Phylogenetic Analyses of Basal Angiosperms Based on Nine Plastid, Mitochondrial, and Nuclear ...

29 Pages·2005·0.49 MB·English

Phylogenetic Analyses of Basal Angiosperms
Based on Nine Plastid, Mitochondrial, and Nuclear
Genes
Citation
Qiu, Yin-Long, Olena Dombrovska, Jungho Lee, Libo Li, Barbara A. Whitlock, Fabiana
Bernasconi-Quadroni, Joshua S. Rest, et al. 2005. Phylogenetic analyses of basal angiosperms
based on nine plastid, mitochondrial, and nuclear genes. International Journal of Plant Sciences
166(5): 815-842.
Published Version
http://dx.doi.org/10.1086/431800
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http://nrs.harvard.edu/urn-3:HUL.InstRepos:2710479
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Int.J.PlantSci. 166(5):815–842.2005.
(cid:1)2005byTheUniversityofChicago.Allrightsreserved.
1058-5893/2005/16605-0012$15.00
PHYLOGENETIC ANALYSES OF BASAL ANGIOSPERMS BASED ON NINE PLASTID,
MITOCHONDRIAL, AND NUCLEAR GENES
Yin-LongQiu,1;*,y,zOlenaDombrovska,*,y,zJunghoLee,2;y,zLiboLi,*,yBarbaraA.Whitlock,3;yFabianaBernasconi-Quadroni,z
JoshuaS.Rest,4;*Charles C. Davis,* ThomasBorsch,§Khidir W.Hilu,kSusanne S.Renner,5;#DouglasE. Soltis,**
PamelaS.Soltis,yy MichaelJ. Zanis,6;zz JamieJ. Cannone,§§RobinR. Gutell,§§Martyn Powell,kk
VincentSavolainen,kkLars W.Chatrou,##and MarkW.Chasekk
*DepartmentofEcologyandEvolutionaryBiology,UniversityHerbarium,UniversityofMichigan,AnnArbor,Michigan48109-1048,U.S.A.;
yBiologyDepartment,UniversityofMassachusetts,Amherst,Massachusetts01003-5810,U.S.A.;zInstituteofSystematicBotany,University
ofZurich,8008Zurich,Switzerland;§Nees-Institutfu¨rBiodiversita¨tderPflanzen,Friedrich-Wilhelms-Universita¨tBonn,Meckenheimer
Allee170,53115Bonn,Germany;kBiologyDepartment,VirginiaPolytechnicInstituteandStateUniversity,Blacksburg,Virginia
24061,U.S.A.;#DepartmentofBiology,UniversityofMissouri,St.Louis,Missouri63121-4499,U.S.A.;**Departmentof
BotanyandtheGeneticsInstitute,UniversityofFlorida,Gainesville,Florida32611,U.S.A.;yyFloridaMuseumof
NaturalHistoryandtheGeneticsInstitute,UniversityofFlorida,Gainesville,Florida32611,U.S.A.;zzSchool
ofBiologicalSciences,WashingtonStateUniversity,Pullman,Washington99164,U.S.A.;§§Institutefor
CellularandMolecularBiology,andSectionofIntegrativeBiology,UniversityofTexas,Austin,Texas
78712,U.S.A.;kkRoyalBotanicGardens,Kew,Richmond,SurreyTW93DS,UnitedKingdom;
and##NationalHerbariumoftheNetherlands,UtrechtUniversity,Heidelberglaan2,
3584CSUtrecht,TheNetherlands
DNA sequences of nine genes (plastid: atpB, matK, and rbcL; mitochondrial: atp1, matR, mtSSU, and
mtLSU;nuclear:18Sand26SrDNAs)from100speciesofbasalangiospermsandgymnospermswereanalyzed
using parsimony, Bayesian, and maximum likelihood methods. All of these analyses support the following
consensusofrelationshipsamongbasalangiosperms.First,Amborella,Nymphaeaceae, andAustrobaileyales
arestronglysupportedasabasalgradeintheangiospermphylogeny,witheitherAmborellaorAmborellaand
Nymphaealesassistertoallotherangiosperms.Anexaminationofnucleotidesubstitutionpatternsofallnine
genesruledoutanypossibilityofanalyticalartifactsbecauseofRNAeditingandGC-contentbiasinplacing
thesetaxaatthebaseoftheangiospermphylogeny.Second,MagnolialesaresistertoLauralesandPiperales
are sister to Canellales. These four orders together constitute the magnoliid clade. Finally, the relationships
amongCeratophyllum,Chloranthaceae,monocots,magnoliids,andeudicotsareresolvedindifferentwaysin
various analyses, mostly with low support. Our study indicates caution in total evidence approaches in that
someofthegenesemployed(e.g.,mtSSU,mtLSU,andnuclear26SrDNA)addedsignalthatconflictedwiththe
othergenes inresolving certainparts of thephylogenetic tree.
Keywords: basal angiosperms, Amborella, magnoliids, multigene analysis, synapomorphic substitutions,
phylogeny.
Introduction and Stevenson 1991; Martin and Dowd 1991; Hamby and
Zimmer 1992; Taylor and Hickey 1992; Chase et al. 1993;
The past 20 years have witnessed significant progress in Qiu et al. 1993, 1999, 2000, 2001; Soltis et al. 1997, 2000;
our understanding of the phylogeny of basal angiosperms Nandietal.1998;Hootetal.1999;MathewsandDonoghue
fromanalysesofmolecularandnonmoleculardata(Dahlgren 1999,2000;Parkinsonetal.1999;Renner1999;Soltisetal.
and Bremer 1985; Donoghue and Doyle 1989; Loconte 1999a; Barkman et al. 2000; Doyle and Endress 2000; Gra-
ham and Olmstead 2000b; Savolainen et al. 2000; Nickrent
etal.2002;Zanisetal.2002,2003;Borschetal.2003;Hilu
1Authorforcorrespondence;[email protected].
et al. 2003; Lo¨hne and Borsch 2005). Specifically, it has be-
2Current address: School of Biological Sciences, Seoul National
come increasingly clear that Amborella, Nymphaeaceae, and
University,Shillim,Kwanak,Seoul,SouthKorea151-747.
