Critical Reviews in Plant Sciences Taxonomy and Biogeography of Apomixis in Angiosperms and

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Taxonomy and Biogeography of Apomixis
in Angiosperms and Associated Biodiversity
Characteristics
Diego Hojsgaarda, Simone Klatta, Roland Baierb, John G. Carmanc & Elvira Hörandla
a Georg August University Göttingen, Albrecht-von-Haller Institute for Plant Sciences,
Department of Systematic Botany, Göttingen, Germany
b Gesellschaft für wissenschaftliche Datenverarbeitung mbH Göttingen (GWDG),
Arbeitsgruppe Anwendungs- und Informationssysteme, Göttingen, Germany
c Plants, Soils and Climate Department, Utah State University, Logan, UT, USA
Published online: 29 May 2014.
To cite this article: Diego Hojsgaard, Simone Klatt, Roland Baier, John G. Carman & Elvira Hörandl (2014) Taxonomy and
Biogeography of Apomixis in Angiosperms and Associated Biodiversity Characteristics, Critical Reviews in Plant Sciences, 33:5,
414-427, DOI: 10.1080/07352689.2014.898488
To link to this article: http://dx.doi.org/10.1080/07352689.2014.898488
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CriticalReviewsinPlantSciences,33:414–427,2014
PublishedwithlicensebyTaylor&Francis
ISSN:0735-2689print/1549-7836online
DOI:10.1080/07352689.2014.898488
Taxonomy and Biogeography of Apomixis in Angiosperms
and Associated Biodiversity Characteristics
DiegoHojsgaard,1 SimoneKlatt,1 RolandBaier,2JohnG.Carman,3
andElviraHo¨randl1
1GeorgAugustUniversityGo¨ttingen,Albrecht-von-HallerInstituteforPlantSciences,Department
ofSystematicBotany,Go¨ttingen,Germany
2Gesellschaftfu¨rwissenschaftlicheDatenverarbeitungmbHGo¨ttingen(GWDG),Arbeitsgruppe
Anwendungs-undInformationssysteme,Go¨ttingen,Germany
3Plants,SoilsandClimateDepartment,UtahStateUniversity,Logan,UT,USA
4
1
0
2
e
n
Ju TableofContents
3
0
4
1
0: I. INTRODUCTION .................................................................................................................................................................................................415
0
at
] II. ASSESSMENTOFOCCURRENCES.........................................................................................................................................................417
n
ge A. DataCollectionandDatabaseConstruction ..........................................................................................................................................417
n
etti B. DataAnalyses ...................................................................................................................................................................................................417
o
G
et III. PHYLOGENETICDISTRIBUTIONS ........................................................................................................................................................419
rsita AB.. NAopvoemliRxiescionrdGse.n..e..r..a..,..F...a..m....i..l.i.e..s....a..n..d....O....r.d...e..r.s..............................................................................................................................................................................................................................................................................................442109
e
niv C. FamilyDiversityandApomixis .................................................................................................................................................................421
U D. BiogeographyandApomixis .......................................................................................................................................................................421
-
st
u
ug IV. APOMIXISANDEVOLUTION ....................................................................................................................................................................422
A
- A. PatternsatHigherTaxonomicLevels.......................................................................................................................................................422
g
or B. Apomixis-sexSystems ..................................................................................................................................................................................422
e
G C. ApomixisBiodiversityParallelsGeneralBiodiversity ......................................................................................................................424
[
y D. TheExpandedTransitionTheory ..............................................................................................................................................................424
b
d
e
ad V. PERSPECTIVESFORFUTURERESEARCH......................................................................................................................................425
o
nl
ow ACKNOWLEDGMENTS ...............................................................................................................................................................................................425
D
FUNDING ..............................................................................................................................................................................................................................425
REFERENCES ....................................................................................................................................................................................................................425
©DiegoHojsgaard,SimoneKlatt,RolandBaier,JohnG.Carman,andElviraHo¨randl
AddresscorrespondencetoElviraHo¨randl,GeorgAugustUniversityGo¨ttingen,Albrecht-von-HallerInstituteforPlantSciences,Department
ofSystematicBotany,UntereKarspu¨le2,D37073Go¨ttingen,Germany.E-mail:[email protected]
Colorversionsofoneormoreofthefiguresinthearticlecanbefoundonlineatwww.tandfonline.com/bpts.
414
APOMIXIS,TAXONOMICDIVERSITY,ANDBIOGEOGRAPHY 415
sis or mitotic-like division, resulting in an unreduced func-
Apomixis in angiosperms is asexual reproduction from seed. tionalspore(diplospory).Ingametophyticapomicts,endosperm
Its importance to angiospermous evolution and biodiversity has formation may require fertilization of polar nuclei (pseudoga-
been difficult to assess mainly because of insufficient taxonomic mousapomixis)oritmaydevelopindependently(autonomous
documentation.Thus,weassembledliteraturereportingapomixis
apomixis).Adventitiousembryosofsporophyticapomictsform
occurrencesamongangiospermsandtransferredtheinformation
from nucellar or integumentary cells, and their formation usu-
to an internet database (http://www.apomixis.uni-goettingen.de).
