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Phylogenetic Position of Titanotrichum Oldhamii (Gesneriaceae) Inferred Fromf Our Different Gene Regions

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Phylogenetic Position of Titanotrichum Oldhamii (Gesneriaceae) Inferred Fromf Our Different Gene Regions SystematicBotany (2004),29(2): pp. 407– 418 q Copyright 2004by the AmericanSociety of PlantTaxonomists Phylogenetic Position of Titanotrichum oldhamii (Gesneriaceae) Inferred FromF our Different Gene Regions CHUN-NENG WANG,1,2,3,4 MICHAEL MO¨ LLER,1 and QUENTIN C. B. CRONK1,2,3 1Royal BotanicGarden, 20AIn verleith Row,Edinburgh EH3 5LR,Scotland, UK; 2Institute ofCell and MolecularBiology ,The University ofEdinburgh ,Edinburgh EH9 3JH,Scotland, UK; 3Present address: BotanicalGarden and Centre forPlant Research, University ofBritish Columbia, VancouverV6T 2TL,Canada 4Author forCorrespon dence ([email protected]) CommunicatingEditor: James F .Smith ABSTRACT. Titanotrichumoldhamii has been variously placed inGesneriace ae orScrophulari aceae, although mostrecent taxonomictreatmentstrea titas amonotypictribe within Gesneriace ae.Inthis study ,wereconstructedabroad-scale phy- logenycontaining Titanotrichum usinggene sequencesfromfour sequence regions(chloropla st trnL-F intronand spacer and atpB-rbcL spacer, nuclear 26S ribosomalDN A, and the low-copy developmentalgene CYCLOIDEA,CYC).The phylogenies inferredfrom eac hindividualdata setand the combinedda ta are congruent inplacing Titanotrichum insideGesneriac eae. The phylogenetic treebased on combinedchloropla stand nuclear DNAsequences grouped Titanotrichum withsubfamilies Gesnerioideae (New World)and Coronantheroideae (SouthP acic and Chile). Wehave isolated CYC, frommost of the species ofGesneriace ae and Scrophulariaceae represented inthis study ,and thisgene phylogenysuggeststhe same placementof Titanotrichum . CYC was found toev olvethreetimes faster than the trnL-F intronand spacer, 3.3 timesfaster than the atpB- rbcL spacer, and eighttimes faster than nuclear 26S rDNA. Althoughthere is considera ble phylogenetic informationin this fastev olving gene, analysis isproblema tic because ofhigh lev els ofhomopla syand paralogy. Inaddition toa duplication predatinga split between New Worldand OldW orldtaxa ( Gcyc1 vs. Gcyc2),thereare several subsequentlineage-related duplications(mainly within Gcyc1). The monotypic taxon, Titanotrichumoldhamii nerioideae(N ewWorld) (Burtt and Wiehler 1995).In (Hemsl.) Soler.,is ofuncertain taxonomicafnity ,being Old World species the cotyledons becomeunequal in variously placedin Scrophulariaceae(sens. lat.;W ett- size soon aftergerminati on (anisocotyly) due tothe stein 1891)and Gesneriaceae(Burtt 1962,1977). The extended activityof a meristem atthe baseof the cot- difculty of classifying Titanotrichum arises becauseit yledon, while New World species ofsubfamily Ges- shares several features with bothScrophulariac eae s.l. nerioideaeand Coronantheroideae are allisocotylous, and Gesneriaceae.The species was rst placedin Reh- lacking such persistent meristematicactivity (Burtt mannia (Scrophulariaceaes.l.) as its racemose inores- 1962).Interestingl y, Titanotrichum ,although geograph- cence and showy bell-shaped owers are reminiscent ically Old World, is isocotylous (Wang and