Editing Apomixis

{{short description|Replacement of the normal sexual reproduction by asexual reproduction, without fertilization}}
{{about|plants|similar processes in animals and Oomycetes|Parthenogenesis}}
{{distinguish|automixis|autogamy}}
[[File:Poa bulbosa, vegetative apomixis.jpg|thumb|right|Vegetative apomixis in ''[[Poa bulbosa]]''; [[bulbil]]s form instead of flowers]]
In [[botany]], '''apomixis''' is [[asexual reproduction|asexual]] development of [[seed]] or embryo without [[Fertilisation|fertilization]]. However, other definitions include replacement of the seed by a [[plantlet]] or replacement of the flower by [[bulbils]].

Apomictically produced offspring are genetically identical to the parent plant, except in nonrecurrent apomixis.  Its etymology is Greek for "away from" + "mixing". 

Normal asexual reproduction of plants, such as propagation from [[Cutting (plant)|cuttings]] or leaves, has never been considered to be apomixis. In contrast to [[parthenocarpy]], which involves [[seedless fruit]] formation without fertilization, apomictic fruits have viable seeds containing a proper embryo, with asexual origin. 

In flowering plants, the term "apomixis" is used in a restricted sense to mean '''agamospermy''', i.e. [[cloning|clonal]] reproduction through seeds. Although agamospermy could theoretically occur in [[gymnosperm]]s, it appears to be absent in that group.<ref name="Bicknell" />

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

'''Male apomixis''' ('''paternal apomixis''') involves replacement of the genetic material of an egg by the genetic material of the pollen.

Some authors included all forms of asexual reproduction within apomixis, but that generalization of the term has since died out.<ref name="Bicknell">{{cite journal|last1=Bicknell|first1=Ross A.|last2=Koltunow|first2=Anna M.|author-link2=Anna Koltunow|year=2004|title=Understanding Apomixis: Recent Advances and Remaining Conundrums|journal=The Plant Cell|volume=16|issue=suppl 1|pages=S228–S245|doi=10.1105/tpc.017921|pmc=2643386|pmid=15131250}}</ref>

==Evolution==
Because apomictic plants are genetically identical from one generation to the next, each lineage has some of the characters of a true [[species]], maintaining distinctions from other apomictic lineages within the same [[genus]], 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 [[species aggregate]]s, typically listed in [[Flora (publication)|flora]]s with the convention "''Genus species'' agg." (such as the [[bramble]], ''Rubus fruticosus'' agg.). In some [[Family (biology)|plant families]], genera with apomixis are quite common, for example in [[Asteraceae]], [[Poaceae]], and [[Rosaceae]]. Examples of apomixis can be found in the genera ''[[Crataegus]]'' (hawthorns), ''[[Amelanchier]]'' (shadbush), ''[[Sorbus]]'' ([[rowan]]s and [[whitebeam]]s), ''[[Rubus]]'' (brambles or blackberries), ''[[Poa]]'' (meadow grasses),  ''[[Nardus stricta]]'' (matgrass), ''[[Hieracium]]'' (hawkweeds) and ''[[Taraxacum]]'' (dandelions).  Apomixis is reported to occur in about 10% of globally extant [[fern]]s.<ref name=Liu>{{cite journal | last1=Liu | first1=Hong-Mei | last2=Dyer | first2=Robert J. | last3=Guo | first3=Zhi-You | last4=Meng | first4=Zhen | last5=Li | first5=Jian-Hui | last6=Schneider | first6=Harald | title=The Evolutionary Dynamics of Apomixis in Ferns: A Case Study from Polystichoid Ferns | journal=Journal of Botany | volume=2012 | date=2012-11-05 | issn=2090-0120 | doi=10.1155/2012/510478 | pages=1–11 | doi-access=free }}</ref>  Among [[Polystichum|polystichoid]] ferns, apomixis evolved several times independently in three different [[clade]]s.<ref name=Liu />

Although the [[evolution]]ary advantages of [[sexual reproduction]] are lost, apomixis can pass along traits fortuitous for evolutionary fitness. As [[Jens Clausen]] put it:<ref>{{cite journal|last= Clausen| first= J.|year=1954|title=Partial apomixis as an equilibrium system|journal=Caryologia|volume=1954, Supplement|pages=469–479}}</ref>{{rp|470}}<blockquote>The apomicts actually have discovered the effectiveness of mass production long before Mr.&nbsp;[[Henry Ford]] applied it to the production of the automobile. ... Facultative apomixis ... does not prevent variation; rather, it multiplies certain varietal products.</blockquote>

'''Facultative apomixis''' means that apomixis does not always occur, i.e., sexual reproduction can also happen. It appears likely that all apomixis in plants is facultative;<ref name=Savidan>{{cite book|author=Savidan, Y.H.|year=2000|title=Plant Breeding Reviews|chapter=Apomixis: genetics and breeding|volume=18|pages=13–86|doi=10.1002/9780470650158.ch2|isbn=9780470650158}}</ref><ref name=Hojsgaard2022>{{Cite Q|Q115563996|doi-access=free}}</ref> in other words, that "obligate apomixis" is an artifact of insufficient observation (missing uncommon sexual reproduction).

