Palynotaxonomy of the genus Gladiopappus (Dicomeae, Asteraceae) with special emphasis on the exine ultrastructure and mesoapertures
Abstract
The pollen morphology of Gladiopappus vernonioides was studied with transmission (TEM) and scanning (SEM) electron microscopy and with light microscopy (LM). An Anthemoid pattern of exine ultrastructure was found. The pollen morphology of Gladiopappus supports the inclusion of this genus in the tribe Dicomeae and subtribe Dicominae but not in the Mutisieae s.str. The apertural system of G. vernonioides includes a mesoaperture that intersects the foot layer and the upper layer of the endexine, a condition already pointed out for several tribes of Asteroideae (Helenieae, Gnaphaliinae, Heliantheae, Inuleae, Senecioneae) and Carduoideae (Cardueae, Dicomeae). It is suggested that the existence of an intermediate aperture could characterize the apertural system of the Asteraceae as a synapomorphy
Full text
© 2018 Naturalis Biodiversity Center You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: Youmustattributetheworkinthemannerspecifiedbytheauthororlicensor(butnotinanywaythatsuggeststhattheyendorseyouoryouruseofthework). Non-commercial: Youmaynotusethisworkforcommercialpurposes. Noderivativeworks: Youmaynotalter,transform,orbuilduponthiswork. Foranyreuseordistribution,youmustmakecleartoothersthelicensetermsofthiswork,whichcanbefoundathttp://creativecommons.org/licenses/by-nc-nd/3.0/legalcode.Anyoftheaboveconditionscanbe waivedifyougetpermissionfromthecopyrightholder.Nothinginthislicenseimpairsorrestrictstheauthor’smoralrights. Blumea63,2018:102–108 ISSN(Online)2212-1676 www.ingentaconnect.com/content/nhn/blumea https://doi.org/10.3767/blumea.2018.63.02.02 RESEARCH ARTICLE INTRODUCTION In1947,whentravellinginthesouthofMadagascar,theFrench botanist Jean-Henri Humbert discovered a new endemic species and genus of AsteraceaeatthecapeSainteMarie,onthe edgeofalimestoneplateau.Inthefollowingyearhedescribed Gladiopappus anditsonlyspecies(G. vernonioidesHumb.), and included it in the Mutisieae s.lat. (Humbert1948).Thistribe, in its classic concept, was described, for the first time, by Cassini (1817)andlateracceptedbythegeneralityofbotanists(e.g., Bentham1873,Hoffmann1894).Oneofthemostimportant wasCabrera(1951,1965,1971,1977),whopublishedseveral of the most relevant works related to the tribe taxonomy. The Mutisieae s.lat. werelaterconsideredbymanyauthors(e.g., Bremer1987,Panero&Funk2002,Katinasetal.2009,Tiangangetal.2011)asanartificialgroupwhichtheydividedin severaltribes.OneofthesetaxawastheDicomeae, a small tribethatPanero&Funk(2002)proposedforthefirsttime.Althoughseveralbotanists(e.g.,Hind2007)followedHumbert’s (1948)taxonomictreatmentandconsideredGladiopappus as belonging to the Mutisieae,Ortizetal.(2009)includedit in the Dicomeae. OtherauthorsacceptedtheinclusionofGladiopappus in this tribe (e.g.,Ortizetal.2013),sometimesstressing that they did so onaprovisionalbasis(e.g.,TreeofLifeWeb Project2009).Therefore,thetribalpositionofthegenusisstill controversial. Manyauthorshavestudiedthepollenmorphologyofthe Mutisieaes.lat.withlightmicroscopy(LM)(e.g.,Wodehouse 1929a,b,Stix1960,Dimon1971,Parra&Marticorena1972, Pastana1989)orscanningelectronmicroscopy(SEM)(with orwithoutLM,asdidHansen1990,Linetal.2005,Zhaoet al.2006,Tellería&Katinas2004,2009andWortleyetal. 2012).Skvarla&Turner(1966),Southworth(1966)andTellería&Katinas(2009)investigated,withtransmissionelectron microscopy(TEM),theexineultrastructureof,respectively Mutisia campanulata, Gerbera jamesonii and Mutisia spinosa, three taxa that belong to the Mutisieae s.str. Although Skvarla etal.(1977)employedTEMtostudytheexineultrastructure of four genera belonging to the Mutisieaes.lat.