3Current address: Department of Biology, University of Miami, Austrobaileyales (sensu APG II 2003) represent the earliest-
Miami,Florida33124-0421,U.S.A. diverging lineages of extant angiosperms. Furthermore, the
4Current address: Department of Ecology and Evolution, magnoliids (sensu APG II 2003; see Qiu et al. 1993 for a re-
UniversityofChicago,Chicago,Illinois60637,U.S.A. view of the history of this term) have been identified as a
5Current address: Department of Biology, Ludwig Maximilians monophyleticgroupinsomeanalyses(Qiuetal.1999,2000;
UniversityMunich,Munich,Germany. Zanis et al. 2002, 2003; Hilu et al. 2003), but their mono-
6Current address: Division of Biological Sciences, University of
phyly (Savolainen et al. 2000; Soltis et al. 2000) and espe-
California,SanDiego,LaJolla,California92093,U.S.A.
ciallyrelationshipsamongtheirmemberorders(Magnoliales,
ManuscriptreceivedNovember2004;revisedmanuscriptreceivedMay2005. Laurales, Piperales, and Canellales) need further evaluation
815
816 INTERNATIONAL JOURNAL OF PLANTSCIENCES
andresolution.Finally,allangiospermsexcludingAmborella, quences were generated by us for mtSSU, matK, and nuclear
Nymphaeaceae,andAustrobaileyalescanbedividedintofive 26S rDNA. For the five genes used in Qiu et al. (1999), sev-
clades: Ceratophyllum, Chloranthaceae, magnoliids, mono- eral new sequences were produced to fill the missing entries
cots,andeudicots(tricolpatessensuJuddandOlmstead2004; inthatmatrix.Theorthologousatp1wasusedtoreplacethe
see also Walker and Doyle 1975; Crane 1989; Donoghue copy we obtained earlier from Amborella (Qiu et al. 1999,
and Doyle 1989; Doyle and Hotton 1991; Chase et al. 2000), which has been shown to be a xenolog horizontally
1993). Relationships among these five lineages, however, are transferred from an asterid (Barkman et al. 2000; Bergthors-
best interpreted as unresolved at present because analyses son et al. 2003). For all nine genes we have taken sequences
withdifferenttaxonandcharacter-samplingschemesandphy- from GenBank when appropriate. Detailed source informa-
logenetic methods have produced conflicting topologies that tion for all sequences and correction to errors in table A1 of
are generally only weakly supported (Barkman et al. 2000; Qiu et al. (2000) are provided in tables 1 and 2. Of all taxa
Soltisetal.2000;Zanisetal.2002,2003;Hiluetal.2003). andallgenes,onlyfourtaxahavemissingdatainoneortwo
Despiteprogress,moreworkisneededtofurtherclarifyre- genes: Metasequoia (mtSSU and matR), Hortonia (matR),
lationships among basal angiosperms. In this study, we add and Dioscorea and Myristica (nu26S) (tables 1, 2). Eight of
sequencedataoffournewgenestoafive-genematrixassem- the nine genes (all except mtSSU) were aligned using Clustal
bled earlier (Qiu et al. 1999, 2000) and conduct parsimony, X (Thompson et al. 1997). Because of extraordinary length
Bayesian, and maximumlikelihood (ML) analyses to address variationinseveralregionsofmtSSU,thisgenewasmanually
several issues. First, we attempt to show that placement of aligned with the alignment editor AE2 (developed by T.
Amborella, Nymphaeaceae, and Austrobaileyales at the base Macke; Larsen et al. 1993). Although these regions typically
of angiosperm phylogeny is free of any analytical artifact. hadminimalsequenceidentitythatcouldnotbealignedbased
This is especially important in light of recent analyses of the on sequence alone, they usually had similar structural ele-
entire plastid genome sequences of Amborella and Nym- ments that facilitated the alignment of these sequences. In
phaea that do not support them as basalmost angiosperms addition,allofthe computer-generatedalignmentswereman-
(Goremykin et al. 2003a, 2003b, 2004; but see Soltis and ually adjusted with the MacClade 4.05 (Maddison and Mad-
Soltis 2004; Soltis et al. 2004; Stefanovic et al. 2004). Sec- dison 2002) alignment editor. All of the aligned positions
ond,weaimtoevaluatethemonophylyofmagnoliidsandto were used in the phylogenetic analyses. We also eliminated
resolve the relationships among their members: Magnoliales, the positions in regions with significant length variations in
Laurales,Piperales,Canellales.Finally,wewishtoresolvere- the four rDNAs from the phylogenetic analyses of the nine-
lationships among Ceratophyllum, Chloranthaceae, magno- gene matrix.These latteranalysesyielded results not substan-
liids,monocots,andeudicots. tiallydifferentfromthosepresentedhere(datanotshown).
