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The origin and diversification of angiosperms

October 2004
American Journal of Botany 9(10):1614-1626

October 2004
9(10):1614-1626

DOI:10.3732/ajb.91.10.1614

Authors:

Pamela S Soltis

University of Florida

Douglas E Soltis

University of Florida

The angiosperms, one of five groups of extant seed plants, are the largest group of land plants. Despite their relatively recent origin, this clade is extremely diverse morphologically and ecologically. However, angiosperms are clearly united by several synapomorphies. During the past 10 years, higher-level relationships of the angiosperms have been resolved. For example, most analyses are consistent in identifying Amborella, Nymphaeaceae, and Austrobaileyales as the basalmost branches of the angiosperm tree. Other basal lineages include Chloranthaceae, magnoliids, and monocots. Approximately three quarters of all angiosperm species belong to the eudicot clade, which is strongly supported by molecular data but united morphologically by a single synapomorphy-triaperturate pollen. Major clades of eudicots include Ranunculales, which are sister to all other eudicots, and a clade of core eudicots, the largest members of which are Saxifragales, Caryophyllales, rosids, and asterids. Despite rapid progress in resolving angiosperm relationships, several significant problems remain: (1) relationships among the monocots, Chloranthaceae, magnoliids, and eudicots, (2) branching order among basal eudicots, (3) relationships among the major clades of core eudicots, (4) relationships within rosids, (5) relationships of the many lineages of parasitic plants, and (6) integration of fossils with extant taxa into a comprehensive tree of angiosperm phylogeny.

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American Journal of Botany 91(10): 1614–1626. 2004.

HE ORIGIN AND DIVERSIFICATION OF ANGIOSPERMS

AMELA

S. S

OLTIS

2,4

AND

OUGLAS

E. S

OLTIS

Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA; and

Department of Botany, University

of Florida, Gainesville, Florida 32611 USA

The angiosperms, one of ﬁve groups of extant seed plants, are the largest group of land plants. Despite their relatively recent origin,

this clade is extremely diverse morphologically and ecologically. However, angiosperms are clearly united by several synapomorphies.

During the past 10 years, higher-level relationships of the angiosperms have been resolved. For example, most analyses are consistent

in identifying Amborella, Nymphaeaceae, and Austrobaileyales as the basalmost branches of the angiosperm tree. Other basal lineages

include Chloranthaceae, magnoliids, and monocots. Approximately three quarters of all angiosperm species belong to the eudicot clade,

which is strongly supported by molecular data but united morphologically by a single synapomorphy—triaperturate pollen. Major

clades of eudicots include Ranunculales, which are sister to all other eudicots, and a clade of core eudicots, the largest members of

which are Saxifragales, Caryophyllales, rosids, and asterids. Despite rapid progress in resolving angiosperm relationships, several

signiﬁcant problems remain: (1) relationships among the monocots, Chloranthaceae, magnoliids, and eudicots, (2) branching order

among basal eudicots, (3) relationships among the major clades of core eudicots, (4) relationships within rosids, (5) relationships of

the many lineages of parasitic plants, and (6) integration of fossils with extant taxa into a comprehensive tree of angiosperm phylogeny.

Key words: Amborella; angiosperms; phylogeny.

The angiosperms, or ﬂowering plants, one of the major

clades of extant seed plants (see Burleigh and Mathews, 2004,

in this issue), are the largest group of embryophytes, with at

least 260000 living species classiﬁed in 453 families (APG II,

2003). Angiosperms are amazingly diverse. They occupy ev-

ery habitat on Earth except the highest mountaintops, the re-

gions immediately surrounding the poles, and the deepest

oceans, and they occur as epiphytes, ﬂoating and rooted aquat-

ics in both freshwater and marine habitats, and terrestrial

plants that vary tremendously in size, longevity, and overall

form. Furthermore, the diversity in chemistry, reproductive

morphology, and genome size and organization is unparalleled

in the Plant Kingdom.