(Dasyphyllum, Doniophyton, Glossarion and Schlechtendalia),furtherstudies(e.g.,Katinasetal.2009)haveshownthatnoneofthese taxacorrespondtothemodernconceptofthetribe.Infact, Dasyphyllum, Doniophyton and Schlechtendalia belong to the Barnadesieae (Barnadesioideae),andevenGlossarion, a genusthatCabrera(1977)andKatinasetal.(2008)includedin the Mutisiinae was not considered as belonging to the modern Mutisieae(Katinasetal.2009). Fortheirpart,Ortiz&Pereira Coutinho(2001)andPereiraCoutinhoetal.(2012)studied,with LM,SEM,and,intwocases(Erythrocephalum and Pleiotaxis), alsowithTEM,thepalynologyofsevengeneraofDicomeae (Cloiselia, Dicoma, Dicomopsis, Erythrocephalum, Macledium, Pasaccardoa and Pleiotaxis). Zhaoetal.(2006)publishedtheonlyobservationsonthepollen morphology of G. vernonioides.TheyemployedLMand SEM–butnotTEM–tostudytheexineofG. vernoni oides, basing their descriptions on the pollen grains of a single specimen(Humbert 20326,isotype)intheKewHerbarium. Onlyfivemeasurementsoftheexinecharactersweretaken, andthestudylackedastatisticalanalysisofthedata.Forthese reasons,weconsiderZhaoetal.’s(2006)pollendescription of G. vernonioidesasincomplete.Inaddition,consideringthe uncertainties in the taxonomic placement of the taxon and the well-known importance of pollen morphology for the taxonomy and ecology of the Asteraceae(e.g.,Wodehouse1935,Wagenitz1976,Skvarlaetal.1977,Bolick1978,Blackmore1982, Wangetal.2009,Blackmoreetal.2010,Wortleyetal.2012, Telleríaetal.2013),wehavedecidedtostudytheexineofthat raregenusingreaterdetail(TEM,SEMandLM). Palynotaxonomy of the genus Gladiopappus (Dicomeae, Asteraceae) with special emphasis on the exine ultrastructure and mesoapertures A.PereiraCoutinho1,D.SádaBandeira2,L.Currais1,E.Soukiazes2,S.Ortiz3 1 CentreforFunctionalEcology(CFE),DepartmentofLifeSciences,Faculty ofSciencesandTechnology,UniversityofCoimbra,CalçadaMartimde Freitass/n,3000-456Coimbra,Portugal; correspondingauthore-mail:[email protected]. 2DepartmentofLifeSciences,FacultyofSciencesandTechnology,UniversityofCoimbra,Coimbra,Portugal. 3FacultyofPharmacy,UniversityofSantiagodeCompostela,PrazaSeminariodeEstudosGalegos,s/n,Campussur,15782SantiagodeCompostela,Galicia,Spain. Key words Dicomeae exine LM Mutisieae pollen SEM TEM AbstractThepollenmorphologyofGladiopappus vernonioides wasstudiedwithtransmission(TEM)andscanning(SEM)electronmicroscopyandwithlightmicroscopy(LM).AnAnthemoidpatternofexineultrastructurewas found.ThepollenmorphologyofGladiopappus supports the inclusion of this genus in the tribe Dicomeae and subtribe Dicominae but not in the Mutisieae s.str. TheaperturalsystemofG. vernonioides includes a mesoaperture that intersects the foot layer and the upper layer of the endexine, a condition already pointed out for several tribes of Asteroideae (Helenieae, Gnaphaliinae, Heliantheae, Inuleae, Senecioneae)andCarduoideae (Cardueae, Dicomeae).Itissuggestedthattheexistenceofanintermediateaperturecouldcharacterizetheaperturalsystem of the Asteraceaeasasynapomorphy. Published on13July2018
103 A.PereiraCoutinhoetal.:PalynotaxonomyofGladiopappus A general point to be also considered is the question of the presenceofmesoapertures,i.e.,‘themiddlepartofacompound aperture in which there is also an ectoaperture and an endoaperture’(Puntetal.2007).Thisisarareconditioninthe angiosperms.ItoccursinthePolygonaceae (Puntetal.2007), some Boraginaceae (Saad-Limametal.2002)andthegreat majorityoftheAsteraceae.Aconsiderablenumberofauthors discussed the questions of the presence of mesoapertures (seeTable1)andwhichexinelayersitinvolved(seeTable2) in the apertural system of the Asteraceae.Itisworthnoting that the structure was recorded in all the main subfamilies (Helianthoideae, Carduoideae, Cichorioideae, Mutisioideae). Ourmainobjectivesweretocharacterizethepollenmorphology of Gladiopappusandtoclarifyitstribalposition.Wealsointended to provide some data about the existence and structural morphology of a mesoaperture in its pollen apertural system and to help to clarify its taxonomic significance for the Asteraceae. MATERIALS AND METHODS Specimens seen Gladiopappus vernonioidesHumb. Madagascar,CapSainteMarie,11July1948,Jean de Dieu 1428-RN(P);FalaiseterminaleduCapSainteMarie,23Sept. 1958,M.G. Cours s.n. (P). General treatment ThepollengrainsoftwospecimensbelongingtotheHerbarium oftheMuséumNationald’HistoireNaturelle,Paris(seeabove) werecollectedandacetolyzedaccordingtoErdtman(1960). Theterminologyforexinedescriptionsfollowed,ingeneral, Puntetal.