==Apogamy and apospory in non-flowering plants==
The gametophytes of [[bryophyte]]s, and less commonly [[fern]]s and [[Lycopodiophyta|lycopods]] can develop a group of cells that grow to look like a sporophyte of the species but with the [[ploidy]] level of the gametophyte, a phenomenon known as apogamy. The sporophytes of plants of these groups may also have the ability to form a plant that looks like a gametophyte but with the ploidy level of the sporophyte, a phenomenon known as apospory.<ref>{{cite journal |author=Steil, W.N. |year=1939 |title=Apogamy, apospory, and parthenogenesis in the Pteridophytes |journal=The Botanical Review |volume=5 |issue=8 |pages=433–453 |doi=10.1007/bf02878704|bibcode=1939BotRv...5..433S |s2cid=19209851 }}</ref><ref>{{cite book |author=Niklas, K.J. |year=1997 |title=The evolutionary biology of plants |publisher=The University of Chicago press |location=Chicago |url=https://books.google.com/books?id=2aSrw70rOKgC|isbn=9780226580838 }}</ref>

See also androgenesis and androclinesis described below, a type of male apomixis that occurs in a conifer, ''[[Cupressus dupreziana]]''.

== In flowering plants (angiosperms) ==

Agamospermy, asexual reproduction through seeds, occurs in flowering plants through many different mechanisms<ref name=Savidan/> and a simple [[hierarchy|hierarchical]] classification of the different types is not possible. Consequently, there are almost as many different usages of terminology for apomixis in [[angiosperm]]s as there are authors on the subject. For English speakers, Maheshwari 1950<ref name=Maheshwari>Maheshwari, P. 1950. An introduction to the embryology of the angiosperms. McGraw-Hill, New York.</ref> is very influential. German speakers might prefer to consult Rutishauser 1967.<ref name=Rutishauser>Rutishauser, A. 1969. Embryologie und Fortpflanzungsbiologie der Angiospermen: eine Einführung. Springer-Verlag, Wien.</ref> Some older text books<ref>Fitting, H., et al. 1930. Textbook of botany (Strasburger's textbook of botany, rewritten). Macmillan, London.</ref> 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 the term [[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 in flowering plants ===
[[File:Agave angustifolia (Caribbean Agave) in Hyderabad W IMG 8660.jpg|thumb|right|[[Caribbean agave]] producing plantlets on the old flower stem.]]
Maheshwari<ref name=Maheshwari/> 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 [[megagametophyte]] 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''', is now more often called '''gametophytic apomixis''': In this type, the megagametophyte has the same number of chromosomes as the mother plant because meiosis was not completed. It generally arises either from an [[archesporium|archesporia]]l cell or from some other part of the [[nucellus]].
*'''Adventive embryony''', also called '''sporophytic apomixis''', '''sporophytic budding''', or [[nucellar embryony]]: Here there may be a megagametophyte 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]]'', ''[[Agave]]'', and some grasses, among others.

====Types of gametophytic apomixis====
Gametophytic apomixis in flowering plants develops in several different ways.<ref name=Nogler>Nogler, G.A. 1984. Gametophytic apomixis. In Embryology of angiosperms. Edited by B.M. Johri. Springer, Berlin, Germany. pp. 475–518.</ref> A megagametophyte develops with an egg cell within it that develops into an embryo through [[parthenogenesis]]. The central cell of the megagametophyte may require fertilization to form the [[endosperm]], '''pseudogamous gametophytic apomixis''', or in '''autonomous gametophytic apomixis''' endosperm fertilization is not required. 
*In '''diplospory''' (also called '''generative apospory'''), the megagametophyte arises from a cell of the [[archesporium]].
* In '''apospory''' (also called '''somatic apospory'''), the megagametophyte arises from some other (somatic) cell of the nucellus.

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 megagametophyte could originate from another archesporium cell.