Threeseriesofanalyseswereperformedtoaddressvarious
issues. First, two separate matrices were assembled to recon-
Material and Methods struct the overall phylogeny of basal angiosperms, one con-
sisting of all nine genes and the other of five protein-coding
We included 100 terminals from 98 genera, representing genes. The decision to make a separate matrix using the five
all major lineages of gymnosperms and basal angiosperms. protein-coding genes was based on the following considera-
Acorus and Ceratophyllum were the only two genera for tions:(1)allpositionswithintheproteingenes shouldevolve
which two species each were sampled. Only two families of more independently than those of rDNAs, many of which
basal angiosperms were not included, Gomortegaceae (Ren- evolve in a coupled fashion due to base pairing in stem re-
ner 1999) and Hydnoraceae (Nickrent et al. 2002), because gions in these genes (Soltis and Soltis 1998; Soltis et al.
of many missing data entries. Most of the terminals consist 1999b; O. Dombrovska and Y.-L. Qiu, unpublished data);
ofsequencesderivedfromasinglespecies(andfrequentlythe (2) the protein-coding genes generally show fewer problems
same DNA sample) and occasionally from different species of paralogy and xenology compared to nuclear 18S and 26S
of the same genus (tables 1, 2). Eight gymnosperms covering rDNAs, for which nonorthologous copies were occasionally
allfourextantlineageswereusedasoutgroups. encountered; and (3) the protein-coding genes are free of
The four new genes added in this study are: plastid matK alignment uncertainties compared to two mitochondrial
(a group II intron-encoded maturase), mitochondrial SSU rDNAs,whichexhibitextraordinarylengthvariationscaused
(small subunit) and LSU (large subunit) rDNAs, and nuclear by insertions and deletions in a few regions. The parsimony,
26SrDNA.Withthefivegenesfromourearlieranalyses(mi- Bayesian, and maximum likelihood (ML) analyses were
tochondrial atp1 and matR, plastid atpB and rbcL, and nu- implementedseparatelyonbothmatrices.Toevaluatethein-
clear 18S rDNA), the total of nine genes used in this study formativeness of the two nuclear rDNAs further, the five-
represents a sampling of a large number of characters from protein-gene matrixwascombined with18Sand26SrDNAs
eachofthethreeplantgenomes.Furthermore,thesegenesen- sequentially to form two more matrices. Only parsimony
compass diverse functions, including energy metabolism, car- bootstrapanalyseswereconductedonthesetwomatrices.
bohydratesynthesis,RNAprocessing,andproteinsynthesis. Second, three separate genome-specific matrices were con-
DNA extraction and sequencing methods follow Qiu etal. structed to address whether placement of Amborella, Nym-
(2000). All primer sequences used for amplifying and se- phaeaceae, and Austrobaileyales as sisters to all other extant
quencing the genes are available from the corresponding au- angiospermsissupportedbydatafromtheplastid,mitochon-
thor on request. All sequences of mtLSU were newly drial, and nuclear genomes separately. This type of analy-
generatedinthisstudy,whereasapproximatelyhalfofthese- sis has only been conducted occasionally (Mathews and
QIU ETAL.—BASALANGIOSPERM PHYLOGENY 817
Donoghue 1999, 2000; Graham and Olmstead 2000b; Savo- for the matrix of five protein genes plus two nuclear rDNAs
lainenetal.2000;Zanisetal.2002).Arobustunderstanding where 5000 resampling replicates were used) with the same
of organismal phylogeny should be based on evidence from tree search procedure as described above except with simple
each of the three plant genomes (Qiu and Palmer 1999) ex- taxonadditionandthesteepestdescentoptionon.
cept in cases of hybridization and horizontal gene transfer. For Bayesian and ML analyses, the optimal models of se-
Only parsimony bootstrap analyses were conducted on these quenceevolutionforthenine-geneandfive-protein-genedata
datasets. sets were estimated using ModelTest 3.6 (Posada and Cran-
Third, we investigated the types of substitutions that pro- dall 1998) and DT-ModSel (Minin et al. 2003). The general
vided phylogenetic signal for identifying Amborella, Nym- time-reversible model (Rodrı´guez et al. 1990) including pa-
phaeaceae, and Austrobaileyales as the earliest-diverging rameters for invariant sites and rate variation (GTRþIþG)
lineages of extant angiosperms. For an issue as critical as bestfitsbothdatasetsandwasusedtoconducttheanalyses.
the rooting of angiosperm phylogeny, merely having high Bayesian analyses were performed using MrBayes version
bootstrap numbers from an analysis is not enough to gain 3.0b4 (Huelsenbeck and Ronquist 2001). For the nine-gene
confidence in the result (Soltis et al. 2004). Some poorly un- matrix,thedatawerepartitionedaccordingtocodonpositions
derstood molecular evolutionary phenomena, such as RNA (first, second, and third, for protein genes only), genomes
editing (Steinhauser et al. 1999; Kugita et al. 2003; (plastid, mitochondrial, and nuclear), and gene types within
DombrovskaandQiu2004)andGC-contentbias(Steeletal. a genome (rRNAvs. protein genes). For the five-protein-gene
1993), both of which can occur in a genome-wide, lineage- matrix,thedatawerepartitionedaccordingtocodonpositions
specific fashion, can generate substitutions that lead to spuri- and genomes. Calculations of likelihood for searches of both
ousgroupingsinphylogeneticanalyses.Hence,itisimportant matrices were implemented under the GTRþIþG model of
that we understand the types of substitutions that are behind sequence evolution, assuming different stationary nucleotide
those high bootstrap percentages. We examined the nine-gene frequencies. The posterior probability (PP) was estimated by
matrixvisuallyandidentifiedthesitesthat containapparently samplingtrees fromthe PPdistributionusingMetropolis cou-
synapomorphicchangesthatseparategymnosperms-Amborella- pled Markov Chain Monte Carlo methods. Two and four
Nymphaeaceae-Austrobaileyales from all other angiosperms. chains of 5,000,000 generations were run for the nine-gene
Siteswereclassifiedasapparentlysynapomorphiciftheycon- matrixand five-protein-genematrix, respectively. Chains were
tainedthesamenucleotideinatleasttwoofthefourgymno- sampled every 100 generations. Likelihood scores converged
sperm lineages (cycads, Ginkgo, conifer II [non-Pinaceae onastablevalueafter500,000generations(theburn-inofthe
conifers], and GnetalesþPinaceae; Bowe et al. 2000; Chaw chain),andcalculationsofPPwerebasedonthetreessampled
et al. 2000) and at least two of the three basal angiosperm afterthisgeneration.