Wethensearchedforcorrelationsbetweenapomixisoccurrences ally occurs in parallel with the formation of sexual embryos.
andwell-establishedmeasuresoftaxonomicdiversityandbiogeog- Bothsexualandadventitiousembryonyrequireendosperm,the
raphy.Apomixiswasfoundtobetaxonomicallywidespreadwith formation of which usually involves fertilization of the polar
no clear tendency to specific groups and to occur with sexuality
nuclei.Speciesexhibitingadventitiousembryonyoftenproduce
atalltaxonomiclevels.Adventitiousembryonywasthemostfre-
multiple embryos per seed. Hence, it is considered a form of
quentform(148genera)followedbyapospory(110)anddiplospory
(68).Allthreeformsarephylogeneticallyscattered,butthisscat- polyembryony,anditiswidespreadamongtropicalplants(Nau-
teringisstronglyassociatedwithmeasuresofbiodiversity.Across mova,1992).Polyembryony,however,canalsoarisefromsex-
apomictic-containing orders and families, numbers of apomict- ualpathways,e.g.fromrarecasesoffunctionaltwinmegasporo-
containing genera were positively correlated with total numbers
4 of genera. In general, apomict-containing orders, families, and cytes(MMC)orbyfertilizationofasynergidthathasassumed
01 subfamiliesofAsteraceae,Poaceae,andOrchidaceaewerelarger, egg-likeproperties.
2
e i.e., they possessed more families or genera, than non-apomict- Gametophyticapomicts,exceptinafewcases,arepolyploid,
n
u containing orders, families or subfamilies. Furthermore, many andtheyareoftenrelatedtospeciesthatexhibitotherdevelop-
J
3 apomict-containinggenerawerefoundtobehighlycosmopolitan. mental abnormalities such as polyspory (Carman, 1997). Ga-
4 0 Inthisrespect,62%occupymultiplegeographiczones.Numbers metophytic and sporophytic apomixis are heritable, but they
1 of genera containing sporophytic or gametophytic apomicts de-
0: creasedfromthetropicstothearctic,atrendthatparallelsgeneral aregenerallyexpressedfacultatively,inindividualplants,along
0
at biodiversity.Whileangiospermsappeartobepredisposedtoshift with sex (Ozias-Akins and van Dijk, 2007). Confusion aris-
] fromsextoapomixis,thereisalsoevidenceofreversionstosexu- ingfromfacultativenessandtheexistenceofmultipleapomixis
n
ge ality.Suchreversionsmayresultfromgeneticorepigeneticdesta- pathways has hampered the gathering of reliable quantitative
n bilizationeventsaccompanyinghybridization,polyploidy,orother
etti cytogeneticalterations.Becauseofincreasedwithin-plantgenetic data for relating apomixis to various evolutionary and biogeo-
o graphicalphenomena.
G andgenomicheterogeneity,rangeexpansionsanddiversifications
et atthespeciesandgenuslevelsmayoccurmorerapidlyuponre- Apomixis and sexuality are not exclusive traits, as almost
rsita vaeprosmioincttsoasmexounaglhitiyg.hTlyhedisviegrnsieficaanndtlgye-oegnrraicphheidcarlleyp-reexsteenntsaivtieotnasxoaf, aplllanaptso,mthiceticsepxluaanltsperxohciebsistfiancuolvtautlievsegseexnuearaliltlyy.Ianboaprtosspdourroinugs
e
v fromgeneratoorders,supportthisconclusion.
ni meiosis or early embryo sac formation, and it is replaced by
U
aposporous embryo sac formation, which occurs more or less
-
ust Keywords angiosperms,biodiversity,biogeography,onlinedatabase, simultaneously. In some ovules, a reduced embryo sac forms,
g evolution,polyploidy,phylogeny,geographicalpartheno-
u andthesemayproducerecombinant1nembryosbyhaploidor
A genesis
- polyhaploid parthenogenesis or recombinant 2n embryos fol-
g
r
o lowing fertilization. In other ovules, a reduced embryo sac
e
G and one or more aposporous embryo sacs may form in par-
[
y I. INTRODUCTION allel,buttheapomicticpathwayisoftenmoresuccessful(e.g.,
b
d Apomixis in angiosperms is reproduction via asexually Hojsgaard et al., 2013). Nevertheless, polyembryony is com-
e
d
a formed seed (Asker and Jerling, 1992). By excluding vege- moninaposporousplants,andoccasionallyanindividualovule
o
nl tative propagation per definition, apomixis is development of will contain sexually and aposporously-produced embryos. In
w
o an embryo from an unreduced and unfertilized egg cell (ga- the case of diplospory, facultative sexuality occurs at lower or
D
metophytic apomixis) or from a somatic cell of the ovule higherfrequenciesduetocompletionofanormalsexualmeiosis
(sporophytic apomixis). Apomixis thus combines the benefits and embryo sac formation followed either by parthenogenesis
of seed dispersal with those of asexual reproduction (Mogie, andtheformationofarecombinant1nhaploid(orpolyhaploid)
1992).Thecellularmechanismsofapomixishavebeenstudied embryo or by fertilization and the formation of a recombinant
for over 100 years and have recently been reviewed (Ozias- 2nembryo(Aliyuetal.,2010).
