Development and evolution of extreme synorganization in angiosperm flowers and diversity: a

19 Pages·2016·2.04 MB·English

AnnalsofBotany117:749–767,2016
doi:10.1093/aob/mcv119,availableonlineatwww.aob.oxfordjournals.org
REVIEW: PART OF A SPECIAL ISSUE ON DEVELOPMENTAL ROBUSTNESS
AND SPECIES DIVERSITY
Development and evolution of extreme synorganization in angiosperm
flowers and diversity: a comparison of Apocynaceae and Orchidaceae
PeterK.Endress*
InstituteofSystematicBotany,UniversityofZurich,Zollikerstrasse107,8008Zurich,Switzerland
*[email protected] D
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Received:25March2015 Returnedforrevision:27May2015 Accepted:22June2015 Publishedelectronically:20August2015 lo
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(cid:2)BackgroundandAimsApocynaceaeandOrchidaceaearetwoangiospermfamilieswithextremeflowersynor- fro
ganization.Theyareunrelated,theformerineudicots,thelatterinmonocots,buttheyconvergeintheformationof m
pooflfllionriaalaonrdgapnoslliisnaarpiar,ewcohnidchitidoon.nIonteoaccchurfaimnailnyyeoxttheenrsiavnegsitousdpieersmonfaflmoiwlye,randdevfeolropwmhiecnhteaxntdreemvoelusytinoonrghaanviezabteioenn https
performed;however,newercomparativestudiesfocusingonflowersynorganizationandinvolvingbothfamiliesto- ://a
c
getherarelacking. a
d
(cid:2)ScopeForthisstudyanextensivesearchthroughthemorphologicalliteraturehasbeenconducted.Basedonthis e
m
andmyownstudiesonflowersinvariousApocynaceaeandOrchidaceaeandcomplexflowersinotherangiosperms ic
withscanningelectronmicroscopyandwithmicrotomesectionseries,areviewonconvergentfloraltraitsinflower .o
u
developmentandarchitectureinthetwofamiliesispresented. p.c
(cid:2) Key Findings There is a tendency of protracted development of synorganized parts in Apocynaceae and om
Orchidaceae(developmentofsynorganizationoftwoormoreorgansbeginsearlierthemoreaccentuateditisatan- /a
o
thesis).Synorganization(orcomplexity)alsopavesthewayfornovelstructures.Oneofthemostconspicuoussuch b
nevoevre,listtrisucpturorebsabinlyAepnohcaynncaecdeabeyissytnhoercgoarnoiznaat,iownhiocfhoitshneor,tethxeisptirnogd,uflcotroaflspyanrotsr.gaInnizcaotniotrnasotftoexsiystninogrgoarngiazneds;phaorwts-, /article
thecoronaappearsdevelopmentallylate. -a
b
(cid:2)ConclusionsSynorganizationoffloralorgansmayleadtoalargenumberofconvergencesincladesthatareonly s
verydistantlyrelated.Theconvergencesthathavebeenhighlightedinthiscomparativestudyshouldbedevelop- tra
c
mentallyinvestigateddirectlyinparallelinfuturestudies. t/1
1
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Key words: Apocynaceae, Orchidaceae, angiosperm flower development, flower evolution, flower symmetry, /5/7
synorganization,congenitalfusion,postgenitalfusion,pollinium,pollinarium,speciesdiversity. 4
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INTRODUCTION 0
recognize the basic organs immediately, especially in androe- 2 b
Theintegrationoffloralorgans,resultinginfunctionallyfitting ciumandgynoecium. y g
positions of all floral organs and covariation of fitting parts, is HarderandJohnson(2008)discussedthefunctionandevolu- ue
s
an evolutionarily important trend in angiosperms (Armbruster tion of aggregated pollen in angiosperms, also addressing t o
et al., 2009, 2014). In contrast to ecological aspects, develop- Apocynaceae and Orchidaceae. It was shown that pollen loss n 0
mental aspects of integration have found much less attention during pollination in plants with pollinia is considerably lower 3 A
m(Wecahganneirs,m20to14i)n.crAeasmeasjuocrhdinevteegloraptmioenntiaslsyannodrgeavnoizluattiioonnaoryf tHhoanweinveprl,atnhteswevitohlugtiroannuolafrppoolllilneina(aHnadrdpeorllainndariRaonuetleedye,d20co0m6)-. pril 2
0
modulesbyhighlysymmetricalarrangementandtangentialand plex morphological preconditions by intimate synorganization 19
radial congenital and postgenital fusion. Such synorganization of floral organs, and this was only achieved in Apocynaceae
is extreme in Apocynaceae (especially Asclepiadoideae) and andOrchidaceaeconvergentlyasaprominentnovelty.Thepre-
Orchidaceaeamongangiosperms. sentpaperfocusesonthemorphology,developmentandevolu-
When we analyse a flower we commonly focus on the four tion of the highly synorganized flowers of these two families.
organ categories sepals, petals, stamens and carpels. They are Without intimate knowledge of the developmental processes
the organs that make up a flower. They are used in basic de- anddiversityitisdifficulttounderstandthestructuralevolution
scriptionsofflowersandarealsothefocusofmoleculardevel- of these flowers. There is an extensive and exciting literature
opmental studies on flowers. The classical ‘ABC model’ of on the functional aspects of flowers of Apocynaceae and
flower development rests on them (Coen and Meyerowitz, Orchidaceae. However, the literatureon comparativefloral de-
1991). In most flowers we encounter, these organs are easily velopmentandmorphologyinthetwofamiliesismuchsmaller
seenandeasytodistinguishfromeachother.However,looking (e.g.Vogel,1959;Schick,1980,1982a,b,1988,1989;Kunze,
at the flower of an orchid or an asclepiad, it is difficult to 1981,1990,1991,1994,1995,1996,1997,2005;Fallen,1986;
VC TheAuthor2015.PublishedbyOxfordUniversityPressonbehalfoftheAnnalsofBotanyCompany.