Diplospory is further subdivided according to how the megagametophyte forms:
* ''[[Allium]] odorum''–''A. nutans'' type. The chromosomes double (endomitosis) and then meiosis proceeds in an unusual way, with the chromosome copies pairing up (rather than the original maternal and paternal copies pairing up).
* ''[[Taraxacum]]'' type: Meiosis I fails to complete, meiosis II creates two cells, one of which degenerates; three mitotic divisions form the megagametophyte.
* ''[[Ixeris]]'' type: Meiosis I fails to complete; three rounds of nuclear division occur without cell-wall formation; wall formation then occurs.
* ''[[Blumea]]''–''[[Elymus (plant)|Elymus]]'' types: A mitotic division is followed by degeneration of one cell; three mitotic divisions form the megagametophyte.
* ''[[Antennaria]]''–''[[Hieracium]]'' types: three mitotic divisions form the megagametophyte.
* ''[[Eragrostis]]''–''[[Panicum]]'' types: Two mitotic division give a 4-nucleate megagametophyte, with cell walls to form either three or four cells.

===Incidence in flowering plants===
Apomixis occurs in at least 33 families of flowering plants, and has evolved multiple times from sexual relatives.<ref>{{cite journal|author=Carman, J.G.|year=1997|title=Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony|journal=Biological Journal of the Linnean Society|volume=61|issue=1|pages=51–94|doi=10.1111/j.1095-8312.1997.tb01778.x|doi-access=free}}</ref><ref name=Nygren>{{cite book|author=Nygren, A. |year=1967 |title= Handbuch der Pflanzenphysiologie |chapter= Apomixis in the angiosperms |publisher=Springer-Verlag |location=Berlin|editor= W. Ruhland |pages= 551–596|volume=18}}</ref> Apomictic species or individual plants often have a hybrid origin, and are usually polyploid.<ref name=Nygren/>

In plants with both apomictic and meiotic embryology, the proportion of the different types can differ at different times of year,<ref name=Nogler/> and [[Photoperiodism|photoperiod]] can also change the proportion.<ref name=Nogler/> It appears unlikely that there are any truly completely apomictic plants, as low rates of sexual reproduction have been found in several species that were previously thought to be entirely apomictic.<ref name=Nogler/>

The genetic control of apomixis can involve a single genetic change that affects all the major developmental components, formation of the megagametophyte, parthenogenesis of the egg cell, and endosperm development.<ref name=Koltunow>{{cite journal|author1=Koltunow, A.M. |author2=Johnson, S.D. |author3=Bicknell, R.A. |year=2000|title=Apomixis is not developmentally conserved in related, genetically characterized ''Hieracium'' plants of varying ploidy|journal=Sexual Plant Reproduction|volume=12|issue=5|pages=253–266|doi=10.1007/s004970050193|s2cid=23186733 }}</ref> However, the timing of the various developmental processes is critical to successful development of an apomictic seed, and the timing can be affected by multiple genetic factors.<ref name=Koltunow/>