Akins,2006;TuckerandKoltunow,2009;Rodriguez-Lealand In natural populations of apomicts, genetic studies using
Vielle-Calzada,2012).Inbrief,gametophyticapomixisinvolves charactercompatibilityanalysishaveconfirmedtheregularap-
development of an unreduced embryo sac (apomeiosis) and pearanceofrecombinantgenotypesandploidyvariants(Bashaw
formation of an embryo from the unreduced egg, within the etal.,1992;VanderHulstetal.,2000;Paunetal.,2006;Aliyu
embryo sac, without fertilization (parthenogenesis). The unre- et al., 2010; Paule et al., 2011; Cosendai et al., 2013). Such
duced embryo sac can develop from a somatic cell of the nu- variations suggest that the reproductive elements of sex and
cellus,whichreplacesthemegaspore(apospory).Alternatively, apomixis,i.e.,meiosis,syngamy,apomeiosisandparthenogene-
the megaspore mother cell may undergo a restitutional meio- sis,involvedifferentgeneticandepigeneticcontrolmechanisms
416 D.HOJSGAARDETAL.
that can be uncoupled. This phenomenon is well documented Facultative apomixis in perennials provides long-term re-
experimentally(Ogawaetal.,2013).Thus,apomeiosisfollowed productive stability for the colonization of large areas. Such
bysyngamyleadstoanincreaseinploidy(2n+n;B offspring), long-term stability may also provide time for multiple genetic
III
whilemeiosisfollowedbyparthenogenesisleadstoareduction andgenomicvariantstoformandbetested,e.g.,progenywith
inploidy(1n+0;haploidorpolyhaploidoffspring).Suchcases unique genetic recombinations and/or genomic translocations,
of partial apomixis and partial sex occur regularly in progeny inversions, aneuploidy, etc. Some of these could be sexual re-
testpopulations(BicknellandKoltunow,2004)andnaturalpop- vertants with normal Polygonum-type embryo sac formation
ulations(CosendaiandHo¨randl,2010;Pauleetal.,2011).The or with developmentally-unusual embryo sac formation, e.g.,
pointofinteresthereisthatsexualprocessesandvariouscom- polyspory.Afterreversiontoobligatesexuality,suchgenetically
binationsofsexualandapomicticprocessesoccurinfrequently enriched and recombined lineages may diversify more rapidly
toregularlyinmostapomicticspecies. thantheirobligately-sexualancestors(Carman,1997;Ho¨randl
ApomixiswasfirstdescribedinAntennariabyJuelin1898 and Hojsgaard, 2012). Hence, the breadth of distribution and
(Nogler, 2006). By 1941, apomixis had been reported in 44 richnessofgeneraandspeciesinfamiliescontainingapomicts
generafrom23families(Stebbins,1941).Gustafsson’sseminal couldreasonablyincreaseasadirectconsequenceofapomixis.
4 treatmentofapomixisinangiosperms(Gustafsson,1946;1947a; For this review, we have updated the apomixis occurrence lit-
1
0 b)listed73agamospermousgenerafrom25families(excluding eratureandhaverelatedittobiodiversityatvarioustaxonomic
2
e viviparousspecies),anditprovidedcomprehensivedescriptions levels.Suchrelationshipshavenotpreviouslybeenextensively
n
u of developmental pathways, evolutionary origins and ecologi- characterized.
J
03 calpreferences.AskerandJerling(1992)recognized108gen- Adeeperinterestinbiogeographicalandecologicalaspects
4 era in which apomixis occurs in at least one species (referred of apomixis emerged in the last decades of the twentieth cen-
1
0: tohereinasapomict-containinggenera),andtheylistedanad- tury. Consequently, it was found that some apomicts have
0
at ditional 26 questionable records. Naumova (1992) recognized larger distributions in higher latitudes than their sexual rela-
n] 116 genera with sporophytic apomixis, and Carman (1997) tivesandhaveabundantlypopulatedpreviouslyglaciatedareas
e
g listed 222 genera that contain sporophytic or gametophytic (Bierzychudek, 1985; Kearney, 2005; Ho¨randl, 2006; Ho¨randl
n
etti apomicts. etal.,2008).Theterm“geographicalparthenogenesis”isused
o
G The phylogenetic distributions of apomicts and their evo- todescribethisphenomenon,butithasbeenstudiedextensively
et lutionary and biogeographical relevance remain unclear. The inonlyafewgenera(Ho¨randletal.,2008).Formostapomic-
a
sit doomed view of Darlington (Darlington, 1939), Stebbins tictaxa,informationondistributionpatternshasnotpreviously
r
e (Stebbins, 1950) and Grant (Grant, 1981), that apomixis is an been assembled or remains too scarce to allow for generaliza-
v
ni evolutionary dead end, was based on the assumption that loss tions.Intropicalapomicts,biogeographicalpatternsofapomic-
U
- ofgenotypeheterogeneityinpopulationswouldresultinlossof ticplantsarelargelyunexplored,andrecordsofpolyembryony
st
u potential to adapt to environmental change. Thus, agamic lin- withoutdetailedinformationonapomicticbiotypeshaveblurred
g
u
A eageswerethoughttobedoomedforextinction.Thisview,ofa the patterns (Carman, 1997). Superior colonizing ability and
g- static,closedsystem,hasbeenrevisedbymorerecenttheoret- polyploidy can make apomicts formidable invaders (Richards,
r
o
e ical papers (Carman, 1997; Whitton et al., 2008; Ho¨randl and 2003),ashasoccurredonallcontinents(Chapmanetal.,2003;
G
[ Hojsgaard, 2012), which are based on empirical observations Brock, 2004; Rambuda and Johnson, 2004; Hao et al., 2011).