Allrightsreserved.ForPermissions,pleaseemail:[email protected]
750 Endress—Developmentandevolutionofextremesynorganizationinflowers
Kurzweil, 1987a, b, 1988, 1993, 1995, 1998; Kurzweil and organsintoacomplexstructureiscalledsynorganization.Thus,
Weber, 1992; Liede and Kunze, 1993; Endress, 1994, 2011; a common general evolutionary direction is from independent
Liede, 1994; M. E.Endress, 2003; Kocyan andEndress, 2001; organstoacomplexoforgans.Intheextreme,thiscomplexof
Kurzweil and Kocyan, 2002; Kunze and Wanntorp, 2008). As organsmay becomesosynorganized that itbehaves like a sin-
Apocynaceae and Orchidaceae are the only angiosperms that glecomplexunitorasingleorgan.
havepolliniaandpollinaria,itisnotsurprisingthatinitialcom-
parisonsbetweenthetwofamiliesweremadelongago(Brown,
1833). Preconditionsforsynorganizationoffloralorgans
An important aspect of the convergent evolution of pollinia
Preciselocalizationoforgans or organparts isnecessaryfor
is economical use of available pollen and male fitness, which
synorganizationindevelopmentofthecomplexstructureandat
appears to be an important principle in floral biology (Barrett
thesametimeforprecisefunctioningoftheflower[e.g.attach-
and Harder, 2006; Harder and Johnson, 2008). Various struc- D
ment of pollinaria to pollinators and deposition of pollinia on o
tural devices have evolved to this end (Erbar and Leins, 1995; w
stigmas,suchasinCatasetinae(Romero,1990),seebelow].An n
Leins and Erbar, 2006, 2010), and the advent of pollinia is a lo
important precondition for such precise mutual position of the a
particularlyconspicuoustrendinthisrespect. floralorgansiswhorledphyllotaxis,incontrasttospiralphyllo- ded
Bothfamiliesarespecies-rich,andtheadventofpolliniaand taxis (Endress, 1987, 1990, 2006). This allows (1) tangential, fro
pollinariamayhavebeenanimportantfactorforthisdiversity. m
However,floralsynorganizationmayalsohaveledtootherfea- circumferential synorganization among the organs of a whorl h
turesdrivingspeciation,suchasdevicesforcingpollinatorsinto (synsepaly,sympetaly,synstemony,syncarpy)and(2)sectorial ttps
precise positions on the flowers for pollinaria removal and de- synorganization (e.g. perianth organs and stamens in many ://a
monocots, and inner perianth organs and stamens in several c
position, or various ways of pollinator deception, especially in a
basaleudicots)(Fig.1).Oneofthemostcommontangentialor de
orchids.Apocynaceaecomprisesalmost5000species.Thesub- m
cladeof Asclepiadoideaeplus Secamonoideae,whichisnested cmiracjuomritfyeroefntaianlgisoysnpoerrgmasni(zEantidornesssi,s1s9y8n2c)a.rpAyl.soItqoucitceurcsominmtohne ic.o
inApocynaceae,hasmorespecies(3180)(Meve,2002)thanall up
other subclades of the family together (Periplocoideae, is sympetaly, which is present in many eudicots, especially .co
asterids, and syntepaly in several monocots. A combination of m
Apocynoideae and the basal grade of Rauvolfioideae), and it both tangential and radial synorganization also occurs, such as /a
has171genera(M.E.Endressetal.,2014),whereastherestof ob
tOfharmechilfiiademasc,ielwyaeithhaarsaepo1pn9roe4xo.gf2et5nhe0er0at0w(osMpme.coiEesst. saEpnnedcdir7ees3s-s5ricgehetnaaenrlg.a,io(2Cs0ph1ear4sm)e. srmaydannitieypianaslytmerpaildnusysafmnudsoinsooonmcobetestr,woasenieddnst(beeep.tgaw.lseGeaannlidppeesittnaalamseeaonnfsdRosnuttaatmhceeeanseas,mEinel /article-a
Ottra et al., 2013), or between stamens and carpels in b
et al., 2015). Apostasioideae have two genera and 14 species OrchidaceaeandApocynaceae(seebelow;Fig.2). stra
(Chase et al., 2015), Vanilloideae 14 genera and 245 species c
(Chaseet al.,2015),Cypripedioideae fivegeneraand 169spe- t/11
7
cies (Chase et al., 2015), Orchidoideae 198 genera and 4575 /5
species(Chaseetal.,2015),Epidendroideae516genera(Chase Developmentalprocessesandresultsofsynorganization; /74
differentkindsoffusion 9
et al., 2015) and 21160 species (Freudenstein and Chase, /1
7
2015), and Cymbidieae and Vandeae of Epidendroideae to- Synorganization most commonly occurs by means of (1) 4
0
gether have 300 genera and 4528 species (Chase et al., 2015). postgenitalfusionor(2)congenitalfusion,and(3) rarelywith- 00
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Family stem ages werecalculated as 52 Mya for Apocynaceae outfusion.Inpostgenitalfusionadjacentfreeorgansorpartsof b
y
and 109 Mya for Orchidaceae (Magallo´n et al., 2015). organsmakesecondarycontactandthecontiguousepidermises g
u
However, when each of the salient morphological innovations fuse.Incongenitalfusiontheprimarymeristemsofadjacentor- e
s
firstappearedwithineachfamilyislargelyunknown. gans become confluent so that these organs develop as a unity t o
n
(confluenceofmeristemsormeristemfusion);thus,theepider- 0
3
mis is not involved in the fusion process. Postgenital and con- A
FLOWER SYNORGANIZATION IN GENERAL gloecnaittiaolnsf.usPioosntgeonftietanl fcuos-iooncchuarsianlsogybneoeencicaallaenddepaitdesrpmeaclifoicr pril 2
Thegeneralevolutionarytrendofsynorganizationinflowers 01
ontogenetic fusion, and congenital fusion has also been called 9
Angiosperm flowers are characterized by basically three kinds phylogenetic fusion (Cusick, 1966). For a discussion on meri-
oforgans,whichservethefollowingbasicfunctions:(1)protec- stem fusion, see Hagemann (1973), and for molecular aspects
tionandopticalattraction(theperianthorgans:tepalsorsepals offusion,seethereviewbySpechtandHowarth(2015).
and petals), (2) male function (the androecial organs: stamens) A general advantage of congenital fusion of organs in a
and (3) female function (the gynoecial organs: carpels). These floweristhatdifferentialelongationofthebasalandupperpart
floralorgansaremodularstructures,repetitiveunitsofthesame of all organs makes possible a broad potential of shapes with
kind. Each kind of organ occurs in different numbers and ar- variousproportionsoffreeandfusedparts.Withoutcongenital
rangementinaflower,althoughtheyalwayshavethesamese- fusionthisisnoteasilyachieved.