== Related terms ==
* '''Apomeiosis''': "Without meiosis"; usually meaning the production of a meiotically unreduced gametophyte.
* '''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 [[ploidy#Dihaploidy and polyhaploidy|dihaploidy]]). This type of apomixis has been recorded in ''[[Solanum nigrum]]'', ''[[Lilium]]'' spp., ''[[Orchis maculata]]'', ''[[Nicotiana tabacum]]'', etc.
**'''Diploid parthenogenesis''': When the megagametophyte develops without completing meiosis, so that the megagametophyte and all cells within it are meiotically unreduced (a.k.a. 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).
*{{anchor|Androgenesis}} '''Androgenesis''' and '''androclinesis''' are synonyms. These terms are used for two different processes that both have the effect of producing an embryo that has "male inheritance".
:The first process is a natural one. It may also be referred to as '''male apomixis''' or '''paternal apomixis'''. It involves fusion of the male and female gametes and replacement of the female nucleus by the male nucleus. This has been noted as a rare phenomenon in many plants (e.g. ''[[Nicotiana]]'' and ''[[Crepis]]''), and occurs as the regular reproductive method in the Saharan Cypress, ''[[Cupressus dupreziana]]''.<ref>{{cite journal |author1=Christian Pichot |author2=Benjamin Liens |author3=Juana L. Rivera Nava |author4=Julien B. Bachelier |author5=Mohamed El Maâtaoui |date=January 2008 |title=Cypress Surrogate Mother Produces Haploid Progeny From Alien Pollen |journal=Genetics|volume=178 |issue=1 |pages=379–383 |doi=10.1534/genetics.107.080572 |pmid=18202380 |pmc=2206086}}</ref><ref>{{cite journal|author1=Christian Pichot|author2=Bruno Fady|author3=Isabelle Hochu|year=2000|title=Lack of mother tree alleles in zymograms of ''Cupressus dupreziana'' A. Camus embryos|journal=Annals of Forest Science|volume=57|issue=1 |pages=17–22|doi=10.1051/forest:2000108|bibcode=2000AnFSc..57...17P |doi-access=free}}</ref><ref>{{cite journal|author1=Pichot, C. |author2=El Maataoui, M. |author3=Raddi, S. |author4=Raddi, P. |year=2001|title=Conservation: Surrogate mother for endangered ''Cupressus''|journal=Nature|volume=412|issue=6842|pages=39|doi=10.1038/35083687|pmid=11452293 |s2cid=39046191 |doi-access=free}}</ref> Recently, the first example of natural androgenesis in a vertebrate, a fish, [[Squalius alburnoides]] was discovered.<ref>{{cite journal |last1=Morgado-Santos |first1=Miguel |last2=Carona |first2=Sara |last3=Vicente |first3=Luís |last4=Collares-Pereira |first4=Maria João |title=First empirical evidence of naturally occurring androgenesis in vertebrates |journal=Royal Society Open Science |year=2017 |volume=4 |issue=5 |pages=170200 |doi=10.1098/rsos.170200 |pmid=28573029 |pmc=5451830 |bibcode=2017RSOS....470200M |doi-access=free }}</ref> It is also known in invertebrates, particularly clams in the genus ''[[Corbicula]]'', and these asexually reproducing males are noted to have a wider range than their noninvasive non-hermaphroditic cousins, more similar to hermaphroditic invasive species in the genus, indicating that this does sometimes have evolutionary benefits.<ref>{{cite journal |last1=Pigneur |first1=L.-M. |last2=Hedtke |first2=S. M. |last3=Etoundi |first3=E. |last4=Van Doninck |first4=K. |title=Androgenesis: a review through the study of the selfish shellfish Corbicula spp |journal=Heredity |date=June 2012 |volume=108 |issue=6 |pages=581–591 |doi=10.1038/hdy.2012.3 |pmid=22473310 |pmc=3356815 |issn=1365-2540|doi-access=free }}</ref>
:The second process that is referred to as androgenesis or androclinesis involves (artificial) culture of haploid plants from [[anther]] tissue or [[microspores]].<ref name=Solnzeva>{{cite journal | last1 = Solntzeva | first1 = M.P. | year = 2003 | title = About some terms of apomixis: pseudogamy and androgenesis | journal = Biologia | volume = 58 | issue = 1| pages = 1–7 }}</ref> Androgenesis has also been artificially induced in fish.<ref>{{cite journal |last1=Grunina |first1=A. S. |last2=Recoubratsky |first2=A. V. |title=Induced Androgenesis in Fish: Obtaining Viable Nucleocytoplasmic Hybrids |journal=Russian Journal of Developmental Biology |date=1 July 2005 |volume=36 |issue=4 |pages=208–217 |doi=10.1007/s11174-005-0035-5 |pmid=16208936 |s2cid=11750658 |url=https://link.springer.com/article/10.1007/s11174-005-0035-5 |language=en |issn=1608-3326|url-access=subscription }}</ref>
*'''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 cells involved in apogamy would be synergids or antipodal cells.
*'''Addition hybrids''', called '''B<sub>III</sub> hybrids''' by Rutishauser:<ref name=Rutishauser/> 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'''.<ref name=Solnzeva/>
*'''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.<ref>Defining species: a sourcebook from antiquity to today, by John S. Wilkins, {{ISBN|1433102161}}, 2009, [https://books.google.com/books?id=pazpr2vJxQAC&dq=agamospecies&pg=PA194 pp. 122, 194]</ref>

== See also ==
* {{annotated link|Cytomixis}}, a process of nuclear fusion that occurs during pollen meiosis
* {{annotated link|Klepton}}, a phenomenon known in zoology where mating with another taxon is required to complete reproduction
* {{annotated link|Meiosis}}
* {{annotated link|Parthenocarpy}}, the production of seedless fruits
* {{annotated link|Parthenogenesis}}, the animal equivalent of apomixis
* {{annotated link|Plant reproductive morphology}}

== References ==
{{reflist}}

== Further reading ==
* 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.&nbsp;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.&nbsp;133–289, In Steward,F.C. (ed.) Plant Physiology, Vol. 6C, Academic Press New York.

== External links ==
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[[Category:Plant reproduction]]
[[Category:Asexual reproduction]]