In botany, apomixis was defined by Winkler as replacement of the normal sexual reproduction by asexual reproduction, without fertilization.[1] This definition notably does not mention meiosis. Thus "normal asexual reproduction" of plants, such as propagation from cuttings or leaves, has never been considered to be apomixis, but replacement of the seed by a plantlet, or replacement of the flower by bulbils are types of apomixis. Apomictically produced offspring are genetically identical to the parent plant.

In flowering plants, the term "apomixis" is commonly used in a restricted sense to mean agamospermy, i.e. asexual reproduction through seeds.

Apogamy is a related term that has had various meanings over time. In plants with independent gametophytes (notably ferns), the term is still used interchangeably with "apomixis", and both refer to the formation of sporophytes by parthenogenesis of gametophyte cells.

See also Male apomixis in a conifer below.


Apomixis and evolution

As apomictic plants are genetically identical from one generation to the next, each has the characters of a true species, maintaining distinctions from other congeneric apomicts, while having much smaller differences than is normal between species of most genera. They are therefore often called microspecies. In some genera, it is possible to identify and name hundreds or even thousands of microspecies, which may be grouped together as aggregate species, typically listed in Floras with the convention "Genus species agg." (e.g., the bramble, Rubus fruticosus agg.). In some plant families, genera with apomixis are quite common, e.g. in Asteraceae, Poaceae, and Rosaceae. Examples of apomixis can be found in the genera Crataegus (hawthorns), Amelanchier (shadbush), Sorbus (rowans and whitebeams), Rubus (brambles or blackberries), Poa (meadow grasses), Hieracium (hawkweeds) and Taraxacum (dandelions).

Although the evolutionary advantages of sexual reproduction are lost, apomixis can pass along traits fortuitous for evolutionary fitness. As Clausen eloquently put it[2] (page 470) "The apomicts actually have discovered the effectiveness of mass production long before Mr Henry Ford applied it to the production of the automobile. ... Facultative apomixis ... does not prevent variation; rather, it multiplies certain varietal products." Facultative apomixis means that apomixis does not always occur, i.e. sexual reproduction also can happen. It appears likely[3] that in plants all apomixis is facultative, i.e. that "obligate apomixis" is an artifact of the observation methods. Böcher[4] noted that facultative apomictic plants increased sexual seed set under stress conditions.

Apomixis in non-flowering plants

Apospory in ferns

Apomixis in flowering plants (angiosperms)

Agamospermy, asexual reproduction through seeds, occurs in flowering plants through many different mechanisms[3] and a simple hierarchical classification of the different types is not possible. Consequently there are almost as many different usages of terminology for apomixis in angiosperms as there are authors on the subject. For English speakers, Maheshwari 1950[5] is very influential. German speakers might prefer to consult Rutishauser 1967.[6] Some older text books[7] on the basis of misinformation (that the egg cell in a meiotically unreduced gametophyte can never be fertilized) attempted to reform the terminology to match parthenogenesis as it is used in zoology, and this continues to cause much confusion.

Agamospermy occurs mainly in two forms: In gametophytic apomixis, the embryo arises from an unfertilized egg cell (i.e. by parthenogenesis) in a gametophyte that was produced from a cell that did not complete meiosis. In adventitious embryony (sporophytic apomixis), an embryo is formed directly (not from a gametophyte) from nucellus or integument tissue (see nucellar embryony).

Types of apomixis in flowering plants

Maheshwari[5] used the following simple classification of types of apomixis in flowering plants:

  • Nonrecurrent apomixis: In this type "the megaspore mother cell undergoes the usual meiotic divisions and a haploid embryo sac is formed. The new embryo may then arise either from the egg (haploid parthenogenesis) or from some other cell of the gametophyte (haploid apogamy)." The haploid plants have half as many chromosomes as the mother plant, and "the process is not repeated from one generation to another" (which is why it is called nonrecurrent). See also parthenogenesis and apogamy below.
  • Recurrent apomixis (also called gametophytic apomixis): In this type, the embryo sac has the same number of chromosomes as the mother plant because meiosis was not completed. It generally arises either from an archesporial cell or from some other part of the nucellus.
  • Adventive embryony, also called sporophytic apomixis, sporophytic budding, or nucellar embryony: Here there may be an embryo sac (gametophyte) in the ovule, but the embryos do not arise from the cells of the gametophyte; they arise from cells of nucellus or the integument. Adventive embryony is important in several species of Citrus, in Garcinia, Euphorbia dulcis, Mangifera indica etc.
  • Vegetative apomixis: In this type "the flowers are replaced by bulbils or other vegetative propagules which frequently germinate while still on the plant". Vegetative apomixis is important in Allium, Fragaria, some grasses, etc.

The most complex of these types of apomixis in flowering plants is recurrent apomixis, now more often called gametophytic apomixis.[8] It is divided into diplospory (generative apospory) in which the embryo sac arises from a cell of the archesporium, and apospory (somatic apospory) in which the embryo sac arises from some other nucellus cell. Considerable confusion has resulted because diplospory is often defined to involve the megaspore mother cell only, but a number of plant families have a multicellular archesporium and the embryo sac could originate from one of the other cells.