quence from the periphery to the centre of the flower: An interesting feature of postgenital fusion is the potential
perianth!androecium!gynoecium.Thereisacommonevolu- for easy reopening at anthesis after tight closure in bud
tionary trend in angiosperms that organs of the same kind or (Endress,2006).Petalsareoften(partiallyorcompletely)post-
also organs of different kinds become more intimately associ- genitally united in bud (and partially also at anthesis) in many
ated.Suchassociationorintegrationofancestrallyindependent asterids, especially campanulids (Araliaceae, Asteraceae,
Endress—Developmentandevolutionofextremesynorganizationinflowers 751
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FIG.1.Differentpotentialforsynorganizationoffloralorgansindifferentphyllotaxispatterns.(A)Spiralphyllotaxiswithlimitedpotential.(B)Whorledfloralphyl- fro
lotaxiswithhighpotentialforradialandtangentialsynorganization.Blacklinesindicatepreferredlocationsforsynorganization. m
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FIG.2.(A,B)Flowerswithhighdegreeofsymmetryandfirmconsistencyoffloralorganswithplastic-likeappearance.(A)Calotropisprocera(Apocynaceae-
Asclepiadoideae).(B)Acinetadensa(Orchidaceae-Epidendroideae).(C,D)Floraldiagramswithsynorganizationsindicated.Green:outerwhorlofperianth;red:in-
nerwhorlofperianth;orange:corona;yellow:androecium;blue:gynoecium;black:pollinarium.Thickredlines:congenitalfusion;thickpinklines:postgenitalfu-
sion.(C)Asclepias(Apocynaceae).(D)MonandrousOrchidaceae,flowershowninresupinateposition.
Campanulaceae), in Gentianales (basal Apocynaceae sensu common in anthers, such as in many buzz-pollinated flowers
stricto (s.s.), Fallen, 1986; Rubiaceae, Robbrecht, 1988; basal (Endress,1994,2006)andinothercomplexflowers,suchasin
lamiids:Icacinaceae,EndressandRapini,2014).Postgenitalfu- Balsaminaceae(e.g.VogelandCocucci,1988).Rarelyitoccurs
sion is most common in gynoecia in intracarpellary and inter- betweenstamensandcarpels(balsaminoids,vonBalthazarand
carpellarypositions(e.g.Baum,1948;Endress,2015).Itisalso Scho¨nenberger,2013).
752 Endress—Developmentandevolutionofextremesynorganizationinflowers
A rare kind of intense synorganization without a particular there is plasticity at other structural levels to attain the present
fusion is known from Geranium robertianum (Endress, 2010). diversity.
Herefusiononlyoccursinthegynoecium,whichissyncarpous. Thecomplexityoftheflowersinasclepiadsishighlightedby
Allothersynorganizedparts(thesepalsamongthemselves,and three structures: (1) gynostegium, (2) pollinarium (five per
the sepals withpetals, stamens and carpels) arefree from each flower)and(3)corona.Thesestructuresarenotbasicfloralor-
otherbutare heldtogetherbyarchitectural modificationsother gans, but rather are already synorganized organs or new parts
thanfusion. enabled by synorganization of other structures (see also
Generalandconspicuousresultsoffloralsynorganizationare Endress,1994).
an enhanced expression of the three-dimensional structure of Theuppermostpartofthegynoecium,thestylehead,andthe
the flowers and of internal morphological spaces. This may anthers are postgenitally fused. This organ complex is called
cause floral parts to become hidden. In addition, organs may gynostegium.Onthesurfaceofthegynostegiumthefunctional
become difficult to distinguish from their neighbours because units for pollen transport are formed. The style head itself de- D
o
theirindividualitybecomesobliterated. velopsbypostgenital fusion ofthe two carpel tips.The corona w
n
Alsoconspicuousisthat synorganizationleads torobustness isanovelstructurebetweencorollaandandroecium;itisoften lo
a
orstabilityofthenovelbauplanbothinindividualdevelopment highly subdivided into a number of parts, which together form de
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and in evolution. Once the synorganized structures are estab- acomplexapparatuswithseveralfunctions.Initssimplestform fro
lishedtheyarestableandarenoteasilylostagain.Thisprinci- thereisacoronaelementbehindeachstamenandisfusedwith m
ple was nicely demonstrated by Simon (1962) with his it, but other parts of the corona are often also present between h
watchmaker parable. At any new level of synorganization it is thestamens.Thepollinariaareformedbythesynorganizedan- ttps
possible to experiment with variations at many single new droeciumandgynoecium. ://a
c
pointswithoutharmingtheentiretyofthebauplanandtoattain The pollinaria are the strangest parts of the flowers. Each a
d
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newdiversity. pollinariumisacompositeapparatusforpollentransfer.Pollen m
from each theca is united to form a compact pollinium, and is ic.o
thusnot dispersedassinglegrains.Inaddition,polliniaarenot up
EXTREME SYNORGANIZATION IN transportedsingly,butalwaystwotogether,oneeachfromtwo .co
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APOCYNACEAE AND ORCHIDACEAE neighbouring anthers. They become connected by a translator. /a
Atawmpooocnfyganmaaniclgeieaiosespw(eeirutmhdisct.hoTetsh)meyaonsadtreeOxnrtocrethmipdheaycfleolaogewene(emrtioscynanollocyrogtrsae)nlaiatzeraedtiobthnuest Eibsuactcohisntncreaocnmtselpdaottsooerdacnoonfasrsimcsut.slTpothfeedatscrealicnprselaatnitoodnrt.dwIotoeissarnumontsu.csuEoanalscifhsotproosfelltciinrsesiutuemed, ob/article
materials to attain such a complex and precisely formed -a
haveconvergentlyevolvedflowerswithpolliniaandpollinaria. b
A conspicuous difference is that the flowers of Apocynaceae structure. stra
Thisraisesseveralquestions:Whereandhowisthistransla- c
a(Freig.p2o)l.ysymmetric, those of Orchidaceae monosymmetric tor formed? What are the mechanisms to take the translators t/117
out of a flower? What are the mechanisms to position the pol- /5
linia at the right site in the recipient flower? The answers to /74
9
these questions are in the precise synorganization of the floral /1
FlowersofthemostelaborateApocynaceae(cladeof 7
parts,especiallythecoronaandthegynostegium. 4
AsclepiadoideaeplusSecamonoideae) 0
The five translators are formed each on a corner of the ex- 00
2
Itiseasiesttobeginwiththe mostextremelycomplexflow- panded, pentagonal style head (Fig. 2A, C). Each corner has a b
y
ers, thus flowers with the highest synorganization, and later longitudinallydirectedconcavity,whichfunctionsasthemould g
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show how the complexity develops during ontogeny and also forthesecretionofaclip(Fig.3A).Thetwoflanksofthecor- e
s
show some of the evolutionary steps that led to the increasing nersecretethearms.Eacharmcontactstheadjacentpollinium, t o
n
synorganization. Floral organ numbers in the Asclepiadoideae whichispresentedatthissitefromtheopenedantherandisat- 0
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plusSecamonoideae(thiscladeherecalled‘ascleps’)areabso- tached to the arm. In this way the clip is presented exactly in A
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lpuetlesly(afsixfeadr:afsivIeksneopwal)s,infivaellp3e1t0a0ls,spfievceiesst,amweitnhsouatndextcweoptcioanr-. theInmAidsdclleepoifatdhoeiduepapee,reeancdhogfuiadgeuriadielirsaiflo(rFmiegds4byanthde5aAd)j.acent ril 2
0
1
Within some species, single aberrant flowers with four or six flanks of two neighbouring anthers. It guides pollinator body 9
petalshavebeenreportedbutareexceptional(Fuchs,2013).In partstothecliportothestigma.Thus,therearefiveguiderails,
thebasalgradeofApocynaceaeitissimilar,butthereareafew five clips and five functional stigmatic units in each flower.