Despite their diversity, angiosperms are clearly united by a

suite of synapomorphies (i.e., shared, derived features), in-

cluding double fertilization and endosperm formation, the car-

pel, stamens with two pairs of pollen sacs, features of game-

tophyte structure and development, and phloem tissue com-

posed of sieve tubes and companion cells (see Doyle and Don-

oghue, 1986; and P. Soltis et al., 2004, for further discussion).

This evidence strongly negates hypotheses of polyphyletic or-

igins of extant angiosperms.

The fossil record of the angiosperms extends back at least

to the early Cretaceous, conservatively 130 million years ago

(mya) (see Crane et al., 2004). Floral size, structure, and or-

ganization among early angiosperms varied tremendously,

ranging from small (i.e., ,1 cm in diameter) ﬂowers of fossil

Chloranthaceae and many other lineages (reviewed in Friis et

al., 2000), both extant and extinct, to the large, Magnolia-like

ﬂowers of Archaeanthus (Dilcher and Crane, 1984). This ﬂoral

diversity in the fossil record is consistent with an early radi-

ation of angiosperms and associated diversiﬁcation in ﬂoral

form (e.g., Friis et al., 2000).

Large-scale collaborations among angiosperm systematists

have greatly improved our understanding of angiosperm phy-

Manuscript received 6 February 2004; revision accepted 1 July 2004.

The authors thank M. Chase, J. Palmer, and an anonymous reviewer for

very helpful comments on the manuscript. This research was supported in

part by NSF grants DEB-0090283 and PGR-0115684.

E-mail: psoltis@ﬂmnh.uﬂ.edu.

logeny. Strong support for many clades that correspond to tra-

ditionally recognized families provided early conﬁdence that

the molecular-based trees were producing reasonable recon-

structions of phylogeny. However, some traditional families

and many orders and higher groups have been shown to be

nonmonophyletic, while many groups of previously uncertain

placement have been placed with great conﬁdence. The An-

giosperm Phylogeny Group, an international consortium of

systematists, recognized the need for a new classiﬁcation that

reﬂects current views of angiosperm phylogeny (APG, 1998;

APG II, 2003). An abridged version of the classiﬁcation is

given in Appendix 1 (see Supplemental Data accompanying

online version of this paper) and at the Deep Time website

(http://ﬂmnh.uﬂ.edu/deeptime).

In this paper, we provide a brief overview of angiosperm

phylogeny as currently understood (Fig. 1) and examine pat-

terns of angiosperm diversiﬁcation. The monocot and eudicot

clades will be considered in greater detail in the accompanying

papers by Chase (2004) and Judd and Olmstead (2004), re-

spectively.

ANGIOSPERM PHYLOGENY

The root of the tree—A mere decade ago, the possibility

of identifying the basal nodes of the angiosperm clade seemed

remote. However, most analyses of the past ﬁve years concur

in placing the monotypic Amborella as the sister to all other

extant angiosperms. Amborella trichopoda, endemic to cloud

forests of New Caledonia, was described in the mid-nineteenth

century (Baillon, 1869) and has since been classiﬁed with var-

ious groups of basal angiosperms, most often with Laurales

(e.g., Cronquist, 1981). However, Amborella clearly differs

from most Laurales in having spirally arranged ﬂoral organs

(except perhaps the carpels; Buzgo et al., in press), rather than

the whorled phyllotaxis typical of most Laurales (see studies

of ﬂoral morphology and development by Endress and Iger-

sheim, 2000b; Posluszny and Tomlinson, 2003; Buzgo et al.,

in press), and lacks those features considered to be synapo-

morphies for Laurales (Doyle and Endress, 2000; see Laurales

later). Amborella has carpels that are closed only by secretion,

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Fig. 1. Overview of angiosperm phylogenetic relationships, based on Qiu

et al. (1999), P. Soltis et al. (1999), D. Soltis et al. (2000, 2003), Zanis et al.