Some terms related to apomixis

  • Parthenogenesis: Development of an embryo directly from an egg cell without fertilization is called parthenogenesis. It is of two types:
    • Haploid parthenogenesis: Parthenogenesis of a normal haploid egg (a meiotically reduced egg) into an embryo is termed haploid parthenogenesis. If the mother plant was diploid, then the haploid embryo that results is monoploid, and the plant that grows from the embryo is sterile. If they are not sterile, they are sometimes useful to plant breeders (especially in potato breeding, see dihaploidy). This type of apomixis has been recorded in Solanum nigram, Lilium spp., Orchis maculate, Nicotiana tabacum etc.
    • Diploid parthenogenesis: When the embryo sac develops without completing meiosis, so that the embryo sac and all cells within it are meiotically unreduced (aka diploid, but diploid is an ambiguous term), this is called diploid parthenogenesis, and the plant that develops from the embryo will have the same number of chromosomes as the mother plant. Diploid parthenogenesis is a component process of gametophytic apomixis (see above).
  • Androgenesis: This term is confusing because it is used for two different processes that both have the effect of producing a haploid organism (plant) that has "male inheritance". The first process is a natural one that has been noted as a rare phenomenon in many plants (e.g. Nicotiana and Crepis); embryos arise from male gametes. The process involves fusion of the male and female gametes and replacement of the female nucleus by the male nucleus. The second process that is referred to as androgenesis involves (artificial) culture of haploid plants from anther tissue or microspores.[9]
  • Apogamy: Although this term was (before 1908) used for other types of apomixis, and then discarded as too confusing, it is still sometimes used when an embryo develops from a cell of the megagametophyte other than the egg cell. In flowering plants the megagametophyte is the embryo sac, and the cells involved in apogamy would be synergids or antipodal cells.
  • Addition hybrids, called BIII hybrids by Rutishauser:[6] An embryo is formed after a meiotically unreduced egg cell is fertilized. The ploidy level of the embryo is therefore higher than that of the mother plant. This process occurs in some plants that are otherwise apomictic, and may play a significant role in producing tetraploid plants from triploid apomictic mother plants (if they receive pollen from diploids). Because fertilization is involved, this process does not fit the definition of apomixis.
  • Pseudogamy refers to any reproductive process that requires pollination but does not involve male inheritance. It is sometimes used in a restrictive sense to refer to types of apomixis in which the endosperm is fertilized but the embryo is not. A better term for the restrictive sense is centrogamy.[9]
  • Agamospecies, the concept introduced by Göte Turesson: "an apomict population the constituents of which, for morphological, cytological or other reasons, are to be considered as having a common origin," i.e., basically synonymous with "microspecies.[10]

Male apomixis in a conifer

A unique example of male apomixis as the regular reproductive method has recently been discovered in the Saharan Cypress, Cupressus dupreziana, where the seeds are derived entirely from the pollen with no genetic contribution from the female "parent".[11][12] Similar mechanisms occur infrequently in other plants and are known as androgenesis or androclinesis.

See also


  1. ^ Winkler, H. (1908). Über Parthenogenesis und Apogamie im Pflanzenreich. 2(3) Progressus Rei Botanicae 293–454.
  2. ^ Clausen, J. (1954). Partial apomixis as an equilibrium system. Caryologia, Supplement: 469–479.
  3. ^ a b Savidan, Y.H. (2000). Apomixis: genetics and breeding. 18 Plant Breeding Reviews 13–86.
  4. ^ Böcher TW. 1951. Cytological and embryological studies in the amphi-apomictic Arabis holboellii-complex. Det Danske Videnskabernes Selskab, Biologiske Skrifter 6(7): 1-59
  5. ^ a b Maheshwari, P. 1950. An introduction to the embryology of the angiosperms. McGraw-Hill, New York.
  6. ^ a b Rutishauser, A. 1969. Embryologie und Fortpflanzungsbiologie der Angiospermen: eine Einführung. Springer-Verlag, Wien.
  7. ^ Fitting, H., et al. 1930. Textbook of botany (Strasburger's textbook of botany, rewritten). Macmillan, London.
  8. ^ Nogler, G.A. 1984. Gametophytic apomixis. In Embryology of angiosperms. Edited by B.M. Johri. Springer, Berlin, Germany. pp. 475–518.
  9. ^ a b Solntzeva, M.P. (2003). About some terms of apomixis: pseudogamy and androgenesis. Biologia. 58(1): 1–7.
  10. ^ Defining species: a sourcebook from antiquity to today, by John S. Wilkins, ISBN 1433102161, 2009, pp. 122, 194
  11. ^ Pichot, C., et al. (2000). Lack of mother tree alleles in zymograms of Cupressus dupreziana A. Camus embryos Annals of Forest Science 57: 17–22.
  12. ^ Pichot, C., et al. (2001). Conservation: Surrogate mother for endangered Cupressus. Nature 412(6842):39–39.
  • Gvaladze G.E. (1976). Forms of Apomixis in the genus Allium L. In: S.S. Khokhlov (Ed.): Apomixis and Breeding, Amarind Pub., New Delhi-Bombay-Calcutta-New York pp. 160–165
  • Bhojwani S.S.& Bhatnagar S.P. (1988). The Embryology of angiosperms. Vikas Publishing house Pvt.Ltd. New Delhi.
  • Heslop-Harrison, J. (1972) "Sexuality in Angiosperms,"pp.133–289, In Steward,F.C. (ed.) Plant Physiology, Vol. 6C, Academic Press New York.
  • Nygren, A 1967, "Apomixis in the Angiosperms" pp. 551–596. In Ruhland, W. (ed.) Encyclopaedia of Plant Physiology, Vol.18, Springer-Verlag, Berlin.

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