taxathathavenormallymorethantwo(uptofive)carpels(e.g. The anther flanks that form the guide rails are the transformed
M.E.Endressetal.,1997),orraremutantswithsurpluspetals (i.e. sterilized and histologically reinforced) dorsal pollen sacs
inspecieswithnormally5-merousflowers(Wangetal.,2011). of each theca. Thus, each anther produces only two pollinia
Inascleps,inaddition,thefloralorgansofallfloralwhorls(ex- (from the ventral pollen sacs). The anther flanks are postgeni-
ceptthesepals)aretangentiallycongenitallyfused.Coronaand tally connected with the style head below the translator glands
stamens are also radially congenitally fused.Postgenital fusion (Fig.5B).Thestigmaisnotontopofthegynoecium,butislo-
occursbetweenthe anthersandthestyleheadandintheupper cated on the underside of the style head. It is subdivided into
zone between the two carpels. In Apocynaceae in general, the fivefunctionalunits.Eachunitisplacedexactlyintheradiusof
corollatubeoftenhasapostgenitallyfusedzoneabovethecon- a guide rail. The stigma units are not visible from the outside
genitallyfusedzone(e.g.Fallen,1986;Kunze,2005).Thissta- because they are hidden in a concavity behind the guide rails
bilityofthebauplanisnecessaryforsynorganization.However, ontheundersideofthestylehead(Fig.5C).Belowthestigma,
Endress—Developmentandevolutionofextremesynorganizationinflowers 753
A arm clip B
b
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FIG.3.Pollinariaandtheirpositionintheflower.(A)Vincetoxicumnigrum(Apocynaceae-Asclepiadoideae),microtometransversesectionofgynostegium,showing D
onecornerofstylehead(s)withsecretedtranslatorconsistingofclipandtwoarms,whichhavebecomeattachedtothepollinium(p)ofthetwoadjacentanthers(a) o
w
andformingthepollinarium.SeealsooverviewofthissectioninFig.5A.(B)Ophrysfusca(Orchidaceae-Orchidoideae),microtomelongitudinalsectionofgynoste- n
mium,showingpartofthepollinarium,consistingofsectilepollinium(p)subdividedintomassulae,caudicula(c)andviscidium(v)withscutellum(s),coveredby loa
bursicula(b);antherwall(a);rostellum(r).Scalebars:A¼100mm,B¼200mm. de
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FIG.4.YoungflowerbudsofAsclepiascurassavica(Apocynaceae-Asclepiadoideae)showingdevelopmentalstepsofsynorganization,scanningelectronmicro- le
graphs,allfromtheside,withoneguiderailinthecentre.(A)Theantherflanksthatlaterformtheguiderailsaremarkedwithyellow.Thezoneofpostgenitalfusion -a
b
oftheantherflankswiththestyleheadmarkedwithpink.Thecoronaelementsarenotyetformed.(B)Laterstage.Theantherflanksthatlaterformtheguiderail s
aremarkedwithyellow.Thecoronaelements,markedwithblue,beginningtobeformed.(C)Stilllaterstage.Theentireanthersaremarkedwithyellow;thelower tra
c
entranceoftheguiderailhasbecomewider.Coronaelementsarenowmuchlonger.Clipofthepollinariumabovetheguiderailismarkedwithpink.Partofthestyle t/1
headabovetheclipismarkedwithred.Scalebars:A¼100mm,B¼200mm,C¼500mm. 1
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at the base of the guide rails, there are five nectaries in niches Whenapollinariumisdrawnoutofafloweritisatfirstposi- 4
0
between the (at this level) congenitally fused stamens (and tioned perpendicular to the insect, but it soon (about 1min) 00
2
stamens fused with the corona elements in the same radii) bendsforwardbyadifferentialdryingprocessofthetranslator. b
y
(Fig.5D).Thenectariesmayalsosecreteadditionalsubstances, The translator is not homogeneous but is composed of lipo- g
u
perhaps in conjunction with pollen tube growth (Christ and philicandhydrophiliccomponents,whichcausebendingbythe e
s
Schnepf, 1985; Vieira and Shepherd, 2002). Thus, in the five drying process (Schnepf et al., 1979). In this way it becomes t o
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radiioftheguide rails,exactlyalignedfrom bottomtotop,are optimallypositionedforinsertionintoaguiderailofarecipient 0
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the nectaries, the stigmas and the clips of the translators. The flower. If a pollinium comes into contact with the stigma, it A
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gwuhiedreertahielsclaipreisblroocaadteesdt(aFtigth.e5Ab–aDse).aTnhdutsa,pbeordtyowpaarrtdsotfhevitsoitp- setliecmksenthtseroefatnhdebcroeraoknsaoafflsforoamctthaesthraonldsilnagtord.eTvhiceeasnftoerstainmseincatsl ril 2
0
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inginsectswilleasilygetcaughtinthebasalpartofaguiderail and,becausetheyprotrudeattheperipheryofthefloralcentre, 9
andthenbedrawnupwardsexactlyintotheclipwhentheinsect often the ends of the legs automatically come to lie into the
moves about on the flower or leaves the flower. Below the guide rails, and most often the pollinaria become attached to
guide rails the corona elements are, in addition, congenitally thelegs.