(2007)and,forsomedetailsoftheexinestructure (columellaenomenclature),Blackmoreetal.(2009). LM Thepollenmaterialwasincludedinsiliconeoil(Andersen 1960)andthenobservedandphotographedwithaMoticBA 310lightmicroscopeequippedwithadigitalcamera.Thirty measurements of the following characters were taken: polar axis(P),equatorialdiameter(E),exinethicknessinthepolar areas, ectoaperture length, mesoaperture length and width, Subfamilies Mesoapertures Authors Barnadesioideae Notreferred Urtubey&Tellería(1998),Stuessyetal.(2009) Famatinanthoideae Yes Freireetal.(2014) Mutisioideae Yes Tellería&Katinas(2009),Freireetal.(2014) Stifftioideae Yes Tellería&Katinas(2004) Wunderlichioideae Notreferred Zhaoetal.(2006),Tellería(2007) Gochnatioideae Yes Telleríaetal.(2013) Hecastocleidoideae No Tellería&Katinas(2005) Carduoideae Yes Leonardisetal.(1983),Tormo-Molina&Ubera-Jiménez(1990,1995), Duistermaat(1996),Wortleyetal.(2008),PereiraCoutinhoetal.(2012) Pertyoideae Notreferred Tellería&Katinas(2005),Katinasetal.(2008) Gymnarrhenoideae Notreferred Zhaoetal.(2006) Cichorioideae Yes ElGhazaly(1980),Blackmore(1982),Wangetal.(2009) Corymbioideae Notreferred Wortleyetal.(2007) Asteroideae Yes Dimon(1971),PereiraCoutinho(2002),PereiraCoutinho&Paiva(2003), Jaramillo&Trigo(2006),PereiraCoutinho&Dinis(2007,2009),Osman(2011), Montes&Murray(2014),PereiraCoutinhoetal.(2014,2016) Table 1 PalynologicalstudiesonthesubfamiliesoftheAsteraceaeandthepresenceofmesoapertures. Subfamily Tribe Exinelayers Microscopies Authors Mutisioideae Mutisieae Innerlayerofthesexine+outerlayerofthenexine LM,SEM Tellería&Katinas(2009) Carduoideae Athroismeae Footlayer+outerlayeroftheendexine TEM PereiraCoutinhoetal.(2012) Cynareae Footlayer+outerlayeroftheendexine SEM,TEM Tormo-Molina&Ubera-Jiménez(1990,1995) Tectum LM Leonardisetal.(1983) Cichorioideae Arctoteae Footlayer LM Dimon(1971) Cichorieae Outerlayeroftheendexine LM,SEM ElGhazaly(1980) Footlayer SEM,TEM Blackmore(1982) Vernonieae Footlayer LM Dimon(1971) Asteroideae Anthemideae Footlayer LM Dimon(1971) Gnaphalieae Footlayer LM Dimon(1971) Footlayer+outerlayeroftheendexine TEM PereiraCoutinho&Dinis(2009) Helenieae Footlayer+outerlayeroftheendexine TEM PereiraCoutinho(2002) Heliantheae Footlayer LM Dimon(1971) Footlayer+outerlayeroftheendexine TEM PereiraCoutinho(2002),PereiraCoutinhoetal.(2016) Inuleae Footlayer LM Dimon(1971) Footlayer+outerlayeroftheendexine TEM PereiraCoutinho&Dinis(2007) Eupatorieae Footlayer LM Dimon(1971) Millerieae Footlayer+outerlayeroftheendexine TEM PereiraCoutinho(2002),PereiraCoutinho&Paiva(2003) Senecioneae Footlayer+outerlayeroftheendexine TEM Montes&Murray(2014) Table 2 Exinelayersinvolvedinthemesoapertures.
104 Blumea–Volume63/2,2018 endoaperturewidth,spineslengthandbasalwidth.Theratios P/Eandspinelength/basalwidthwerethencalculated. SEM After dehydration in an increasing ethanol gradient, the pollen grains were mounted on aluminium stubs, covered with goldpalladiumwithanionsputtercoaterJEOLJFC-1100(1200V, 6mA,10minutes)andobservedwithaHitachiSU-70scanning electronmicroscopeoperatingat4kV.Twentymeasurements of the diameter of the spine and inter-spines perforations were taken. TEM Thepollengrainswerefixedwithosmiumtetroxide2%in 0.1Msodiumcacodylatebuffer(pH7.2,24h),dehydratedin anincreasingethanolgradient(70–100%)andembeddedin Spurr’sresin.Ultra-thinsectionsweremadewithaLeicaEM UC6EMFC6ultramicrotomefittedwithadiamondknife,and