(2002), Hilu et al. (2003), Kim et al. (2004b).

rather than by fused tissue as in most angiosperms (Endress

and Igersheim, 2000a)—a feature that may represent a ple-

siomorphy (i.e., ancestral feature) for the angiosperms. Vessels

(Judd et al., 2002; but see Feild et al., 2000; Doyle and En-

dress, 2000) and pollen grains with a reticulate tectum (Doyle

and Endress, 2001) appear to be synapomorphies for all extant

angiosperms except Amborella. Ethereal oil cells—common

throughout basal angiosperms—and columellate pollen grains

with a perforate tectum are synapomorphies for all extant an-

giosperms except Amborella and Nymphaeaceae (Doyle and

Endress, 2001).

The evidence for Amborella—Nearly all multigene analyses

of basal angiosperms have identiﬁed Amborella as the sister

to all other extant angiosperms (e.g., Mathews and Donoghue,

1999, 2000; Parkinson et al., 1999; Qiu et al., 1999; P. Soltis

et al., 1999; Graham and Olmstead, 2000; Graham et al., 2000;

D. Soltis et al., 2000; Magallo´n and Sanderson, 2001; Zanis

et al., 2002; see also Nickerson and Drouin, 2004), with vary-

ing levels of support. The genes that support this position

come from all three plant genomes and represent relatively

‘‘slowly evolving’’ protein-coding and ribosomal RNA genes.

Furthermore, analyses of the ‘‘rapidly evolving’’ plastid gene

matK (Hilu et al., 2003) and mostly noncoding trnL-trnF

(Borsch et al., 2003) each showed these same results. In all of

these studies, Nymphaeaceae and Austrobaileyales (both sensu

the Angiosperm Phylogeny Group, APG II, 2003) ‘‘followed’’

Amborella as successive sisters to the remaining extant angio-

sperms. Furthermore, the structural organization of the ﬂoral

MADS-box genes Apetala3 and Pistillata also supported the

position of Amborella and Nymphaeaceae as sisters to all other

extant angiosperms, and analyses of nucleotide and amino acid

sequences of these genes also placed Amborella, either alone

or with Nymphaeaceae, in this position (Kim et al., in press).

Alternative views—Despite general support for the place-

ment of Amborella as sister to the rest of the extant angio-

sperms, a few studies have found alternative rootings, using

either different genes or different methods of analysis. For

example, Amborella 1 Nymphaeaceae (e.g., Parkinson et al.,

1999; Barkman et al., 2000; Mathews and Donoghue, 2000;

Qiu et al., 2000; P. Soltis et al., 2000; Kim et al., in press) or

Nymphaeaceae alone (e.g., Parkinson et al., 1999; Graham and

Olmstead, 2000, with partial sampling of Nymphaeaceae; Ma-

thews and Donoghue, 2000) have occasionally been reported

as sister to all other angiosperms. However, statistical analyses

of these alternative rootings using a data set of up to 11 genes

generally favor the tree with Amborella as sister to the rest,

although the Amborella 1 Nymphaeaceae tree could not al-

ways be rejected (Zanis et al., 2002). Nearly all of these stud-

ies are consistent in noting that conﬂicting topologies are not

strongly supported. Furthermore, the difference among these

three topologies is relatively minor and consists solely of the

relative placement of Amborella and Nymphaeaceae.

A more dramatic alternative, based on a selection of 61

genes from the totally sequenced plastid genomes of 13 plant

species, placed the monocots (represented only by three grass-

es—rice, maize, and wheat) as the sister to all other extant

angiosperms (Goremykin et al., 2003). Whereas all molecular

analyses of angiosperms with dense taxon sampling strongly

supported monophyly of the monocots and most placed this

clade among the basal nodes of the angiosperm tree, none has

indicated that monocots are sister to all other extant angio-

sperms. In the analysis by Goremykin et al. (2003), Amborella

was sister to Calycanthus of Laurales, a position consistent

with the original description of Amborella, but clearly at odds

with other aspects of morphology (see Laurales section). Go-

remykin et al. (2003) attributed their results to the increased

character sampling (30017 nucleotides in their aligned matrix)