lineages (Amborella, Nymphaeaceae, and Austrobaileyales) Maximum likelihood analyses were performed separately
but had a different and generally invariable nucleotide in all on the nine-gene and five-protein-gene data sets using
other angiosperms (hence a synapomorphy for euangio- PHYML version 2.4.4 (Guindon and Gascuel 2003) under
sperms, sensu Qiu et al. 1999). We then performed both a the optimal model of sequence evolution. For both data sets,
most parsimonious tree search and a parsimony bootstrap the GTRþIþG model was implemented with parameter
analysis with these sites removed to verify our identification. valuesfortheproportionofinvariantsites(nine-gene¼0:19,
These synapomorphic substitutions were finally checked to five-gene-protein¼0:21) and the gamma distribution (nine-
determine if they could have been generated by RNA editing gene¼0:43, five-gene-protein¼0:68) as estimated by
or GC-content bias. In addition, codon position and type of ModelTest 3.6 and DT-ModSel. The optimal rate of nucleo-
change(transitionvs.transversion) werenotedfor thesesub- tide substitution and transition/transversion ratios was esti-
stitutions. mated from the data during ML searches. Maximum
These last two series of analyses were designed to comple- likelihood support values were similarly estimated from 100
ment the analyses we performed earlier (Qiu et al. 1999, bootstrapreplicatesinPHYML.
2000, 2001), to ensure that the placement of Amborella,
Nymphaeaceae, and Austrobaileyales as basal lineages is in-
deedbasedonhistoricalsignalrecordedinthemultiplegenes Results
from all three plant genomes rather than the result of yet
poorly understood analytical artifacts. These analyses are Forthenine-genedataset,whichcontained26,990aligned
particularlyrelevantintheongoingdebateoverwhetherAm- nucleotides, two islands with two and four shortest trees
borella and Nymphaea are basal angiosperms (Goremykin (length¼51;834 steps; consistency index ½CI(cid:1)¼0:47; reten-
etal.2003a,2003b,2004;Soltisetal.2004;SoltisandSoltis tion index ½RI(cid:1)¼0:57) were found 259 and 315 times, re-
2004;Stefanovicetal.2004). spectively, out of 1000 random taxon-addition replicates in
Inparsimonysearchesweusedequalweightingforallposi- the parsimony search. One of the six trees is shown (fig. 1),
tions and character-state changes using PAUP* 4.0b10 (Swof- with the nodes that are not present in the strict consensus of
ford 1998). When searching for the shortest trees, a heuristic allsixtreesindicatedbyasterisks.
searchwasconductedusing1000randomtaxon-additionrep- For the five-protein-gene data set, which contained 9351
licates, one tree held at each step during stepwise addition, aligned nucleotides, a single island of two shortest trees
TBR branch swapping, steepest descent option off, MulTrees (length¼18;839 steps; CI¼0:42; RI¼0:59) was found in
option on, and no upper limit of MaxTrees. For bootstrap all 1000 random taxon-addition replicates in the parsimony
analyses, 1000 resampling replicates were performed (except search.Oneofthetwotreesisshown(fig.2),withthenodes
Table 1
Vouchers,Contributors,GenBankAccessionNumbers,andReferencesfortheSequencesUsedinThisStudy
Familyandspecies mt-SSUrDNA mt-LSUrDNA cp-matK nu-26SrDNA
Acoraceae:
AcoruscalamusL. Parkinsonetal.1999; Qiu94052;OD/FBQ/YQ FuseandTamura2000; Qiu94052;OD/YQ;
AF193976 DQ008817 AB040154 DQ008654