contrastedwithuranylacetateandleadcitrate.Thentheywere observedwithaFEI-TecnaiG2SpiritBiotwintransmission electronmicroscopeoperatingat100kV.Twentymeasurements of the following characters were taken: tectum, internal tecta,footlayerandendexinethickness(thesetwocharacters innon-aperturalareas);inter-spinesmiddleandoutercolumellaewidth. Statistics Themaximumandminimumvalues,arithmeticmeanand standarddeviationarereportedforallobservedmeasures. RESULTS Pollen grains description Polleninmonads,isopolar(Fig.1a,b),withradiatesymmetry, 3-zono-colporate,ellipticinmeridianopticalsection(Fig.1a, b),subcircularinequatorialopticalsection,oblate-spheroidal tosubprolate,P/E=0.96–1.31(1.10±0.09).P=32.50– 49.20(40.70±4.08)μm,E=32.50–40.80(37.00±1.97) μm.Ectoapertures:colpi,acuteattheends(Fig.1c,d,2a), 23.00–28.00(25.20±2.16))μmlong;mesoapertureslalongate,elliptic(Fig.1c,d),length=4.50–12.40(8.60±2.74)μm, width=6.80–18.60(9.73±3.02)μm;endoapertureslalongate, constrictedatthecentre,moreorlessacuteattheends(Fig. 1c,d),width=13.30–20.00(16.20±1.81)μm;costaepresent. ExinewithanAnthemoidpattern,i.e.,acaveate(Fig.1a,b,2c, e,3a–f),withoutinternalforamina(Fig.3a–f),withalarge series of supporting columellae bearing shorter levels of outer columellaethatalternatewithinternaltecta;exine5.00–9.20 (7.25±1.20)μmthickatthepoles;tectumperforate(Fig. 2a–e,3a–f),0.16–0.27(0.21±0.03)μmthick;outerinternal tectum0.08–0.20(0.14±0.03)μmthick,perforate(Fig.3c–f); innerinternaltectum0.29–1.00(0.70±0.19)μmthick,withan interlacedmorphology(Fig.2c–e,3a–f);inter-spinessupporting columellae longer and thicker than the inter-spines middle andouterlayerscolumellae(Fig.3a–f),frequentlydistally ramified(Fig.2c–e,3b–e);inter-spinesmiddlelayercolumellae0.14–0.29(0.23±0.05)μmthick,inter-spinesouterlayer columellae0.07–0.23(0.13±0.05)μmthick;footlayerthicker thantheendexine(Fig.2c,3a–f)exceptattheaperturalareas (Fig.3a,b).Sculptureechinate,spinesacutetoobtuse(Fig.1a, b,2a–e),2.10–4.20(3.10±0.52)μmlong,4.20–6.70(5.36± 0.68)μmwideatthebase,spinelength/basalwidth=0.42– 0.71(0.58±0.08),spinessupportingcolumellaelongerthan Fig. 1LMmicrographs.a,b.Obliqueviewofameridionalopticalsection;c,d.meridionalsuperficialviewofanaperture.—ea–endoaperture;ec–ectoaperture;ma–mesoaperture;ne–nexine;sc–supportingcolumellae;se–sexine;sp–spines.—Scalebars:10µm. c b d a ne se sp sc ec ec ea ea ma ma
105 A.PereiraCoutinhoetal.:PalynotaxonomyofGladiopappus Fig. 2SEMmicrographs.a.Meridionalview,showinganaperture;b.detailofthesameview;c–e.detailsoffracturedexines.—ea–endoaperture;ec –ectoaperture;en–endexine;fl–footlayer;iit–innerinternaltectum;ma–mesoaperture;oc–outercolumellae;sc–supportingcolumellae;spf-spine perforations.—Scalebars:5µm. theinter-spinessupportingcolumellae(Fig.3b–d,f),reaching 1/3–1/2ofthespinelength(Fig.3b–d,f);perforationsreaching 1/3–1/2ofthespinelength(Fig.2a–e),increasingindimensionstotheapex(Fig.2a–e),diameter=0.09–0.57(0.29± 0.14)μm;inter-spinessculpturescabrate-perforate(Fig.2a, b,d,e),perforationsdiameter=0.05–0.19(0.11±0.04)μm. DISCUSSION Palynotaxonomy Ourresultsagree,ingeneral,withZhaoetal.(2006).Nevertheless,thevaluesofP/Ewefoundindicatethattheshapeof the pollen grains of Gladiopappus is more variable than they reported.They are oblate-spheroidal to prolate, and not simply prolateasZhaoetal.(2006)indicated.Theseauthorspostulated,butcouldnotprove,theexistenceof‘possiblymorethan onecolumellaelayeraboveproximal(basal)columellae’.The useofTEMallowedustosecurelyobservetwolevelsofcolumellaeandtwointernaltectaabovethesupportingcolumellae. ItmustbestressedthatSkvarlaetal.