in their study relative to other analyses that included fewer

genes but many more taxa. However, further analyses of a data

set of three genes and nearly equivalent taxon sampling indi-

cated that the ‘‘monocots basal’’ topology is an artifact of lim-

ited taxon sampling (Soltis and Soltis, 2004). When either

Nymphaea or Austrobaileya, representing Nymphaeaceae and

Austrobaileyales, respectively, was substituted for Amborella,

each appeared as the sister to Calycanthus, in exactly the same

position that Amborella had occupied, presumably because the

data set, which was limited to a subset of those plant species

for which entire plastid genome sequences are available, con-

tained no other close relatives. Furthermore, representing

monocots by taxa other than grasses, which reside at the end

of a long branch (e.g., Gaut et al., 1992, 1996; Chase et al.,

2000), broke up the long branch to the monocots and resulted

in the ‘‘Amborella basal’’ topology. Likewise, broader sam-

pling of the monocots beyond grasses (the sole monocots in-

cluded by Goremykin et al., 2003) also severed the long mono-

cot branch and yielded the ‘‘Amborella basal’’ tree. Finally,

when plastid sequences of the monocot Acorus were added to

the data set of Goremykin et al., also disrupting the long branch

to the grasses, Amborella resumed its position as sister to the

other angiosperms (S. Stefanovic et al., Indiana University,

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Fig. 2. Summary of phylogenetic relationships among clades of basal an-

giosperms, based primarily on Zanis et al. (2002).

unpublished data). Although increasing the number of char-

acters will generally lead to greater accuracy (Hillis, 1996) and

support (e.g., Givnish and Sytsma, 1997; Soltis et al., 1998),

the increase in characters cannot come at the expense of ad-

equate taxon sampling (e.g., Chase et al., 1993; Sytsma and

Baum, 1996; Zwickl and Hillis, 2002; Pollock et al., 2002;

Soltis et al., in press-a). Limited taxon sampling, such as that

dictated by the small number of organisms with complete ge-

nome sequences, may lead to artifacts, as apparently occurred

in the analysis by Goremykin et al. (2003).

The fossil record—The fossil record does not clarify basal

groups within the angiosperms. However, it clearly identiﬁes

a number of morphologically diverse lineages early in angio-

sperm evolution (e.g., Crane et al., 1995; Friis et al., 2000).

Although some of these early fossils seem to belong to extant

families, many do not ﬁt easily into extant groups. For ex-

ample, two species of Archaefructus (Sun et al., 1998, 2002)

may be the sister to all other angiosperms (Sun et al., 2002),

although a reanalysis of their data, with the inclusion of ad-

ditional material, indicated alternative placements (Friis et al.,

2003). Notably, with regard to the plastid topology of Gore-

mykin et al. (2003), the monocots are not among the earliest

angiosperm fossils, although both the fossil record (Gandolfo

et al., 2002) and molecular clock estimates (K. Bremer, 2000;

Wikstro¨m et al., 2001; Davies et al., 2004) have indicated that

many lineages of monocots date back at least 80–100 mya.

However, Nymphaeaceae are among the earliest angiosperm

fossils: a water lily from approximately 125 mya (Friis et al.,

2001) is consistent with the basal or near-basal position of the

Nymphaeaceae branch in most molecular-based trees, and the

ﬂoral features of Microvictoria (90 mya; Gandolfo et al., 2004)

provide evidence of beetle entrapment pollination in early an-

giosperms. Likewise, the abundance of fossils of Chlorantha-

ceae and Ceratophyllaceae from the early Cretaceous (e.g.,

Couper, 1958; Walker and Walker, 1984; Dilcher, 1989; Friis

et al., 2000; see Endress, 2001, for review) is also consistent

with the placement of these clades among extant angiosperms

in molecular-based trees (Figs. 1, 2).