fusedwitheachother(Fig.5E,F). Inmostcases,aninsertedpolliniumprovidesonlyoneofthe
Movements of insects on the flower are greatly encouraged two carpels with pollen tubes (Sage et al., 1990; survey in
by the compartmentalized location of the nectar. In Asclepias Vieira and Shepherd, 2002; Vieira et al., 2012). Thus, there is
nectar is stored (and presented) in ten sectors of the flower by nofunctionalcompitum.Onlyrarelyarebothcarpelsservedby
troughs formed by coronal elements, which are provided with thepollentubesofasinglepollinium(Kunze,1991).Thereisa
nectar by capillary forces from the five nectaries (Galil and strange asymmetry because one carpel may be served from
Zeroni, 1965). These flowers are thus intricately differentiated threestigmaticchambers,butthesecondcarpelonlyfromtwo.
revolver flowers, i.e. flowers in which nectar is available for Oftenonlyonecarpeldevelopsintoafruit.
pollinatorsnotfromasingleposition,butinthiscasefromfive How can the style head of a dimerous gynoecium (Fig. 6A)
ortendifferentpositions. produce five pollinaria? The mismatch between the
754 Endress—Developmentandevolutionofextremesynorganizationinflowers
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FIG.5.CentreofaflowerwithgynostegiumofVincetoxicumnigrum(Apocynaceae-Asclepiadoideae),microtometransversesectionseriesatsixlevels,fromtop, /5
downwards.(A)Levelofthefivetranslatorglandsatstylehead.Thetwocarpelspostgenitallyfusedandformingfiveedges,eachwithatranslatorgland,thetwo /7
4
maincarpellaryvascularbundlesstilldistinct.(B)Levelofpostgenitalfusionofantherflankswithstyleheadandhistologicalreinforcementofantherflanksfor 9
guiderailfunction.(C)Levelofthefivestigmasatlowerendofstylehead.(D)Levelofthefivenectariesinthefivegroovesbelowtheguiderails.Thefivecorona /17
portionscongenitallyfusedwiththestamens.(E)Levelofthefivecorona/stamenportionscongenitallyfusedwitheachother,leavingfiveholesbetweenthem.The 40
twocarpelsfree.(F)Levelofcoronaandstamensformingaringaroundthegynoecium,atthebaseofthefiveholes.Carpelsattheupperportionoftheovary.Scale 00
bars:all¼500mm. 2 b
y
g
u
pentamerous outer region of the flower and the dimerous gy- with regard to nectar holder function (Kunze, 1997). Units of e
s
noecium has been overcome by the early postgenital fusion of the corona maybesimpleinsmallflowers(e.g.Vincetoxicum) t o
n
the carpels and by complete conformation of the gynoecium or complex inlarger flowers(Fig. 7) (e.g.Asclepias, Galil and 0
3
symmetrytothatoftheandroecium.Thus,theupperpartofthe Zeroni, 1965, or Hoya, Kunze and Wanntorp, 2008), and con- A
ginygnodeecvieulmopmbeecnotm(Feisgs.e6cBo)n.dTahriilsyisfunniccteiloynsaelleynpinenctaasmeserionuwshdiucrh- vAoslculteepdiaidnoCidaelaoetriospsistro(PnugrlyiainndfluSehnicaemd,b1y96t6h)e.iSnttaemgreantioshnaopfeailnl pril 2
0
1
the two carpels have a random, irregular position with respect parts of the gynostegium (Liede, 1994; Kunze, 1996). The 9
to the outer floral whorls. Thisis an impressive example of an shapeofthestylehead(Simo˜esetal.,2007a)andthedepthof
imprinted shape, a shape superimposed (moulded) by the five- the guide rails are evolutionarily plastic, correlated with the
angledshapeoftheimmediateneighbourhood(Endress,2008). size of the pollinators (Fig. 8). Diversity in size of the entire
Thegynoeciumremainsclearlydimerousatthebase,butlooks flowers is addressed below. The synorganization of flowers in
pentamerouson top at anthesis. Only the two vascular bundles Asclepiadoideaeunderlyingthediversityasdescribedhereisa
inthestyleheadatanthesisgivetestimonytoitsdimerousori- constantfeaturethroughthesubfamily,asseveraldetailedmor-
gin(Fig.5A–C).Thedispositionofapentamerousandroecium phological and developmental studies have shown (Corry,
and dimerous gynoecium ismost common in Gentianales (and 1884; Demeter, 1922; Kunze, 1981, 1990, 1991, 1994, 1995,
inearlybranchingApocynaceae),andthusismostprobablyan- 2005;Demarco,2014).
cestralinthefamilyandwaspresentintheevolutionaryhistory A pinnacle of complexity is exhibited by the flowers of
beforethesynorganizationofandroeciumandgynoecium. Ceropegia, a genus of over 200 species (Huber, 1957; Vogel,
Among asclepiads, diversity isexpressed inparticular inthe 1961; The Plant List, http://www.theplantlist.org/; Figs 9 and
shape of the corolla and corona. The corona is highly plastic 10).Here,notonlyarethecorona,androeciumandgynoecium
Endress—Developmentandevolutionofextremesynorganizationinflowers 755
A B
D
o
w
n
lo
a
d
e
d
FIG. 6. Style head moulding from disymmetry to pentasymmetry in two developmental stages, from above, in Gomphocarpus fruticosus (Apocynaceae- from
Asclepiadoideae),scanningelectronmicrographs(modifiedfromEndress,2006).(A)Veryyoungstage,withthetwocarpelsstilldistinct.(B)Olderstage,withthe h
twocarpelspostgenitallyunitedandoutlinechangedtofive-angled.Scalebars:A¼50mm,B¼500mm. ttp
s
://a
c
a
d
e
A B m
ic
c .ou
p
.c
o
m
/a
o
p b/a
rtic
le
c -a
b
s
p trac
t/1
1
7
/5
/7
4
9
/1
FIG.7.FlowersofApocynaceae-Asclepiadoideaetoshowdiversityinproportionsofpetals(p)andcorona(c).(A)Vincetoxicumnigrum,withrelativelysmalland 74
simplecorona.(B)Asclepiascurassavica,withrelativelylargeandcomplexcorona. 0
0
0
2
b
y
g
u
e
s
t o
n
0
3
A
p
ril 2
0
1
9
A B
FIG.8.Diversityinextensionoftheedgesofthestylehead(markedwithred),depthoftheguiderails(markedwithyellow,togetherwithuppermostpartofthesta-
mens)andexpositionofthepollinaria(markedwithpink),correlatedwithpollinatorsize,inApocynaceae-Asclepiadoideae.(A)Gomphocarpusfruticosus(style
headedgesnotextended,guiderailsdeep,pollinariahidden–forlargepollinators).(B)Carallumapenicillata(styleheadedgeslongextended,guiderailsshallow,
pollinariaexposed–forsmallpollinators).Scalebars:both¼500mm.