y
b that agamic complexes harbor considerable genetic variability Butgeneralizingtheseobservationstothemajorityofapomicts
d
e (Grant,1981;Ho¨randlandPaun,2007)andrepresentdynamic is premature. The necessary biogeographical surveys simply
d
oa andflexiblesystems. havenotbeenconducted.
nl Three large families, Poaceae, Asteraceae, and Rosaceae, Hereinweprovideacomprehensivesurveyoftheliterature
w
o contain a majority of the known apomict-containing genera, that describes the occurrence and biogeography of apomict-
D
and this has led to speculations that a developmental predis- containing genera, and we discuss hypotheses relating phylo-
position may exist in these families or that apomixis is more geniesandbiogeographicalpatternstobiodiversityatmultiple
likelytoemergeinlargefamilies(Richards,1997;Ozias-Akins taxonomiclevels.Specifically,wetestedwhetherangiosperms
and van Dijk, 2007). It has also been postulated that a rapid in general are predisposed to apomixis or whether a predispo-
spread of apomixis in major clades could account for the ob- sitionstatisticallyfavorscertainfamilies.Further,weexamined
servedpattern(vanDijkandVijverberg,2005).Recentphyloge- frequencies of the three major forms of apomixis (apospory,
neticreconstructionsofthemajorclades(orders)ofangiosperms diplospory,adventitiousembryony)andrelatedthesetoputative
(Ho¨randl and Hojsgaard, 2012) support the view of a broadly taxonomicandbiogeographicalpreferences.Wealsotestedfor
scattered distribution of apomixis over the entire phylogeny positive correlations between apomixis frequencies and biodi-
of angiosperms coupled with rapid spread in large families. versityacrossapomictandnon-apomict-containingsisterclades
However, correlation analyses have not previously been con- among orders and families. Such correlations are expected if
ductedbetweenapomixisoccurrencesandgeneralmeasuresof highly-successful apomixis-to-sex reversals occur. Finally, we
biodiversity. report frequencies of apomict-containing genera that occupy
APOMIXIS,TAXONOMICDIVERSITY,ANDBIOGEOGRAPHY 417
multiple geographic zones and discuss hypotheses for inter-
preting the observed patterns. The database constructed for
this review is publically available (http://www.apomixis.uni-
goettingen.de)andincludeslistsofapomict-containinggenera,
typesofapomixisfound,andoriginalreferences.
II. ASSESSMENTOFOCCURRENCES
A. DataCollectionandDatabaseConstruction
We updated the occurrence of apomixis in angiosperms as
representedinCarman(1997)bysearchingtheWebofKnowl-
edge (Thomson Reuters (http://www.webofknowledge.com/),
ScientificCommons(St.Gallen,InstituteforMediaandCom-
munications Management, http://en.scientificcommons.org/),
4 Redalyc (Universidad Auto´noma del Estado de Me´xico,
01 http://www.redalyc.org/home.oa, version 2.0© 2012), Ingenta
2
e Connect(http://www.ingentaconnect.com/),andTheReference
n
u in Scientific Document Supply (French National Center for
J
3 ScientificResearch,CNRS,http://www.refdoc.fr/).Articlesnot
0
4 inthepublicdomainwereaccessedthroughtheLibraryofthe
1
0: University of Goettingen, the Library of the University of Vi-
0
at enna, or the Merrill Library, Utah State University. Literature
n] was searched through December, 2012. Records were main-
e
g tained at the genus level. For records originating before 1997,
n
etti onlythefirstdocumentationofapomixispergenusisreported,
o andonlyrecordswithsufficientreliabilitywereaccepted.Cri-
G
et teriaforacceptanceincludedverificationbymicroscopicinves-
a
sit tigationsofembryosacand/orembryodevelopment,flowcyto-
er metricseedscreening(Matzketal.,2000),molecularprogeny FIG.1. Apomixisamongordersofangiosperms.Ovalsindicatesisterclades
v
ni tests, or well documented isolation and emasculation experi- containingandnotcontainingapomixis;filledovalsindicatepolytomies.(A)
U apospory.(D)diplospory.(E)adventitiousembryony.ExpandedfromHo¨randl
- ments.Preliminaryrecordsbasedonindirectobservation(e.g.,
st andHojsgaard(2012).