(1977)suspectedthat the quantification of columellae levels and internal tecta could beusefulfromataxonomicperspective. ThepollensculptureoftheMutisieaes.str.isgenerallymicroechinateormicrogranulate(Katinasetal.2009),macrogranulate(Linetal.2005),or,morerarely(asinsomespeciesof Mutisia),microechinate-rugulateorrugulate(Tellería&Katinas 2009).Parra&Marticorena(1972)pointedoutheightsof 0.5–1.5(1.8)μmfortheexineof61taxaofthefivegenera (Brachyclados, Chaetanthera, Chaptalia, Mutisia, Trichocline)of Mutisieae s.str.theystudied.Conversely,theDicomeae present a clearly echinate sculpture, with a spine average length of about3μmandreachingamaximumof8μm(Ortiz&Pereira Coutinho2001,Zhaoetal.2006,PereiraCoutinhoetal.2012). ThisisalsoafeatureofthepollengrainsofGladio pappus (see Results),thetypeofsculptureandthespinesizeapproaching this taxon to the Dicomeae, but not to the Mutisieae s.str. Another pollen feature that, as a trend, separates Gladio pappus from the Mutisieae s.str. istheratioE/exinethickness,which Bolick(1991)describedasusefulforthetaxonomyandphyloc b d a e ec ec ea ma oc sc sc sc iit fl en spf
106 Blumea–Volume63/2,2018 geny of the Asteraceae.Infact,theaverageratioforG. vernonioides is5.1,avaluethatissomewhatlowerthantheratio foundbyPereiraCoutinhoetal.(2012)fortheDicomeae(6.1), but, even so, closer to it than to the average values of all the genera of Mutisieae s.str. that we have calculated based on otherauthors’data(seeTable3).Itcanbenotedthateven Bolick’s(1991)averagevalue(6.6)ofthementionedratiofor the Mutisieaes.lat.(whichcomprisedseveraltaxathatarecurrentlyincludedinothertribes)isfarfromthatofG. vernonioides. Also, the mesoapertures involve different exine layers in the Dicomeae and Mutisieae s.str.(seeTable2andthesubsection MesoaperturesoftheDiscussion). Skvarlaetal.(1977)describedtheAnthemoidpatternofultrastructure for the Anthemideae and Barnadesieae.Itwasalso reported for most of the Cardueae (Skvarlaetal.1977,TormoMolina&Ubera-Jiménez1995),theMutisieae(Tellería&Katinas2009)andtheDicomeae (Ortiz&PereiraCoutinho2001, PereiraCoutinhoetal.2011).Thispatternalsocharacterizes the exine of Gladiopappus, and it is relevant to compare its detailswiththetwosubtypesthatPereiraCoutinhoetal.(2011) reported for the Dicomeae. Theydescribedtheexistenceof ‘supportingcolumellaethick,denselydistributedandmoreor lessstraight’fortheDicominae and‘atleastsomeofthesupGenera E/exinethickness Authors (average) Brachyclados 7.7 Tellería&Katinas(2004) Chaetanthera 7.6 Tellería&Katinas(2004) Chaptalia 6.8 Parra&Marticorena(1972) Mutisia 7.5 Tellería&Katinas(2009) Pachylaena 6.3 Parra&Marticorena(1972) Trichocline 6.6 Parra&Marticorena(1972) Table 3 AverageratioE/exinethicknessofthegeneraofMutisieaes.str. Fig. 3TEMmicrographs.a.Detailofanaperture;b.generalequatorialsection;c–f.detailsofexinesections.—ea–endoaperture;ec–ectoaperture; en–endexine;fl–footlayer;iit–innerinternaltectum;isp–inter-spineperforations;ma–mesoaperture;oc–outercolumellae;oit–outerinternaltectum; mc–middlecolumellae;sc–supportingcolumellae;spf–spineperforations;te–tectum.—Scalebars:2µm. c b d a ef ec en ma ec en ea ma fl fl mc mc te te te spf spf iit isp iit oit oit oc oc sc
107 A.PereiraCoutinhoetal.:PalynotaxonomyofGladiopappus porting columellae thin, more or less loosely distributed and moreorlesscurved’forthePleiotaxinae. Clearly, the exine of Gladiopappus belongs to the first subpattern, which supports the inclusion of this genus in the subtribe Dicominae. Mesoapertures OurresultsagreewiththosedescribedbyTormo-Molina& Ubera-Jiménez(1990,1995)andPereiraCoutinhoetal. (2012)fortheCarduoideaeandbyPereiraCoutinho(2002), PereiraCoutinho&Paiva(2003),PereiraCoutinho&Dinis (2007,2009),PereiraCoutinhoetal.