756 Endress—Developmentandevolutionofextremesynorganizationinflowers
A B
D
o
w
n
FIG. 9. Flowers with extremely complex corolla. (A) Ceropegia distincta (Apocynaceae-Asclepiadoideae). (B) Coryanthes macrantha (Orchidaceae- loa
Epidendroideae). de
d
fro
m
intimately synorganized, but also the corolla is involved in the and non-receptive zones in some groups (e.g. Condylocarpon, h
complexityina unique way. Theflowersare trap flowerswith Aspidosperma, M. E. Endress, pers. comm.). An incipient co- ttps
alongandslendertubeformedbycongenitalfusionofthepet- ronamaybepresentasalternipetalouslobesonthecorolla(cor- ://a
c
als. The complex pollination apparatus is small and hidden in ollinecorona)asalsointhesisterfamilyGentianaceae;insome a
d
e
thebaseofthecorollatube.Thus,notonlyarepartsofthean- genera of Rauvolfioideae these corona lobes are conspicuous. m
droecium and gynoecium hidden, but the entire pollinationap- Thecorollaissympetalous,andthestamensarefusedwiththe ic.o
paratus.Intheuppermostzoneofthecorollathepetalsarefree corollaandhavetwopollensacspertheca.However,theflow- up
butarepostgenitallyfusedinbud.Atanthesisthispostgenitally ersarealreadyrevolverflowers,asalsoinsomeotherpolysym- .co
m
fused zone opens differentially. In the most complex species, metricasterids. /a
suchasC.distincta,atthebaseitopenstoprovidefiveseparate There are trends in the evolutionary pathway of the pollinia ob
eznotnrea.ncTehseinntfooltlhoewcsoraolzloanteubwe,heearechthweitpheatawlsarxe-mcoavinerefudsgeldidainngd aRnaduvoplfoiolliidneaarieaandanAdpocoyfnoisdtyealee,phoellaednisdnioffremreanlltyiadtiiosnp.erseIdn /article
formakindofcentralstalk.Abovethis,asecondzoneofopen- as single grains, but in both subfamilies there are some taxa -a
b
ingpresentsaflagwiththeinnerpetalsurfacesturnedoutward with tetrads. The proboscis of pollinating insects becomes stra
and acting as an osmophore to attract flies (Ollerton et al., sticky by touching the style head and takes up pollen, which c
2009).Thetipsofthepetalsremainclosed,formingafirmtop may be deposited on the stigmas of recipient flowers. Schick t/11
7
of the flag. Some species have flickering hairs directed out- (1982a) distinguished two types and Fallen (1986) found four /5
wardsatanthesisintheopeningzones,whichaddtotheattrac- levels of increasing complexity of the style head in /74
9
tivityforflies.Thus,thecorollaexhibitsfivezoneswithregard Apocynaceae s.s.: (1) the entire style head is secretory and /1
7
to differential fusion, from base to top: (1) congenitally fused, (probably) stigmatic in its entirety; (2) the stigma is restricted 4
0
(2)open,(3)postgenitallyfused,(4)openand(5)postgenitally to the lowermost part of the style head below a downward di- 0
0
2
fused(Fig.10). rected collar, which collects incoming pollen, whereas the up- b
y
per part of the style head secretes the adhesive for pollen g
u
transport, and an upper ring of hairs presents the pollen shed e
s
from the anthers; (3) in addition, the anthers are postgenitally t o
Stepwisesynorganizationoftheflowersinthephylogenyand n
fused with the style head, and thus the gynostegium emerged 0
evolutionofApocynaceaesensulato(s.l.) 3
(occursonlyinApocynoideae);(4)thedownwarddirectedcol- A
stuTdhieedpinhythloegpeansyt2o0f yAeparosc,yannadcefaoer sso.ml.ehsausbcbleaednesinatsepnescitvseolyf laarreapnrdesethnet ounpptehrervinengtroaflhsiadiersodfisthapepaenatrheedrsa,nwdh,iicnhstsecarda,pheaiinrs- pril 2
0
1
floralevolutionhavebeenanalysed(Nilssonetal.,1993;M.E. comingpollenfromtheproboscisofinsects.Themostinterest- 9
Endress et al., 1996, 2007a, b, 2014; Sennblad and Bremer, ing innovation in Apocynoideae, found in Apocynum and
1996,2002;Civeyreletal.,1998;Sennbladetal.,1998;M.E. Forsteronia, is a precursor of a translator. It consists of five
Endress and Bruyns, 2000; M. E. Endress, 2003, 2004; M. E. small platelets of a gummy consistency secreted between the
Endress and Stevens, 2001; Rapini et al., 2003, 2006, 2007; anthers on the style head, which take up pollen from the adja-
Verhoeven et al., 2003; Simo˜es et al., 2004, 2007b, 2010; centthecaeoftwoanthersandareremovedandtransportedby
Liede-Schumann et al., 2005; Ionta and Judd, 2007; Livshultz pollinators(Demeter,1922;Nilssonetal.,1993;M.E.Endress,
et al., 2007; Livshultz, 2010; Rapini,2012; Nazar et al., 2013; 2003); pollen still occurs as single grains (as tetrads in
M.E.Endressetal.,2014;Straubetal.,2014).Inthebasalsub- Apocynum), and the translator is without attachment device to
cladesofApocynaceae(gradeofRauvolfioideae),thedegreeof pollinators,exceptforstickysecretion.
floralsynorganizationisrelativelylow.Therearenopollinaria, In Periplocoideae, the translator is spoon-shaped. Pollen is
nopolliniaandnogynostegium.Theverytopofthegynoecium transported inthe formof free tetrads or tetrads packed in soft
is commonly not secretory, but the secretory part somewhat pollinia (without pollinium wall) (Verhoeven and Venter,
lower down is without functional differentiation into receptive 2001),andisdepositedinthestickyconcavepartofthespoon.