AcorusgramineusSoland. Qiu97131;JL/LL/YQ; Qiu97131;OD/FBQ/YQ; FuseandTamura2000; Kuzoffetal.1998;AF036490
DQ008668 DQ008818 AB040155
Alismataceae:
Alismaplantago-aquaticaL. Qiu96177;JL/LL/YQ; Qiu96177;OD/FBQ/YQ; Qiu96177;LL/YQ;
DQ008669 DQ008812 DQ008651
AlismacanaliculatumA.Br.&Bouche´ FuseandTamura2000;
AB040179
Amborellaceae:
AmborellatrichopodaBaill. Parkinsonetal.1999; B.Hallsn,IND,Qiu97123*; Hiluetal.2003;B.Hallsn, Zanisetal.2003;AY095449
AF193987 OD/FBQ/YQDQ008832 BONNAF543721(TB)
Annonaceae:
AnnonamuricataL. Qiu90031;JL/LL/YQ; Qiu90031;OD/FBQ/YQ; K.W.Hilu,K.Mu¨ller,and Sun&An98130,KUN;
DQ008670 DQ008783 T.Borsch,unpublished OD/YQ;DQ008634
manuscript;Borsch3460,
BONNAF543722(KH)
Canangaodorata(Lam.)Hook.f.&Thomson Chase219,NCU;JL/LL/YQ; Chase219,NCU;OD/FBQ/ Borsch&Lo¨hne3555,BONN Chase219,NCU;OD/YQ;
DQ008671 YQ;DQ008784 AY437817 DQ008635
Araceae:
8
1 OrontiumaquaticumL. Qiu97112;JL/LL/YQ; Qiu97112;OD/FBQ/YQ; Hiluetal.2003;Borsch3457, Qiu97112;OD/YQ;
8
DQ008672 DQ008813 BONNAF543744(KH) DQ008652
Spathiphyllum3‘Clevelandii’ Qiu94140;JL/LL/YQ; Qiu94140;OD/FBQ/YQ;
DQ008673 DQ008814
Spathiphyllumfloribundum(Lind.&Andre)N.E.Br. Hiluetal.2003;Borsch3408
BONNAF542575
SpathiphyllumwallisiiHort. Zanisetal.2003;AY095473
Aristolochiaceae:
AristolochiamacrophyllaLam. Qiu91019;JL/LL/YQ; Qiu91019;OD/FBQ/YQ; Zanisetal.2003;AY095450
DQ008674 DQ008796
AristolochiaPistolochiaL. Hiluetal.2003;Borsch3257,
FRAF543724(TB)
AsarumcanadenseL. Kuhlmansn,IND,Qiu Kuhlmansn,IND,Qiu Kuhlmansn,IND,Qiu
96018*;JL/LL/YQ; 96018*;OD/FBQ/YQ; 96018*;OD/YQ;
DQ008676 DQ008799 DQ008643
AsarumyakusimenseMasam. Hiluetal.2003;Hubersn,
BONNAF542571(TB)
SarumahenryiOliv. Qiu91018;JL/LL/YQ; Qiu91018;OD/FBQ/YQ; Murataetal.2001;AB060736 Qiu91018;OD/YQ;
DQ008677 DQ008800 DQ008644
ThotteatomentosaDingHou Chase1211,K;JL/LL/YQ; Chase1211,K;OD/FBQ/YQ; Murataetal.2001;AB060738 Chase1211,K;OD/YQ;
DQ008675 DQ008797 DQ008642
Asparagaceae:
AsparagusofficinalisL. Qiu94063;JL/LL/YQ; Qiu94063;OD/FBQ/YQ; Qiu94063;OD/YQ;
DQ008678 DQ008807 DQ008646
Asparagusfilicinus J.Yamashitaetal.,unpublished
data;AB029805
Atherospermataceae:
AtherospermamoschatumLabill. Qiu92007;JL/LL/YQ; Qiu92007;OD/FBQ/YQ; Qiu92007;Kew;AJ966790 Qiu92007;LL/YQ;
DQ008679 DQ008775 DQ008628
Daphnandramicrantha(Tul.)Benth. Whalen132,NSW;JL/LL/YQ; Whalen132,NSW;OD/FBQ/ Whalen132,NSW;Kew; Whalen132,NSW;OD/YQ;
DQ008680 YQ;DQ008776 AJ966791 DQ008629
DoryphorasassafrasEndl. Qiu98109;JL/LL/YQ; Qiu98109;OD/FBQ/YQ; Hiluetal.2003;Borsch3409, Qiu98109;OD/YQ;
DQ008681 DQ008777 BONNAF542568(TB) DQ008630
Austrobaileyaceae:
AustrobaileyascandensC.T.White Parkinsonetal.1999; Qiu90030;OD/FBQ/YQ; Hiluetal.2003;Borsch3464 Zanisetal.2003;AY095452
AF193988 DQ008827 BONNAF543726(TB)
Berberidaceae:
Mahoniabealei(Fortune)Carr. Qiu74;JL/LL/YQ;DQ008682 Qiu74;OD/FBQ/YQ; Qiu74;OD/YQ;DQ008613
DQ008754
Mahoniajaponica Hiluetal.2003;Borsch3405,
BONNAF542585(TB)
PodophyllumpeltatumL. Qiu92003;JL/LL/YQ; Qiu92003;OD/FBQ/YQ; Hiluetal.2003;Borsch3393, Qiu92003;OD/YQ;
DQ008683 DQ008755 BONNAF542586(TB) DQ008614
Buxaceae:
BuxussempervirensL. Qiu97057;OD/FBQ/YQ; Qiu97057;Kew;AJ966792 S.Kimetal.,unpublisheddata;
DQ008743 AF389243
Buxussp. Parkinsonetal.1999;AF193996
PachysandraprocumbensMichx. Chase207,NCU;JL/LL/YQ; Chase207,NCU;OD/FBQ/ Qiusn,Z(QiuL99028*);
DQ008684 YQ;DQ008742 OD/YQ;DQ008607
PachysandraterminalisSieb.&Zucc. Hiluetal.2003;Borsch3407,
8 BONNAF542581(KH)
1