(2011,2016)andMontes &Murray(2014)fortheAsteroideae.Nevertheless,theyonly partiallyagreewiththedatareportedbyElGhazaly(1980)and Blackmore(1982)fortheCichorioideae.Infact,theseauthors considered the mesoaperture as involving, respectively, the outer layer of the endexine and the foot layer, but all our observations indicate that it intersects the foot layer and the upper layeroftheendexine.Tellería&Katinas(2009)describedthe mesoaperture of Mutisia (Mutisioideae) asinvolving‘theinner layerofthesexineandtheouterlayerofthenexine’.Although theyemployedLM,SEMandTEM,itisnotclearwhichofthese techniquestheyspecificallyusedtoobservethesestructures. BearinginmindTellería&Katinas’(2009)description,wethink thattheydidnotobservethedetailsoftheapertureswithTEM. Thisimpliesthat,inMutisia, the columellae, the foot layer and the distal part of the endexine or the columellae and the foot layer are involved in the mesoaperture, in any case a different situation from that we observed in Gladiopappus andothertaxa. In the case of Gladiopappus it was relatively easy to observe themesoapertureslimitswithLMandSEM,butthisisnot always the case because, sometimes, they are either diffuse (Tellería&Katinas2004)ormoreorlesscoveredbythoseof theendoapertures(Dimon1971,Tellería&Katinas2004)or ectoapertures(PereiraCoutinho&Dinis2007,2009).Inthe lastcase,theinternalview,withSEM,offracturedexines,can revealthepresenceofthemesoapertures(PereiraCoutinho& Dinis2007),andwesuspectthat,insomecases,theauthors didnotobservethembecausetheydidnotemployTEMor SEMtostudytheexineultrastructureand/ortheendexine infracturedpollengrains.Inconclusion:ourdataandother authors’(seeTable2)revealthatthepresenceofmesoaperturescharacterizesnotonlyallthemostimportantsubfamilies of the Asteraceae(Asteroideae, Cichorioideae, Carduoideae, Mutisioideae)butalsomanyofthesmallerones(Famatinanthoideae, Stifftioideae, Gochnatioideae),althoughsomevariation can occur in the exine layers that are intersected by these pollenstructures.Itisourconvictionthat,atleastasatrend, theexistenceofamesoaperturecharacterizestheapertural system of the Asteraceae as a synapomorphy, and that future carefulexaminationswithTEMandSEMwillrevealitspresence in more subfamilies of Asteraceae. REFERENCES AndersenS.1960.Siliconeoilasamountingmediumforpollengrains. DanmarksGeologiskeUndersøgelse4:116–140. BenthamG.1873.Compositae.In:BenthamG,HookerJD(eds),Genera Plantarum2:163–533.Reeve,London. BlackmoreS.1982.AfunctionalinterpretationofLactuceae(Compositae) pollen.PlantSystematicsandEvolution141:153–168. BlackmoreS,WortleyAH,SkvarlaJJ,etal.2009.Evolutionofpollenin Compositae. In:FunkVA,SusannaA,StuessyTF,etal.(eds),Systematics, evolution,andbiogeographyofCompositae:101–130.InternationalAssociationforPlantTaxonomy,InstituteofBotany,UniversityofVienna,Vienna. BlackmoreS,WortleyAH,SkvarlaJJ,etal.2010.Developmentaloriginsof structuraldiversityinpollenwallsofCompositae.PlantSystematicsand Evolution284:17–32. BolickM.1978.Taxonomic,evolutionaryandfunctionalconsiderationsof Compoditaepollenultrastructureandsculpture.PlantSystematicsand Evolution130:209–218. BolickM.1991.Pollendiameter,exinethicknessandultrastructuretypein thetribesoftheCompositae.CompositaeNewsletter19:17–21. BremerK.1987.TribalinterrelationshipsoftheAsteraceae. Cladistics3: 310–353. CabreraAL.1951.NotassobrecompuestasdeAméricaAustral.Darwiniana 9:363–386. CabreraAL.1965.RevisióndelgéneroMutisia(Compositae).OperaLilloana13:5–227. CabreraAL.1971.Compositae.In:CorreaMN(ed.),FloraPatagónica:1– 451.ColecciónCientíficadelINTA,BuenosAires. CabreraAL.1977.Mutisieae–systematicreview.In:HeywoodVH,HarborneJB,TurnerBL(eds),ThebiologyandchemistryoftheCompositae 2:1039–1066.Academic,London. CassiniH.1817.QuatrièmemémoiresurlafamilledesSynanthérées,contenantl’analysedel’ovaireetdesesaccessoires.JournaldePhysique, deChimie,d’HistoireNaturelleetdesArts85:5–21. DimonMT.1971.ÉtudedestypespolliniquesdesComposésechinuléesdu BassinMediterranéenOccidental.PhDThesis,UniversitédesScienceset TechniquesduLanguedoc. DuistermaatH.1996.MonographofArctiumL.