Bay Aquarium Research Institute, http://www.mbari.org/staff/conn/botany/greens/anna/frontpages/default.htm, retrieved 2011-01-01 
• Shyam, R. (1980), "On the life-cycle, cytology and taxonomy of Cladophora callicoma from India", American Journal of Botany 67 (5): 619–24, doi:10.2307/2442655, JSTOR 2442655 
• Sporne, K.R. (1974a), The Morphology of Angiosperms, London: Hutchinson, ISBN 978-0-09-120611-6 
• Sporne, K.R. (1974b), The Morphology of Gymnosperms (2nd ed.), London: Hutchinson, ISBN 978-0-09-077152-3 
• Stewart, W.N. & Rothwell, G.W. (1993), Paleobotany and the Evolution of Plants (2nd ed.), Cambridge, UK: Cambridge University Press, ISBN 978-0-521-38294-6 
• Watson, E.V. (1981), British Mosses and Liverworts (3rd ed.), Cambridge, UK: Cambridge University Press, ISBN 978-0-521-28536-0 
• Taylor, T.N.; Kerp, H. & Hass, H. (2005), "Life history biology of early land plants: Deciphering the gametophyte phase", Proceedings of the National Academy of Sciences 102 (16): 5892–5897, doi:10.1073/pnas.0501985102, PMC 556298, PMID 15809414, http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=556298