Endress—Developmentandevolutionofextremesynorganizationinflowers 757
Floral bud Open flower
Unfused
Postgenitally
fused
D
Congenitally o
w
fused n
lo
a
d
e
d
fro
m
h
ttp
s
://a
c
a
d
e
m
ic
FIG.10.LongitudinaldifferentiationofcorollaanddifferentialopeningofzoneofpostgenitalfusionofpetalsatanthesisinCeropegiadistincta(Apocynaceae- .o
Asclepiadoideae).Left:floralbud.Corollacongenitallyfusedinthelowerhalf,postgenitallyfusedintheupperhalf.Right:openflower.Corollawithfivezones up
frombasetotop:(1)congenitallyfused(floraltube),(2)open(fiveentranceswithglidingzonesforpollinators),(3)postgenitallyfused(stalkofflag),(4)open .c
o
(osmophoricflag),(5)postgenitallyfused(upperendofflag). m
/a
o
b
/a
The other end of the spoon, the ‘handle’, has a sticky pad un- morphologicallyand functionallywiththe androecium.A nov- rticle
derneath, which is attached to pollinators (Demeter, 1922; M. eltyhereisthatcoronaelementsalsodevelopinalternistaminal -a
b
E. Endress, 2003). It has been assumed that pollinia evolved position. All elements together may form a complex nectar stra
twice in Periplocoideae (Verhoeven and Venter, 2001) or at holder (and a holding device for nectar-seeking pollinators) of c
leastthreeorfourtimes(IontaandJudd,2007). these revolver flowers (Liede and Kunze, 1993; Asclepias, t/11
7
InSecamonoideaeandAsclepiadoideaethepollinariaareat- Galil and Zeroni, 1965; Hoya, Kunze and Wanntorp, 2008). /5
tachedtopollinatorswithaclip.InSecamonoideaae,thetrans- Theconsistencyofthecoronaisthenconspicuouslyfirm.This /74
9
lator consists only of this clip, and pollen is in tetrads within is also true for the corolla in many Asclepiadoideae (Fig. 2A). /1
7
the soft pollinia (without pollinium wall). In Asclepiadoideae Associatedwithsuchfirmconsistencyisalsoadiversityofsur- 4
0
the translator has, in addition, two arms, and the pollinia are face sculptures of corolla and corona (Ehler, 1975; Bruyns 00
2
hard,havingapolliniumwall,andpollenisnolongerinrecog- et al., 2005). If the staminal corona is large and the five units b
y
nizable tetrads within the pollinium (Verhoeven and Venter, arebulging,asinAsclepias,each oftheseconvex,smooth and g
u
2001).WithinAsclepiadoideae,onlyFockeastillhastetradsin slipperyunitsleadsapollinatorlegexactlytowardsaguiderail e
s
the pollinia, which are soft and lack a pollinium wall (Fig.7B). t o
n
(VerhoevenandVenter,2001). 0
3
AnotherimportantinnovationinAsclepiadoideaeisareorga- A
nstiezaadtiotnheofntohweasnttehreilres.aTnhtehedrorfslaanlkpsolfleonrmsacthsedirsiagpipdea(lri,gannifdieidn-) FlowersofthemostelaborateOrchidaceae pril 2
0
1
guide rails that direct pollinator body parts precisely into the AsinApocynaceaes.l.,animpressiveincreaseinsynorgani- 9
clip of the translators (Kunze, 1996). In addition to this en- zation can be observed following evolutionary trends through
hanced precision, the diversity of the depth of the guide rails the family Orchidaceae. I will also begin with the most ex-
addstoenhancedpollinatorspecificity(Fig.8).Anotherconse- tremely synorganized clade, which constitutes the largest sub-
quence is that each pollinarium here consists of only two pol- family Epidendroideae (with 20000 species; Chase et al.,
linia (in contrast to the four pollinia from the ancestral two 2015) and then show aspects of the evolution of this complex-
pollensacsperthecainSecamonoideae;Safwat,1962). ity. As in the derived subfamilies of Apocynaceae, in
Thecoronaisancestrallycorolline,andthusdevelopsonthe Epidendroideae the number of floral organs is also completely
corolla in alternipetalous positions (Fishbein, 2001; Kunze, fixed, always with 3þ3 perianth organs, 1 stamen and 3 car-
2005). This is not only the case in Apocynaceae but also in pels. The same is true in Orchidoideae and Vanilloideae.