(Asteraceae)–Generic delimitation(includingCousiniaCass.p.p.)revisionofthespecies,pollen morphologyandhybrids.Gorteria.Supplement3:1–143. ElGhazalyG.1980.PalynologyofHypochoeridinaeandScolyminae(Compositae).OperaBotanica8:1–45. ErdtmanG.1960.Theacetolysismethod–areviseddescription.Svensk BotaniskTidskrift54:561–564. FreireSE,BarbozaGE,CanteroJJ,etal.2014.Famathinanthus,anew AndeangenussegregatedfromAphyllocladus(Asteraceae).Systematic Botany39:349–360. HansenHV.1990.SEM-studiesandgeneralcommentsonpollenintribeMutisieae(Compositae)sensuCabrera.NordicJournalofBotany10:607–623. HindDJN.2007.Mutisieae.TribeMutisieaeCass.In:KadereitJW,JeffreyC (eds),Thefamiliesandgeneraofvascularplants,floweringplants,Eudicots, Asterales8:90–123.Springer,Berlin,Heidelberg,NewYork. HoffmannOF.1894.Compositae.In:EnglerA,PrantlK(eds),Dienatürlichen Pflanzenfamilien4:87–391.Engelmann,Leipzig. HumbertJH.1948.UngenrenouveauremarquabledeMutiséesàMadagascar.BulletindelaSociétéBotaniquedeFrance95:181–183. JaramilloP,TrigoMM.2006.PollenmorphologyoftheGalapagosendemic genusScalesia(Asteraceae).GalapagosResearch64:26–30. KatinasL,PruskiJ,SanchoG,etal.2008.ThesubfamilyMutisioideae (Asteraceae).BotanicReview74:469–716. KatinasL,SanchoG,TelleríaMC,etal.2009.Mutisieae sensustricto(Mutisioideaesensustricto).In:FunkVA,SusannaA,StuessyTF,etal.(eds), Systematics,evolution,andbiogeographyofCompositae:229–248.InternationalAssociationforPlantTaxonomy,InstituteofBotany,Universityof Vienna,Vienna. LeonardisW,DePiccioneV,ZizzaA.1983.Premièrecontributionàl’étude taxonomiquedugenre“Centaurea”delaSicilesurlabasedesdonnées polliniquestraitéesparl’analyseinformatique.Webbia38:185–208. LinNN,WangH,LiDZ,etal.2005.Pollenmorphologyofeightgeneraofthe subtribeMutisiinaeLess.sensuBremer(Compositae)fromAsia.Journal ofIntegrativePlantBiology47:1036–1046. MontesB,MurrayMG.2014.PollenmorphologyofSeneciobergii(Asteraceae),withspecialattentiontothemesoaperture.Phyton84:201–208. OrtizS,CarbajalR,SerranoM,etal.2009.Dicomeae(Carduoideae).In: FunkVA,SusannaA,StuessyTF,etal.(eds),Systematics,evolution,and biogeographyofCompositae:267–278.InternationalAssociationforPlant Taxonomy,InstituteofBotany,UniversityofVienna,Vienna. OrtizS,CarbajalR,SerranoM,etal.2013.PhylogenyoftheAfricanMutisieaes.l.(Asteraceae)basedonndhF andtrnL-F sequences(cpDNA). Taxon62:525–536. OrtizS,PereiraCoutinhoA.2001.AchyrothalamusreducedtoErythrocephalum(Asteraceae,Mutisieae).Taxon50:389–403. OsmanAKE.2011.PollenmorphologyoftribesGnaphalieae,Helenieae, PlucheaeandSenecioneae(SubfamilyAsteroideae)ofCompositaefrom Egypt.AmericanJournalofPlantSciences2:120–133. PaneroJL,FunkVA.2002.Towardaphylogeneticsubfamilialclassification fortheCompositae(Asteraceae).ProceedingsoftheBiologicalSociety ofWashington115:909–922. ParraO,MarticorenaC.1972.Granosdepollendeplantaschilenas.II. Compositae-Mutisieae.Gayana,Botanica21:1–107. PastanaGII.1989.ContribuiçãopreliminaraostipospolínicosdatriboMutisieae(Compositae).ActaBotânicaBrasileira2:55–66.
108 Blumea–Volume63/2,2018 PereiraCoutinhoA.2002.PalinologiadastribosInuleaeCass.(s.s.),GnaphalieaeBenth.,Helenieae(Benth.)eHeliantheaeCass.(Asteraceae) em PortugalContinentaleAçores.PhDthesis,FacultyofSciencesandTechnology,UniversityofCoimbra. PereiraCoutinhoA,AguiarCF,SádaBandeiraD,etal.2011.Comparative pollenmorphologyoftheIberianspeciesofPulicaria(Asteraceae,Inuleae, Inulinae)anditstaxonomicsignificance.PlantSystematicsandEvolution 297:171–183. PereiraCoutinhoA,AlmeidaR,SádaBandeiraD,etal.2012.PollenmorphologyintribeDicomeaePanero&Funk(Asteraceae).PlantSystematics andEvolution298:1851–1865. PereiraCoutinhoA,DinisA.2007.AcontributiontotheultrastructuralknowledgeofthepollenexineinsubtribeInulinae(Inuleae,Asteraceae).Plant SystematicsandEvolution269:159–170. PereiraCoutinhoA,DinisA.2009.Alight,scanningelectron,andtransmission electron microscopic study of pollen wall architecture in the subtribe Gnaphaliinae(Gnaphalieae,Asteraceae).PlantSystematicsandEvolution 283:79–92. PereiraCoutinhoA,OrtizS,ValenteM,etal.2014.Acontributiontothe exineultrastructureknowledgeinsubtribeAnisopappinae(Athroismeae, Asteraceae).Willdenowia44(3):431–437. PereiraCoutinhoA,PaivaJ.2003.PalynologyofthegenusGalinsogaRuíz &Pavón(Asteraceae)inPortugal.Polen12:127–136. PereiraCoutinhoA,Valente,M.,FrançaR.,etal.2016.Acontributionto the knowledge of the exine, with special reference to the ultrastructure, insubtribeEcliptinae(Heliantheae,Asteraceae).PlantSystematicsand Evolution302:1207–1216. PuntW,HoenPP,BlackmoreS,etal.2007.Glossaryofpollenandspore terminology.ReviewofPalaeobotanyandPalynology143:1–81. Saad-LimamSB,NabliMA,RowleyJR.2002.ExineontogenyinBorago officinalispollen.Grana41:216–226. SkvarlaJJ,TurnerBL.1966.SystematicimplicationsfromelectronmicroscopicstudiesofCompositaepollen–areview.AnnalsoftheMissouri BotanicalGarden53:220–257. SkvarlaJJ,TurnerBL,PatelVC,etal.1977.PollenmorphologyintheCompositaeandinmorphologicallyrelatedfamilies.In:HeywoodVH,Harborne JB,TurnerBL(eds),ThebiologyandchemistryofCompositae 2:141–265. AcademicPress,London. SouthworthD.1966.UltrastructureofGerberajamesonii pollen.Grana Palynologica6:324–337. StixE.1960.PollenmorphologischeUntersuchungenanCompositen.Grana Palynologica2:41–104. StuessyT,UrtubeyE,GruenstaeudlM.2009.Barnadesieae(Barnadesioideae).In:FunkVA,SusannaA,StuessyTF,etal.(eds),Systematics, evolution,andbiogeographyofCompositae:215–228.InternationalAssociationforPlantTaxonomy,InstituteofBotany,UniversityofVienna,Vienna. TelleríaMC.2007.TaxonomicsignificanceofpollentypesintheGuyana Highland-centredcompositegeneraofMutisioideae(Asteraceae).Botanical JournaloftheLinneanSociety156:327–340. TelleríaMC,KatinasL.2004.ApalynologicandcomparativestudyofChaetanthera(Asteraceae,Mutisieae)andalliedgenera.SystematicBotany 29:752–773. TelleríaMC,KatinasL.2005.TheunusualoccurrenceoftricolpatepollenwithinMutisieae(Asteraceae).Grana44:91–97. TelleríaMC,KatinasL.2009.Newinsightsintothepollenmorphologyofthe genusMutisia(Asteraceae,Mutisieae).PlantSystematicsandEvolution 280:229–241. TelleríaMC,SanchoG,FunkVA,etal.2013.Pollenmorphologyandits taxonomicsignificanceinthetribeGochnatieae(Compositae,Gochnatioideae).PlantSystematicsandEvolution299:935–948. TiangangG,YoushengC,HindDJN,etal.2011.Mutisieae. In:WuZY,Raven PH,HongDY(eds),FloraofChina(Asteraceae)20–21:9–32.Science Press,Beijing,MissouriBotanicalGardenPress,St.Louis. Tormo-MolinaR,Ubera-JiménezJL.1990.Theaperturalsystemintribes AnthemideaeandCardueae(Compositae)withspecialreferencetothe mesoaperture.ReviewofPalaeobotanyandPalynology62:1–9. Tormo-MolinaR,Ubera-JiménezJL.1995.Tipospolínicosdelatribu CardueaeenlaPenínsulaIberica.MonografíasdelJardínBotánicode Córdoba2:5–52. TreeofLifeWebProject.2009.DicomeaePanero&V.A.Funk.Version11 January2009(temporary).http://tolweb.org/Dicomeae/104544/2009.01.11 inTheTreeofLifeWebProject,http://tolweb.org/ UrtubeyE,TelleríaMC.1998.PollenmorphologyofthesubfamilyBarnadesioideae(Asteraceae)anditsphylogeneticandtaxonomicsignificance. ReviewofPaleobotanyandPalynology104:19–37. WagenitzG.1976.SystematicsandphylogenyoftheCompositae(Asteraceae).PlantSystematicsandEvolution125:29–46. WangH,WortleyAH,BlackmoreS.2009.PollenmorphologyofCrepidinae andLactucinae(Asteraceae:Cichorieae)anditssystematicsignificance. Grana48:160–178. WodehouseR.1929a.PollengrainsintheidentificationofplantsIII.The Nassauvinae.BulletinoftheTorreyBotanicalClub56:123–138. WodehouseR.1929b.PollengrainsintheidentificationofplantsIV.The Mutisieae. AmericanJournalofBotany16:297–315. WodehouseR.1935.Pollengrains.McGrawHillBookCompany,NewYork, London. WortleyAH,BlackmoreS,ChissoeWF,etal.2012.RecentadvancesinCompositae(Asteraceae)palynology,withemphasisonpreviouslyunstudied andunplacedtaxa.Grana51:158–179. WortleyAH,FunkVA,RobinsonH,etal.2007.AsearchforpollenmorphologicalsynapomorphiestoclassifyroguegenerainCompositae(Asteraceae).ReviewofPalaeobotanyandPalynology146:169–181. WortleyAH,FunkVA,SkvarlaJJ.2008.PollenandtheevolutionofArctotideae(Compositae).BotanicalReview74:438–466. ZhaoZ,SkvarlaJJ,JansenRK.2006.Mutisieae(Asteraceae)pollenultrastructureatlas.Lundellia9:51–76.