u clonality in wild populations, lack of pollen tubes on stig-
g
u mas,etc.)wereincludedasuncertain,butthesewereexcluded
A
g- fromstatisticalinvestigations.Recordsofpolyembryonywith- B. DataAnalyses
r
eo outproofofadventitiousembryonyarereportedseparately.We Frequencies of apomict-containing families and genera
G
[ didnotincludereportsofoccasionalhaploidparthenogenesisin were compared across orders. In modern systematics, these
by sexualplants.RecordsforAsteraceaerejectedbyNoyes(2007) taxonomic units represent almost exclusively clades, i.e.,
ed were included in the uncertain category to encourage detailed they are phylogenetic groups reflecting common diversifi-
d
oa re-investigation.Weconsiderallangiospermousapomictstobe cation processes and representing hierarchically-nested enti-
nl facultative,withthepossibleexceptionofAlchemilla(Askerand ties. We refrained from species-level taxonomy because of
w
o Jerling, 1992), which means both sexually and apomictically- (i) scarcity of information concerning apomixis at the species
D
produced seeds can form on the same plant. Since apomixis level, and (ii) difficulties in defining species in agamic com-
as a reproductive character state is not exclusive, we refrained plexes where reticulate evolution and other speciation pro-
from standard phylogenetic tests of diversification, e.g., John- cesses are occurring (Grant, 1981; Ho¨randl, 1998). To pro-
sonetal.(2011).Allrecordsweretransferredtothetaxonomic vide an overview, we mapped records onto the phylogenetic
system of families and orders as in APG III (Bremer et al., treeoftheAPGIIIclassificationasinHo¨randlandHojsgaard
2009), and records published since 1997 were plotted by year (2012),andweaddedinformationconcerningtypesofapomixis
ofpublication. (Figure1).Moredetailedphylogeneticanalysesondiversifica-
ThereferencesreportedinCarman(1997)werere-examined tion rates (as in Johnson et al., 2011) are difficult to conduct
andtracedbacktotheoriginalliterature,andonlyoriginaldocu- because of facultativeness, which exists at the population and
mentsareincludedinourdatabase.Typesofapomixisexpressed individual levels. Sex and facultative apomixis simply are not
arealsoreported.RecordswereimportedintoOracle(cid:2)R,andthe exclusive binary character states. Hence, they cannot be cor-
online query application was generated using Oracle Applica- related with speciation and extinction rates on a phylogenetic
tionExpress(APEX). tree.
418 D.HOJSGAARDETAL.
To test the hypothesis that apomixis is causal to diver-
sity (Ho¨randl and Hojsgaard, 2012), we selected apomict and
non-apomict-containing sister clades in the phylogenetic tree
(Figure1).Incasesofpolytomies(seeFigure1),everycombi-
nationamongbrancheswasevaluated.AShapiro-Wilktestfor
normality was applied to numbers of genera and families, and
similaritiesinmediansweretestedusinganon-parametricone-
tailedWilcoxonMatched-PairsSigned-RankTestwherediffer-
ences in scores were assumed to be distributed symmetrically
aroundtheirmedian.Numbersofgeneraperfamilywereasin
Heywood(2007)exceptforminoradjustmentstoaccommodate
theAPGIIIsystem.AQ–Qplotcomparingnumbersofapomict
tonon-apomict-containinggeneraperordersuggestedthedata
arenotdistributednormally(X∼N(0,1)).Thehypothesisthat
4 apomixis occurs preferentially in certain orders was tested by FIG.2. Discoveriesofapomixisingenerawherepreviouslyithadnotbeen
1 reported(1997–2012).
0 non-parametric Spearman’s rank correlation (r ). Numbers of
2 s
e apomict-containinggeneraperorderwereplottedagainsttotal
n
Ju numbers of genera per order for all 63 angiospermous orders. ofPoaceae(http://archive.is/4yN5E),andgenerainAsteraceae
03 Regressionmodelswereevaluated,andthreeresidualstatistics, andOrchidaceaewereaccordingtotheAngiospermPhylogeny
14 Mahalanobisdistance,Cook’sdistanceandStandarizedDFFit, Website (http://www.mobot.org/MOBOT/research/APweb/).
0: wereusedtodetectthepresenceofoutliersandtoexplaintheir PhylogenetictreesweremodifiedafterPaneroandFunk(2008)
0
at influencesonmodelpredictability. for Asteraceae, the Grass Phylogeny Working Group (GPWG
n] Familiesweregroupedinto21categoriesbasedonnumbers II, 2012) for Poaceae, and Freudenstein et al. (2004) for
e
ng of genera per family (family richness). The percentage of Orchidaceae.