9 Cabombaceae:
BraseniaschreberiJ.Gmelin Qiu91031;JL/LL/YQ; Qiu91031;OD/FBQ/YQ; Lesetal.1999;AF092973 Qiu91031;LL/YQ;
DQ008685 DQ008830 DQ008661
Cabombasp. Parkinsonetal.1999; Qiu97027;OD/FBQ/YQ;
AF193982; DQ008831
CabombacarolinianaA.Gray Lesetal.1999;AF108719 Soltisetal.2003;AF479239
Calycanthaceae:
CalycanthusfloridusL. Parkinsonetal.1999;AF193989 Qiu94155;OD/FBQ/YQ; K.W.Hilu,K.Mu¨ller,and
DQ008780 T.Borsch,unpublished
manuscript;Borsch3455
BONNAF543730(KH)
CalycanthusoccidentalisHook.&Arn. Zanisetal.2003;AY095454
Chimonanthuspraecox(L.)Link Qiu9;JL/LL/YQ;DQ008686 Qiu9;OD/FBQ/YQ; Hiluetal.2003;Borsch3396, Qiu9;OD/YQ;DQ008632
DQ008781 BONNAF542569(TB)
Canellaceae:
Canellawinterana(L.)Gaertn. Qiu90017;JL/LL/YQ; Qiu90017;OD/FBQ/YQ; K.W.Hilu,K.Mu¨ller,and Zanisetal.2003;AY095455
DQ008687 DQ008804 T.Borsch,unpublished
manuscript;Borsch3466
BONNAF543731(TB)
CinnamodendronekmaniiSleum. Zanoni&Jimenez47067; Zanoni&Jimenez47067; Zanoni&Jimenez47067; Zanoni&Jimenez47067;
JL/LL/YQ;DQ008688 OD/FBQ/YQ;DQ008805 Kew;AJ966793 MZ/DES/PSSAY095458
Table 1
(Continued)
Familyandspecies mt-SSUrDNA mt-LSUrDNA cp-matK nu-26SrDNA
Ceratophyllaceae:
CeratophyllumdemersumL. Parkssn,IND,Qiu95003*; Parkssn,IND,Qiu95003*; Parkssn,IND,Qiu95003*; Zanisetal.2003;AY095456
JL/LL/YQ;DQ008689 OD/FBQ/YQ;DQ008766 Kew;AJ966794
CeratophyllumsubmersumL. Qiu98088;JL/LL/YQ; Qiu98088;OD/FBQ/YQ; Qiu98088;Kew;AJ581400 Qiu98088;OD/YQ;
DQ008690 DQ008767 DQ008622
Chloranthaceae:
AscarinarubricaulisSolms Thien500,NO;JL/LL/YQ; Thien500,NO;OD/FBQ/YQ; Thien500,NOKew; Thien500,NO;OD/YQ;
DQ008691 DQ008821 AJ966795 DQ008656
ChloranthusbrachystachysBl. Hiluetal.2003;Borsch3467
BONNAF543733(KH)
ChloranthusmultistachysPei K.Wurdack92-0010,NCU; K.Wurdack92-0010,NCU; Zanisetal.2003;AY095457
JL/LL/YQ;DQ008692 OD/FBQ/YQ;DQ008819
HedyosmumarborescensSw. Chase338,NCU;JL/LL/YQ; Chase338,NCU;OD/FBQ/ Chase338,NCU;Kew;
DQ008693 YQ;DQ008822 AJ581402
HedyosmumbonplandianumL. Zanisetal.2003;AY095461
SarcandrachloranthoidesGardner Parkinsonetal.1999; Qiu92002;OD/FBQ/YQ; Qiu92002;Kew;AJ966796 Qiu92002;OD/YQ;
AF193992 DQ008820 DQ008655
Cycadaceae:
CycasrevolutaThunb. Chawetal.2000;AB029356 Qiu94051;OD/FBQ/YQ; Qiu94051;OD/YQ;
8 DQ008840 DQ008667
2
0 Cycaspanzhihuaensis Wangetal.2000;AF143440
Cyclanthaceae:
CarludovicapalmataRuiz&Pavon Qiu97021;JL/LL/YQ; Qiu97021;OD/FBQ/YQ; Hiluetal.2003;Rothsn, Qiu97021;OD/YQ;
DQ008694 DQ008809 BONNAF542578(TB) DQ008648
Degeneriaceae:
Degeneriavitensis JMMiller1189-63;JL/LL/YQ; JMMiller1189-63;OD/FBQ/ Azumaetal.,unpublished JMMiller1189-63;OD/YQ;
DQ008695 YQ;DQ008787 data;AB055549 DQ008637
Didymelaceae:
DidymelesperrieriOlivier Andrianantoanina387,MO; Andrianantoanina387,MO; Andrianantoanina387,MO; Andrianantoanina387,MO;
JL/LL/YQ;DQ008696 OD/FBQ/YQ;DQ008744 Kew;AJ581406 OD/YQ;DQ008608
Dioscoreaceae:
Dioscoreasp. Qiu94044;JL/LL/YQ; Qiu94044;OD/FBQ/YQ;
DQ008697 DQ008806
Dioscoreaalata FuseandTamura2000;
AB040208
Eupomatiaceae:
EupomatiabennettiiF.Muell. Qiu90022;JL/LL/YQ; Qiu90022;OD/FBQ/YQ; Qiu90022;Kew;AJ966797 Qiu90022;OD/YQ;
DQ008698 DQ008785 DQ008636
Eupteleaceae:
EupteleapolyandraSieb.&Zucc. Parkssn,IND,Qiu95098*; Parkssn,IND,Qiu95098*; Parkssn,IND,Qiu95098*; Zanisetal.2003;AF389249
JL/LL/YQ;DQ008699 OD/FBQ/YQ;DQ008763 Kew;AJ581413
Fumariaceae:
Dicentrasp. Qiu95026;JL/LL/YQ; Qiu95026;OD/FBQ/YQ; Qiu95026;Kew;AJ966798
DQ008700 DQ008764
DicentraeximaTorrey Zanisetal.2003;AF389262