other Gentianales (Gentianaceae). In addition, there isa stami- Orchidaceae witha singlestamen areoften called monandrous
nal corona in some Periplocoideae and in Secamonoideae and orchids(buttheydonotformaclade).Inthetwosmallestsub-
Asclepiadoideae(Rudjiman,1982;Kunze,2005).Thisalsode- familiesstamennumberishigher:2–3inApostasioideaeand2
velops in alternipetalous position but is closely associated in Cypripedioideae. In many of the derived Orchidaceae
758 Endress—Developmentandevolutionofextremesynorganizationinflowers
A B C
to
to
I
I
ti ti ti ti
to
to
FIG.11.CongenitalfusionofallorgansinveryyoungflowersofOncidiumornithorhynchum(Orchidaceae-Epidendroideae),scanningelectronmicrographs,flowers
notresupinated,andthusliplocatedinupperpart(modifiedfromEndress1994).(A)Allsixperianthorganscongenitallyfused,formingaringwall,individualor-
gansnotyetvisible.(B)Individualperianthorgansvisible:outertepals(to),innertepals(ti),lip(l).(C)Moreadvancedstage,withlateraloutertepalsremoved, D
o
gynostemiumhiddenbymedianoutertepalandlip;abbreviationsasin(B).Scalebars:all¼50mm. w
n
lo
a
d
e
d
(dOevrcehloidpomideenataellaynedarElypidfoernmdreodidlaetaeer)alwoiuthtgaroswinthgsleosftathmeegny,ntowso- pfooullrinpaorliluinmia.,Poonlelepneropfoltlheenasancth.eInr misabnaysgicraolulypsotrhgeatnwizoedpoilnletno from
temium are interpreted as staminodia; they may canalize the massesofthetwopollensacsinathecaformasinglepollinium h
movements of the pollinators (Burns-Balogh and Bernhardt, so that the pollinarium has only two pollinia (Rasmussen, ttps
1985; Kurzweil and Kocyan, 2002). However, lateral append- 1986a), comparable to Asclepiadoideae (but where dimery re- ://a
c
agesinsomeOrchidoideaemaynotberemnantsofstaminodia sults from transformation of the dorsal pollen sacs into sterile a
d
e
but late elaborations of the fertile stamen (reviewed by but mechanically reinforced parts). The stamen is in the sym- m
Kurzweiland Kocyan,2002).Incontrast to the polysymmetric metryplaneoftheflowerandoneofthethreecarpelsisalsoin ic.o
Apocynaceae, the flowers of Orchidaceae are monosymmetric. the symmetry plane and is adjacent to the stamen. The tip of up
Thesinglestamenisinthesinglesymmetryplane(Fig.2B,D). thiscarpelisdifferentiatedintoaproximalstigmaticzoneanda .co
m
AllOrchidaceaehaveaninferiorovary. terminal secretory zone (viscidium) that comes into contact /a
The organs (tepals) of the two perianth whorls are congeni- withthepollinia,andthesecretedmaterialactsasagluetoat- ob
tTahlleythfureseedc,aarptellesasatreatcothnegebnaitsael,lyanfudseadlsoupbteotwtheeentotph.eAwlshoorthlse. tSacchhiltlh,e20p0o0ll)i.naTrhiuemjotiontabpeotwllieneantotrhe(Ypeoulnlign,ia19(c8o7ma;inPgruftrsocmhatnhde /article
single stamen is congenitally fused with the gynoecium up to androecium) and the viscidium (coming from the gynoecium) -a
b
the top, androecium and gynoecium together forming a gynos- is a piece of disintegrated tissue from the anther (elastoviscin) stra
temium (also called column). Note the difference between withelasticproperties(Dressler,1986;SchillandWolter,1986; c
Orchidaceae and Apocynaceae: gynostemium (congenitally Wolter and Schill, 1986) in most Orchidaceae. However, in t/11
7
fused) vs. gynostegium (postgenitally fused). The perianth or- Cymbidieae and Vandeae of Epidendroideae, this joint is a /5
ganontheoppositesideoftheflowertothestamen,thelip,is pieceoftissuefromtheshorttipofthemediancarpel.Thiscar- /74
9
commonly more elaborate and larger than the other five. It is peltipiscalledarostellum.Dependingonthesiteoforiginthe /1
7
partoftheinnerperianthwhorl.Itmainlyfunctionsasalanding joint is called a caudicle (caudicula) (if from the androecium) 4
0
platformforpollinators.InallOrchidaceaeearlyfloraldevelop- orastipe(stipes)(iffromthegynoecium);thereareevenaddi- 0
0
2
ment is remarkably similar. The flowers are pronouncedly tional terms used in the literature (Rasmussen, 1982, 1985, b
y
monosymmetricfromthebeginning,andallsixtepalsoriginate 1986a,b).Pollinariawithastipealsohaveashortportionofa g
u
as a conspicuous medianly compressed ring wall, without dis- caudicle adjacent to the pollinia. Thus, there is a combination e
s
tinction of the single organs, and thus they apear congenitally of caudicle and stipe, whereby the largest part of the joint is t o
n
fusedbeforetheirtipsbecomevisible(Bletia,Kurzweil,1987a, madeupbythestipe.Thejointfunctionallycorrespondstothe 0
3
fig. 2C; Malaxis, Kurzweil, 1987a, fig. 4A, B; Dactylorrhiza, armsofthetranslatorinApocynaceae.Conspicuousdiversityis A
K4Aur,zwBe;ilL,i1st9e8r7ab,,Kfiugr.z1wAei–lC, ;1P98re8s,cofitgti.a,6KAu;rzPwherial,gm19ip8e8d,iufimg,. athlseogeyxnhoisbtietmediubmy,thwehpicrhopaoidrtiionnsatatancdhidnigrecptoiollninsaorifactuorvdaitfuferereonft pril 2
0
1
Kurzweil, 1993, fig. 4B, C; Oncidium, Endress, 1994, fig. body parts of different pollinators (Vogel, 1959; Garay, 1972; 9
8.67.1–3;thisstudy,Fig.11;Satyrium,Kurzweil,1996,fig.3a; Rasmussen, 1982, 1986a, b; Burns-Balogh and Bernhardt,
Pholidota, Kurzweil, 1998, fig. 6A; Hemipilia, Luo and Chen, 1985; Manning and Linder, 1992). Dressler (1981) mentioned
2000,fig.1B,C;Amitostigma,LuoandChen,2000,fig.3B,C; 13areasforpollinariumattachmentineuglossinebees.
Gymnadenia, Luo and Chen, 2000, fig. 5B, C; Platanthera, Becauseoftheiroftenfirmstructure,theperianthorgans,es-
Luo and Chen, 2000, fig. 5S, T; Telipogon, Pabo´n-Mora and pecially the lip (labellum), are extremely plastic in shape and
Gonza´lez,2008,figs2D,4D–F,5B,E).OnlyinApostasioideae diverseindetailsofsurfacedifferentiations(holdingstructures,
is this early fusion less pronounced, but also present (Kocyan secretorystructures,three-dimensionalsurfacesculpturesofop-
andEndress,2001,figs2B,C,H,I,N,O,11B,G,L).Floralde- tical significance) (e.g. Davies et al., 2002; Davies and
velopment of orchids has been reviewed by Kurzweil (1998) Stipczynska, 2006; Bradshaw et al., 2010). The firm structure
andKurzweilandKocyan(2002). also allows the differentiation of a spur (another means of di-
The complete congenital fusion between the stamen and the versification is by spur diversity, e.g. Kurzweil and Weber,
gynoecium ensures the immediate proximity of the androecial 1992; Micheneau et al., 2009).Rarely, two collateral spursare
and gynoecial parts that contribute to the formation of the present(Satyrium,Satyridium,Vogel,1959;Kurzweil,1996)or