etti familiesineachcategorythatcontainapomictswasthencalcu- Biogeography information for apomict-containing genera
o
G lated (apomixis presence), and family richness and apomixis was taken from Mabberley (2008) and Tropicos.org (Missouri
et presencewerecomparedbySpearman’srankcorrelation.Three Botanical Garden, http://www.tropicos.org) with minor taxo-
a
sit families, Asteraceae (eudicot with gametophytic apomixis), nomic adjustments as described above. Distributions of these
r
e Poaceae (monocot with gametophytic apomixis), and Or- genera were then classified according to floral zone (Meusel,
v
ni chidaceae (monocot with sporophytic apomixis), were then 1978)withthegoalofdeterminingwhethernumbersofapomict-
U
- analyzed for intra-familial patterns of apomixis by regressing containing genera increase or decrease when moving from
st
gu numbers of apomict-containing genera per subfamily against warmertocolderclimates.Thisanalysiswasbasedonapomict-
u
A total numbers of genera per subfamily. Genera in Poaceae containing genera per climatic zone only, not frequencies of
g- were according to A World-wide Phylogenetic Classification apomict-containinggenerarelativetototalnumbersofgenerain
r
o
e
G
[
y TABLE 1
b
d Newrecordsofapomict-containingfamiliesaddedsinceCarman(1997)
e
d
a
o Family Order Genera Type Reference
nl
w
o Bignoniaceae Lamiales Tabebuia AE Saloma˜oandAllem,2001
D
Cannabaceae Rosales Humulus AorD Wettstein,1925
Erythroxylaceae Malpighiales Erythroxylum A Berryetal.,1991
Juglandaceae Fabales Juglans A SanandDumanoglu,2006;Guoliangetal.,2010
Lauraceae Laurales Lindera A Dupont,2002
Lecythidaceae Ericales Cariniana AE Saloma˜oandAllem,2001
Magnoliaceae Magnoliales Woonyoungia A Zengetal.,2003
Orobanchaceae Lamiales Orobanche,Cistanche D Jensen,1951;Pazy,1998
Phyllanthaceae Malpighiales Uapaca AE MaliroandKwapata,2000
Potamogetonaceae Alismatales Potamogeton D Teryokhinetal.,2002
Rubiaceae Gentianales Coprosma AorD Heenanetal.2002,2003
Sapindaceae Sapindales Magonia AE Saloma˜oandAllem,2001
Note.A=Apospory;D=Diplospory;AE=Adventitiousembryony.Forfullreferences,seetheapomixisdatabase(http://www.apomixis.uni-
goettingen.de).
APOMIXIS,TAXONOMICDIVERSITY,ANDBIOGEOGRAPHY 419
4
1
0
2
e
n
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J
3
0
4
1
0:
0
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e
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etti
o
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[
y FIG.3. Percentagesofapomict-containingfamiliesandgenerabyorder.
b
d
e
d
a therespectivezones.Thesixclimaticzonesincludedwere:arc- (http://www.apomixis.uni-goettingen.de). Total numbers of
o
nl tic(includingtheantarcticregion),boreal,temperate(including generavariedfrom12,758to13,150dependingoncircumscrip-
w
o submeridional,warmtemperate,andaustralzones),meridional tion.Fifty-onegenerawereaddedtothelistofCarman(1997)
D
(includingtheMediterraneanregion),subtropical(includingN- asnewlyidentifiedapomicts(Figure2;67papers),andanother
orboreosubtropicalandS-oraustrosubtropicalzone),andtrop- 35 were identified that had been reported between 1918 and
ical. 1997butwerenotincludedinCarman(1997).Thus,86genera
Statistical analyses were performed using IBM(cid:2)R SPSS(cid:2)R have been added. These represent 12 new apomict-containing
Statistics, Version 20 for Windows. For all evaluated cases, families from among 10 orders (Table 1). According to our
significance was tested at the p ≤ 0.05 (significant) and updatedlist,adventitiousembryony,apospory,diplospory,and
p≤0.01(highlysignificant)levelsofprobability. apospory and diplospory together occur in 148, 110, 68, and
17 genera, respectively. Adventitious embryony and gameto-
phytic apomixis also occur together in some genera, i.e., they
III. PHYLOGENETICDISTRIBUTIONS
arenotexclusivetraits.Thetypeofapomixisisnotknownfor
A. NovelRecords afewgenerawhereexperimentalevidenceconfirmsapomixis,
Thirty-two orders (52%), 78 families (19%) and 293 andanadditionalfivegenera,resultsofwhichwerepublished
genera (≈2.2%) were found to contain apomictic species from1998-2012,expressdevelopmentalfeaturessuggestiveof
420 D.HOJSGAARDETAL.
allsevenmajorcladesofangiospermsandinmostlargeorders
(Figure1).Thesethreeformsofapomixisoccurin24,17,and28
orders, respectively, which parallels distributions at the family
andgenuslevels.Insomeclades,apomixisisreconstructedas
ancestral. But here, the trait is often lost on certain terminal
branches, e.g., Canellales, Arecales, Oxalidales, Cornales and
Garryales(Figure1).
B. ApomixisinGenera,FamiliesandOrders
Among the 32 apomict-containing orders, apomict-
containing families ranged from 6.25–100% with a mean of
28.3%(Figure3).Interestingly,thethreeorderscontainingthe
three most apomixis-populated families, Poaceae, Asteraceae,
andRosaceae,alsocontainmultiplefamiliesinwhichapomixis
4 has not been reported. To date, Poaceae and Asteraceae are
1
0 the only apomict-containing families in the Poales (16 fam-
2
e ilies) and Asterales (11 families). Four of nine families in the
n
u
J Rosalescontainapomicts.Orderswiththehighestfrequenciesof
3
0 apomict-containingfamiliesweresmall,e.g.,Dipsacales(both
4
1 families),Dioscoreales(2of3families),andSapindales(5of9
00: families).
at FIG.4. Apomict-containinggeneraversustotalgenerabyorder.Twooutliers, Numbers of apomict-containing genera in apomict-
n] AandP,wereremovedfromthedatasetpriortopowerregression.(A)Asterales. containing orders were positively correlated with total num-
ge (P)Poales.