Ginkgoaceae:
GinkgobilobaL. Chawetal.2000;AB029355 Qiu94015;OD/FBQ/YQ; Hiluetal.2003;Borsch3469 Qiu94015;OD/YQ;
DQ008838 BONNAF543736(KH) DQ008665
Gnetaceae:
GnetumgnemonL. Qiu97141;JL/LL/YQ; Qiu97141;OD/FBQ/YQ; Hiluetal.2003;Borsch3470 Kuzoffetal.1998;AF036488
DQ008701 DQ008833 BONNAF542561(KH)
Gyrocarpaceae:
GyrocarpusamericanaJacq. Chase317,NCU;JL/LL/YQ; Chase317,NCU;OD/FBQ/ Chase317,NCU;Kew; Chase317,NCU;OD/YQ;
DQ008702 YQ;DQ008770 AJ581417 DQ008624
Hernandiaceae
Hernandianymphaeifolia(Presl)Kub. Zanisetal.2003;AY095462
HernandiaovigeraL. Qiu01007;JL/LL/YQ; Qiu01007;OD/FBQ/YQ; Qiu01007;Kew;AJ966799
DQ008703 DQ008771
Himantandraceae:
Galbulimimabelgraveana(F.Muell.)Sprague Weston929,NSW;JL/LL/YQ; Weston929,NSW;OD/FBQ/ Weston929,NSW;Kew; Zanisetal.2003;AY095459
DQ008704 YQ;DQ008788 AF465294
Idiospermaceae:
Idiospermumaustraliense(Diels)S.T.Blake Qiu91042;JL/LL/YQ; Qiu91042;OD/FBQ/YQ; Qiu91042;Kew;AJ581425 Qiu91042;OD/YQ;
DQ008705 DQ008782 DQ008633
Illiciaceae:
IlliciumfloridanumEllis Qiu61;JL/LL/YQ;DQ008706 Qiu61;OD/FBQ/YQ; K.W.Hilu,K.Mu¨ller,and Qiu61;OD/YQ;DQ008659
DQ008825 T.Borsch,unpublished
manuscript;Borsch3552,
BONNAF543738(TB)
8 Juncaginaceae:
21 TriglochinmaritimaL. Qiu97106;JL/LL/YQ; Qiu97106;OD/FBQ/YQ; Hiluetal.2003Borsch3392 Qiu97106;LL/YQ;
DQ008707 DQ008811 BONNAF542566(TB) DQ008650
Lactoridaceae:
LactorisfernandezianaPhil. Chase1014,K;JL/LL/YQ; Chase1014,K;OD/FBQ/YQ; L.W.Chatrouetal., Zanisetal.2003;AY095463
DQ008708 DQ008798 unpublisheddata;AF465297
Lardizabalaceae:
AkebiaquinataDecne. Qiu91020;JL/LL/YQ; Qiu91020;OD/FBQ/YQ; Hiluetal.2003;Borsch3412 Qiu91020;OD/YQ;
DQ008709 DQ008761 BONNAF542587(TB) DQ008619
LardizabalabiternataRuiz&Pavon Qiu97135;JL/LL/YQ; Qiu97135;OD/FBQ/YQ; Qiu97135;TB/KH;AY437809 Qiu97135;OD/YQ;
DQ008710 DQ008760 DQ008618
Lauraceae:
Cinnamomumcamphora(L.)T.Nees&Eberm. Qiu102;JL/LL/YQ;DQ008711 Qiu102;OD/FBQ/YQ; Qiu102;Kew;AJ966800 Qiu102;OD/YQ;DQ008625
DQ008772
Cryptocaryaalba(Molina)Looser Rohwer2000;AJ247158
CryptocaryameisnerianaFrodin Qiu98048;JL/LL/YQ; Qiu98048;OD/FBQ/YQ; Qiu98048;OD/YQ;
DQ008712 DQ008774 DQ008627
LaurusnobilisL. Parkinsonetal.1999; Qiu94209;OD/FBQ/YQ; Qiu94209;Kew;AJ966801 Qiu94209;OD/YQ;
AF193990 DQ008773 DQ008626
Magnoliaceae:
Liriodendronchinense(Hemsl.)Sarg. Parkinsonetal.1999;AF193993 Qiu28;OD/FBQ/YQ; Zanisetal.2003;AY095464
DQ008786
LiriodendrontulipiferaL. Azumaetal.1999;AB021016
MagnoliadenudataDesr. Zanisetal.2003;AF389256
MagnoliagrandifloraL. Chawetal.2000;AF161089
Table 1
(Continued)
Familyandspecies mt-SSUrDNA mt-LSUrDNA cp-matK nu-26SrDNA
MagnoliatripetalaL. Qiu3;OD/FBQ/YQ; Azumaetal.1999;AB021001
DQ008741
Menispermaceae:
CissampelospareiraL. Chase347,NCU;JL/LL/YQ; Chase347,NCU;OD/FBQ/ Chase347,NCU;Kew; Chase347,NCU;OD/YQ;
DQ008713 YQ;DQ008758 AJ966802 DQ008616
Cocculustrilobus(Thunb.)DC Qiu91016;JL/LL/YQ; Qiu91016;OD/FBQ/YQ; Qiu91016;OD/YQ;
DQ008714 DQ008759 DQ008617
CocculuslaurifoliusDC. Hiluetal.2003;Borsch3406
BONNAF542588(TB)
Monimiaceae:
HedycaryaarboreaJ.R.&G.Forst. Qiu90028;JL/LL/YQ; Qiu90028;OD/FBQ/YQ; Qiu90028;Kew;AJ581436 Qiu90028;LL/YQ;
DQ008716 DQ008769 DQ008623
HortoniafloribundaWightexArn. Qiu02002*;JL/LL/YQ; Qiu02002*;OD/FBQ/YQ; Qiu02002*;TB;AY437811 Zanisetal.2003;AF264143
DQ008717 DQ008778
PeumusboldusMolina EdinburghBG19870707; EdinburghBG19870707; Rohwer2000;AJ247183 Zanisetal.2003;AY095466
JL/LL/YQ;DQ008715 OD/FBQ/YQ;DQ008768