Cronk ofScrophularia ceaesuch as Rehmannia and Digitalis 2003). Titanotrichum alsohas someuniquem orpholog- (Hemsley 1895).Later ,in 1909,Solerede rnamed it as icalcharacters, such asbulbil proliferati on in inores- a new genus Titanotrichum in Gesneriaceaebased on cences (Wang and Cronk 2003),not seen in anyother the unilocularov ary (Solereder1909).It w asplaced in Gesneriaceaespecies. the Old World subfamilyCyrtandroid eae on account Toresolve the placement of Titanotrichum , we use ofits superior ovary and geographic distribution(So- anapproach combining molecularevidenc efrom two lereder 1909).Recent taxonomictreatmentsraised it to chloroplast DNA(cpDNA)sequence s, trnL-F intron amonotypic tribe in the Cyrtandroideae because ofits and spacerand atpB-rbcL spacer,the 26Sn uclearri- unique morphology (Wang and Pan1992; Burtt and bosomalD NA(nrDNA)and anucleardev elopmental Wiehler 1995).A recent molecular phylogenetic study gene, CYCLOIDEA (CYC).F or comparisons atthe fam- using chloroplast ndhF gene sequences addressed its ily level or above(as this gene is conservative),26S position within Gesneriaceae; it wasplaced as sister to datahas proven tobe ph ylogeneticallyuseful, partic- the rest ofsubfamily Cyrtandroid eae butwith little ularly forprevious ly unresolvedclades and taxa(e.g., branchsupport (Smith et al.1997a, 1997b). On the oth- Circaeaster ,Oxelman and Lide´n1995;angiosperm phy- er hand, achemotaxonomic study on phenolic acid logeny,Hershkovitzet al.1999). The chloroplast trnL- compoundsgrouped Titanotrichum , Cyrtandromoea , and F intron and spacerand atpB-rbcL spacerhav ebeen Rehmannia into Scrophulariaceae(Kvist and Pedersen successfully used forinferring phylogenies atthe ge- 1986).Sealy (1949)allied Titanotrichum to New World neric and intragenericlev el (Taberlet et al.1991; Go- Gesneriaceaegenera, Isoloma (5Kohleria) and Naegelia lenberg et al.1993; Gielly and Taberlet 1994;Manen et (5Smithiantha ),becausethey possess asimilar habit al.1994), and have alsorecently been used successfully and scaly rhizome.Anisocotyly is probablythe most on Gesneriaceae(M ayer et al.2003). reliable characterto separate Cyrtandroid eae and Ges- CYCLOIDEA belongs toa multigene family,the TCP 407 408 SYSTEMATIC BOTANY [Volume 29 family,which comprises axillary meristem identity reading frame(O RF)w ere amplied forour studyusing forw ard primer GcycFS and reverseprimer GcycR (forthe exact amplied genes in Zea mays (TB1),oralsymmetry genes in An- CYC regionsee Mo¨lleret al. 1999). Toamplifyfour different gene tirrhinummajus (CYC)and DNA-binding protein regionsef ciently across distantlyrela ted species inour study,one genes in Oryzasativa (PCF)(Cubaset al.1999a, 1999b; new PCR primerw as designedor existing ones modied from Cubas2002). The gene family encodes putativetran- originalpublica tions. Forthe amplication ofthe complete atpB- rbcL spacer, anew forward primer‘ ABF’(5 9-GGA AACCCC AGA scription factors(Doebley and Lukens 1998).The TB1/ ACC AGA AG-39)was designedand combinedwith the reverse CYC subfamilyis characterisedbytw oconserved re- primer‘ JF5’from Manen et al. (1994). Toobtain the complete trnL- gions: abasichelix-loop- helix TCPdomain and anar- F intronand spacer region,primers ‘ c’and ‘f’from T aberlet et al. (1991) were chosen. Toobtain the upper part ofthe 26S ribosomal ginine-richRdomain (Cubas1999b). Mo ¨ller et al. DNAregion,forw ard primer‘ ITS-3P’located in5.8S (Mo¨llerand (1999)have isolated twoputative paralogues in Ges- Cronk1997) and reverse primer‘ 28S2R’w ere used (Oxelmanand neriaceae (Gcyc1 vs. Gcyc2)from species with different Lide´n1995). Circa 1,200 base pairs (bp)(35%) fromthe 5 9end of ower symmetries, in anattem ptto test their sequence the 26S gene were amplied. 