n bers of genera in the respective orders. This occurred regard-
etti less as to whether the total number of genera was considered
Go apomixisbutverificationstudieshavenotyetbeenconducted. to be 13,150 (Figure 4, r = 0.66, p < 0.01) or 12,758 (r
s s
et Werecordedtheseinthedatabaseas“uncertain.” = 0.68, p < 0.01). However, frequency values (numbers of
a
sit Apomixis occurs scattered over the whole phylogeny and apomict-containinggeneradividedbytotalnumbersofgenera
r
e appearsbothinbasalstemgroupsandinthederivedcladesof in the respective orders) were negatively correlated with to-
v
ni monocotsanddicots(Figure1).Adventitiousembryonyisthe tal numbers of genera (r = −0.513, p < 0.11). Two orders
U s
st- predominantmodeofapomixisinfabids,malvids,andlamiids. werelargelyresponsibleforthisnegativecorrelation:Asterales,
gu Otherthanthis,clearphylogenetictendenciesarenotapparent, with 1829 genera but with only one of 11 families containing
u
A i.e., apospory, diplospory and adventitious embryony occur in apomicts (1.5% of genera), and Poales, with 930 genera but
-
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o
e
G
[
y
b
d
e
d
a
o
nl
w
o
D
FIG.5. Familybiodiversityandapomixis.(grayline)Familycategoriesbasedonnumbersofgeneraperfamily.(blackline)Percentageoffamiliesineachgroup
thatcontainapomicticspecies.(dashedline)Percentageofangiospermousfamiliesthatcontainapomicts.
APOMIXIS,TAXONOMICDIVERSITY,ANDBIOGEOGRAPHY 421
with only one of 16 families containing apomicts (6.25% of
genera). In contrast, high frequencies of apomict-containing
genera per order were observed in small orders, e.g., Buxales
(16.7%) where six genera and 100 species are grouped into
twofamilies.Frequenciesofapomict-containinggenerainmost
orderswerelow,whichfitsapatternofabroadtaxonomicdis-
tributionforapomixisamongmanyordersratherthanaconcen-
trationofapomixisinfeworders.Spearman’srankcorrelations
betweennumbersofapomict-containinggeneraandtotalnum-
bersofgeneraamongapomict-containingordersrevealedsim-
ilarhighlysignificantcorrelationcoefficientsforgametophytic
(r =0.477,p<0.05)andsporophytic(r =0.475,p<0.05)
s s
apomixis.
AsshownbyQ-Qplotanalysisofthecompletedatasetand
4 Shapiro-Wilktestsofsisterorders,normalityatthe1–α=0.99
01 confidencelevel(SW=0.757;P<0.01)couldnotbeassumed.
2
e Wilcoxon tests revealed that median values for families and
n
u generaofsisterclades(W =3,Z=−2.8241,p=0.0024,N=
J
03 12)aresignificantlyhigherinapomicticclades,andtheydepict
4 anexceptionallylowprobabilityofrandomnessforthesevalues.
1
0: Hence,apomixisisstronglyassociatedwithbiodiversity.
0
at
]
n C. FamilyDiversityandApomixis
e
g
n Mostfamiliesofangiospermslackdiversity,e.g.,252fami-
etti lies(61%)containonly1–5genera.Inthisrespect,presenceof
o
G apomixisinfamilieswaspositivelycorrelatedwithnumbersof
et genera per family (Figure 5). Fifty percent of families with >
a
sit 40generacontainedatleastoneapomict.Thisincreasedto63%
ver forfamilieswith>80genera,andallfamilieswith>250gen-
ni era contained apomicts. Likewise, case studies of three highly
U
st- diversefamiliesrevealedstrongcorrelationsbetweenpresence
u
g of apomixis in intra-familial taxa and total numbers of genera
u
A inthesetaxa(Figure6).However,thesecorrelationsdonottell
-
g thewholestory.Averagelevelsofbiodiversityamongfamilies
r
o
e are also important. For example, a genus selected at random
G
y [ fromalargegroupofgeneracomposedofacombinationoflow
b diversity families, e.g., 1–5 genera each, was less likely to be
d
e apomicticthanifitwereselectedfromasimilar-sizedgroupof
d
a
o generatakenfromamongfamiliesorsub-familiesthatcontain
nl
w manygenera.
o
D
D. BiogeographyandApomixis
Apomict-containinggeneraweredistributedworldwidewith
38, 13, and 11% occurring in 2, 3, and > 3 climatic zones,
respectively. They also tended to occur mostly in tropical to
temperate zones. Few apomict-containing genera were found
in boreal to arctic zones compared to lower latitude zones
(Figure 7A, B). Sporophytic and gametophytic apomixis ex-
hibited similar patterns of distribution across climatic zones
(parametric Spearman correlation r = 0.95, p < 0.05) with
FIG. 6. Apomixis in subfamilies. (A) Asteraceae. (B) Poaceae. (C)
sporophyticapomixisbeingslightlymoreabundantinthetrop-
Orchidaceae.
ics and gametophytic apomixis being slightly more abundant
elsewhere(Figure8).