Myristicaceae:
MauloutchiachapelieriWarb. Schatz3847A,MO;JL/LL/YQ; Schatz3847A,MO;OD/FBQ/ Schatz3847A,MO;TB; Schatz3847A,MO;OD/YQ;
DQ008719 YQ;DQ008790 AY437812 DQ008638
MyristicafragransHoutt. Qiu92014;JL/LL/YQ; Qiu92014;OD/FBQ/YQ; Qiu92014;Kew;AJ966803
8
22 DQ008718 DQ008789
Nelumbonaceae:
Nelumbolutea(Willd.)Pers. Zanisetal.2003;AF389259
NelumbonuciferaGaertner Parkinsonetal.1999; Qiu91028;OD/FBQ/YQ; K.W.Hilu,K.Mu¨ller,and
AF193983 DQ008753 T.Borsch,unpublished
manuscript;Borsch&
Summers3220,
FRAF543740(TB)
Nymphaeaceae:
Nupharsp. Parkinsonetal.1999; QiuM114;OD/FBQ/YQ; QiuM114;LL/YQ;
AF193981 DQ008829 DQ008660
NupharluteaL. Hiluetal.2003;Borsch3337,
FRAF543741(TB)
Nymphaeasp. Chawetal.2000;AF161091 Qiu91029;OD/FBQ/YQ; Zanisetal.2003;AY095465
DQ008828
NymphaeaodorataAiton Hiluetal.2003;Borsch&
Wilde3132,VPI&BONN
AF543742(TB)
Papaveraceae:
SanguinariacanadensisL. Qiu91032;JL/LL/YQ; Qiu91032;OD/FBQ/YQ; Qiu91032;Kew;AJ966804 Qiu91032;OD/YQ;
DQ008720 DQ008765 DQ008621
Pinaceae:
Pinussp. Qiu94013;JL/LL/YQ; Qiu94013;OD/FBQ/YQ;
DQ008721 DQ008835
PinusdouglasianaMartinez L.G.Geadaetal.,unpublished
data;AB063520
PinuswallichianaA.B.Jackson I.Capesius,unpublisheddata;
AJ271114
Piperaceae:
PeperomiagraveolensRauh&Barthlott Hiluetal.2003;Prinslers.n.
BONNAF542574(TB)
Peperomiaobtusifolia Qiu94135; Qiu94135; Qiu94135;
A.Dietr. JL/LL/YQ;DQ008722 OD/FBQ/YQ;DQ008794 LL/YQ;DQ008641
PiperbetleL. Chawetal.2000;AF161088 Qiu91048;OD/FBQ/YQ; Zanisetal.2003;AY095467
DQ008795
PipercrocatumR.&P. Hiluetal.2003;Slottas.n.,
VPIAF543745(KH)
Platanaceae:
PlatanusoccidentalisL. Chawetal.2000;AF161090 Qiu94152;OD/FBQ/YQ; K.W.Hiluetal.,unpublished Fishbeinetal.2001;AF274662
DQ008752 data;AF543747
Podocarpaceae:
PodocarpuscostalisPresl Chawetal.2000;AF029369
Podocarpusmacrophyllus(Thunb.)Sweet Qiu95006;OD/FBQ/YQ; WangandShu2000; Qiu95006;OD/YQ;
DQ008837 AF228111 DQ008664
Potamogetonaceae:
PotamogetonberchtoldiiFieber Qiu96063;JL/LL/YQ; Qiu96063;OD/FBQ/YQ; Qiu96063;OD/YQ;
DQ008723 DQ008810 DQ008649
PotamogetondistinctusArth.Benn. Tanakaetal.1997;AB002581
Proteaceae:
GrevilleabanksiiR.Br. Hiluetal.2003;Borsch3413
8 BONNAF542583(TB)
23 GrevillearobustaCunn.&R.Br. Parkinsonetal.1999; Qiu94087;OD/FBQ/YQ; Qiu94087;OD/YQ;
AF193995 DQ008751 DQ008612
PersooniakateraeP.Weston&L.Johnson Weston1120,NSW;JL/LL/YQ; Weston1120,NSW;OD/FBQ/ Weston1120,NSW;TB; Weston1120,NSW;OD/YQ;
DQ008724 YQ;DQ008750 AY437813 DQ008611
PetrophilecanescensCunn.exR.Br. Qiu98018;JL/LL/YQ; Qiu98018;OD/FBQ/YQ; Qiu98018;Kew;AJ966805 Qiu98018;OD/YQ;
DQ008725 DQ008749 DQ008610
Ranunculaceae:
Ranunculussp. Chawetal.2000;AF161093 Qiu95024;OD/FBQ/YQ;
DQ008756
RanunculusficariaL. Borsch3554BONN;TB;
AY437814
RanunculuskeniensisMilne-Redhead&Turrill Zanisetal.2003;AF389269
XanthorhizasimplicissimaMarshall Qiu91030;JL/LL/YQ; Qiu91030;OD/FBQ/YQ; Hiluetal.2003;Borsch3394 Qiu91030;OD/YQ;
DQ008726 DQ008757 BONNAF542567(TB) DQ008615
Sabiaceae:
Sabiasp. Qiu91025;JL/LL/YQ; Qiu91025;OD/FBQ/YQ; Qiu91025;Kew;AJ966806
DQ008727 DQ008747
SabiaswinhoeiHemsl. Zanisetal.2003;AF389272
MeliosmasquamulataHance B.Shih3749,HAST;JL/LL/YQ; B.Shih3749,HAST;OD/FBQ/ B.Shih3749,HAST;OD/YQ;
DQ008728 YQ;DQ008748 DQ008609
MeliosmaveitchiorumHemsl. Chase2989,K;Kew;AJ581449
Sargentodoxaceae:
Sargentodoxacuneata(Oliv.)Rehder&Wilson Pan93001,NCU;JL/LL/YQ; Pan93001,NCU;OD/FBQ/ Pan93001,NCU;Kew; Pan93001,NCU;OD/YQ;
DQ008729 YQ;DQ008762 AJ966807 DQ008620