50–100 ngtempla te DNAwas incor- porated in50 mlreactions, containing 1 mMprimer,100 mM each divergencein relation tomorpholo gicalchanges (zy- dNTPs (Roche, USA),2.5mM MgCl 2, and 0.5U Taq polymerase gomorphyvs. actinomorphy).H owever,their results, (Bioline,UK) and 1X Taq buffer(16mM (NH 4)2SO4, 67mM Tris- together with afollow-upstudy (Citerne et al.2000), HCl (pH 8.8), 0.01% Tween20). did not suggest loss offunctional genes in actinomor- Except forthe CYCLOIDEA region(PCR conditions described in Citerneet al. 2000), auniversal PCR prole for trnL-F,atpB-rbcL, phic taxa.They found that Gcyc evolution wasconsis- and 26S was used as follows: 3mina t95 8C, then ve cycles of1 tent with Gesneriaceaeph ylogenies atthe generic and min at 958C, 1 min at 578C, 2 min at 728C, followed by30 cycles triballevels (Mo¨ller et al.1999; Citerne et al.2000). of 45 s at 948C, 45 s at 578C, 2 min at 728C, witha nal extension step at 728Cfor7 minutes. Amplication products were checked Since CYC belongs toa multi-copygene family,it is on 1% agarose gelsin 1X TBE bufferand visualized under UV reasonable toexpect that two or more homologues afterethidium bromide staining (0.1 mg/ml).PCR products were would beisolated in eachtaxon studied. Orthologues puried usingQiagen puri cation columns (QiagenLtd, Dorking, and paraloguesmay beidenti ed by phylogenetic Surrey,UK) according tothe manufacturer’s protocols. Sequencing. Direct cycle sequencingwas carried out usingthe analysis (Baum1998; Eisen 1998;Ba um et al.2002). big-dyeterminator ready reaction mix(P erkinElmer Applied Bio- The aim ofthis study is toobtain chloropla st trnL- systemsdivision, Warrington,UK) followingstandard protocols. F,atpB-rbcL, nuclear 26S,and CYCLOIDEA gene se- Sequencingproducts were analysed on an ABIPRISM 3100 au- tomatic DNAsequencer (Applied Biosystems,W arrington,UK). quences from selected taxato in vestigate the phylo- The PCR amplifyingprimers of all gene regionsw ere also used genetic position of Titanotrichum oldhamii , and to in- as sequencingprimers.Several internal primersw ere designedfor vestigate how the Gcyc homologues evolved in these our samples toallow complementarysequence conrma tion. species with respect togene duplicationor extinction These were forthe atpB-rbcL spacer region(atpB-VMF forw ard: 5 9- GAATTC CGC CTW TTT TCACATCTA-3 9;VM-Rre verse: 5 9- events. Because Titanotrichum has been placedin both TAGATG TGAAAAT AGGCG GAAT -3 9),for 26S (26S-Q1Ffor- Scrophulariaceae s.l. and Gesneriaceae,we sampled a ward: 59-CATTCG ACC CGT CTT GAAA C-3 9;26S-Q1R reverse: large number ofrepresenta tive taxafrom bothfami- 59-TTTC AAG ACGGG TCG AATGG-3 9), and for CYCLOIDEA lies. (Cyc-NFforw ard: 5 9-GCR AGG GCB AGR GAA AGAAC-3 9; Cyc- NR reverse: 5 9-GCACATTTT CTC YYT YGT TCT TTC-3 9). Cloning of CYCLOIDEA Homologues.
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