422 D.HOJSGAARDETAL.
FIG.7. Geographicdistributionsofapomict-containinggenera.(A)Byclimaticzone.(B)Byoccupationofonetomultipleclimaticzones.
4 IV. APOMIXISANDEVOLUTION and it also involves the differential expression of gene fami-
1
20 liesthatregulatesexualdevelopment(Grimanelli,2012).Thus,
ne A. PatternsatHigherTaxonomicLevels the totipotency and epigenetic flexibility of plant cells makes
u Apomixisiswidespreadandscatteredtaxonomicallyamong
J various routes toapomixis possible.Adirectintervention dur-
3 orders, and we found strong evidence that it has arisen multi-
0 ing meiosis, as occurs in diplospory, is perhaps more difficult
4 pletimeswithnocleartiestospecificplantfamilies.However,
1 toachieveinnaturalplantpopulations.Thus,diplosporyisthe
0: the phylogenetic tree (Figure 1) does suggest that apomixis is
0 leastfrequentpathway.TheartificialMiMesystemofproduc-
at potentiallyancientinsomemajorcladesespeciallythoselead- ing clonal embryos in seeds of Arabidopsis requires a com-
en] ing to the commelinids, fabids and lamiids. While sexuality is bination of mutations in three meiosis genes (d’Erfurth et al.,
g ancestralinangiosperms,howandwhenapomixisaroseinthis
n 2009). As pointed out earlier, such combinations of mutations
etti group is less certain. What we can say is that stable forms of are unlikely to occur in natural populations because selec-
o apomixis either repeatedly evolved de novo during angiosper-
G tion would act against each intermediate step (Van Dijk and
et mous evolution (hypothesis of multiple de novo origins) or its Vijverberg, 2005). Meiosis itself is highly conserved in eu-
a
sit expressionintypicallysexuallineageswasrepeatedlytriggered karyotes(Maliketal.,2007),andinfacultativelydiplosporous
ver during evolution (conserved pathways hypothesis). The latter plants, steps of meiosis tend to be skipped rather than altered
Uni suggests unreduced gamete formation coupled with partheno- (Carman,1997).
st- genesis(basicapomixis)isanancientepigeneticcompetencyin- Likeapomixisingeneral,apospory,diplosporyandadventi-
u heritedfromangiospermousancestorswithinnovationsintypes
g tiousembryonyareeachtaxonomicallywidespread(Figure1),
u ofapomixisarisingthereafter(Carmanetal.,2011).Inthisre-
A and their genetic or epigenetic regulatory mechanisms differ
rg- spect, it is remarkable that adventitious embryony is the most (Ozias-Akins and van Dijk, 2007). The hypothesis of a tax-
o frequenttypeofapomixis.Thedirectdevelopmentofembryos
e onomic predisposition for the evolution of apomixis within
G
y [ has been reported from other plant tissues, e.g., from anthers certain clades with apomixis-inducing genetic factors moving
ded b 1(S9o7r9ia).nIonegtenael.r,a2l,0e1m3)b,rlyeoanvyesc,aannbdeoatchteivraotergdainnsm(Tanisyseprlaatntetcealll.s, rnaoptisdulyppwoirttheidnbtyheosuercclaodmepsil(aVtaionnD.IinjkcaonndtraVsitj,voeurbredragt,a2s0u0g5g)esist
a independentoffertilization(Carman,1990).
o thatangiospermsingeneralhaveacapacitytoswitchfromsex
nl Thesecondaspectofgametophyticapomixis,i.e.,partheno-
w to apomixis. But this capacity, particularly with regard to ga-
o geneticdevelopmentofaneggcell,alsooccursspontaneously
D metophyticapomixis,ismorepronouncedinlarge,diverseand
in otherwise sexual plants (Asker and Jerling, 1992). In this
genomically-complexclades(Figures5and6).
respect, methylation patterns and other epigenetic marks are
knowntoparticipateinregulatingembryoandendospermdevel- B. Apomixis-sexSystems
opment(LawandJacobsen,2010).Incontrastwithmammals, Thelowfrequencyofapomixisweobservedatthegenuslevel
whereaparentalcontributionisessentialforembryony,genomic (about 2%) is likely due to (i) under-sampling, as suggested
imprintinginplantsappearstoberequiredforendospermfor- by the linear increase in newly discovered apomicts per year
mationonly,andnotforembryoformation(Engelsta¨dter,2008). between1997and2012(Figure2)coupledwithmethodological
Independencefromapaternalepigenomiccontributionmayal- problemsofrecognizingapomixis(Leblanc,2000;Matzketal.,
low for more flexibility in the evolution of alternative asexual 2000;Ho¨randletal.,2008),(ii)naturalconstraintsthatinhibit
reproductivepathways. shifts from sexuality to apomixis (van Dijk and Vijverberg,
Strikingly, our data indicate that apospory is more frequent 2005;Engelsta¨dter,2008;Ho¨randletal.,2008;Ho¨randl,2009),
than diplospory. Apospory involves activation of gametophyte and (iii) spread of apomictic lineages followed by reversions
development in a nucellar cell rather than in the megaspore, to sexuality and further diversification. According to the latter