Basal lineages—The positions of Amborellaceae and Nym-

phaeaceae as successive sisters to the rest of the angiosperms

are followed in turn by Austrobaileyales. Although these ﬁrst

three nodes are well supported (e.g., Zanis et al., 2002; Hilu

et al., 2003), resolution and support for relationships of the

next few nodes are poor (Fig. 2). Ceratophyllaceae, monocots,

Chloranthaceae, magnoliids, and eudicots are each well sup-

ported, and both the fossil record and molecular-based trees

identify these lineages as ancient. However, their interrelation-

ships remain unclear. It is clear, however, that angiosperms do

not fall into two major groups that correspond to monocots

(Liliopsida) and dicots (Magnoliopsida) of longstanding clas-

siﬁcation systems (such as Cronquist, 1981; Takhtajan, 1997,

and their predecessors). Although monocots clearly form a

strongly supported clade, dicots in the traditional sense do not:

most are found in the eudicot clade, but the remaining non-

monocot basal branches (i.e., Amborellaceae, Nymphaeaceae,

Austrobaileyales, Ceratophyllaceae, Chloranthaceae, magno-

liids) were also ‘‘traditional’’ dicots. The nonmonophyly of the

dicots has long been suspected, and the lack of monophyly

precludes their recognition in current classiﬁcations (e.g., APG

II, 2003). The concept of ‘‘dicot’’ should be abandoned in

favor of eudicots, with recognition that considerable diversity

exists outside the monocot and eudicot clades.

Nymphaeaceae—The phylogenetic position of Nymphae-

aceae as one of the two basalmost lineages of extant angio-

sperms is strongly supported by nearly all molecular analyses.

This clade of eight genera has a worldwide distribution, con-

sistent with both the ancient age of this lineage and aquatic

habitats. Although all genera occupy aquatic habitats, these

habitats range from temperate to tropical. Floral diversity

among genera is extensive, ranging from the small, simple,

trimerous, monocot-like ﬂowers of Cabomba to the large,

showy, elaborate ﬂowers of Nymphaea and Victoria. Although

the latter were considered ‘‘primitive’’ by most authors,

Schneider (1979) suggested that the numerous ﬂoral organs of

Nymphaea and Victoria resulted from secondary increase.

Phylogenetic analyses (Les et al., 1999) and character recon-

structions (Ronse DeCraene et al., 2003; Soltis et al., in press-

b) supported Schneider’s (1979) hypothesis. Floral diversiﬁ-

cation in Nymphaeacae may be related to changes in pollina-

tion: proliferation of parts in response to beetle pollination in

Nymphaea and Victoria and a reduction in number of parts

associated with a shift to cleistogamy in Euryale (Gottsberger,

1977, 1978; Williams and Schneider, 1993; Lipok et al., 2000).

Austrobaileyales—This small clade comprises Austrobail-

eyaceae (Austrobaileya) and Trimeniaceae (Trimenia) from

Australasia plus Schisandraceae sensu APG II (2003), i.e.,

Schisandraceae (Schisandra and Kadsura) and Illiciaceae (Il-

licium) of most other recent classiﬁcations (Qiu et al., 1999;

Renner, 1999; Savolainen et al., 2000a, b; P. Soltis et al., 1999;

D. Soltis et al., 2000). Although the traditional Illiciaceae and

Schisandraceae have typically been united in Illiciales, a re-

lationship between these taxa and Austrobaileya and Trimenia

had not been suspected. No morphological synapomorphies

have been identiﬁed for this clade, despite the strong molec-

ular support for its monophyly.

Ceratophyllaceae—Ceratophyllaceae (Ceratophyllum) had

the distinction of appearing as the sister to all other angio-

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sperms in the ﬁrst large molecular phylogenetic analysis based

on rbcL (Chase et al., 1993). The aquatic habit and simple

ﬂowers seemed at odds with most hypotheses about the earliest

angiosperms, although Ceratophyllum has a long fossil record,

going back at least 125 mya (Dilcher, 1989). Subsequent anal-

yses demonstrated that this placement was unique to the rbcL

data set, but the position of Ceratophyllum, based on evidence

from many other genes, is still not clear. It appears as the sister

to monocots in some analyses (e.g., Zanis et al., 2002; Davies

et al., 2004), but further work is needed to identify its proper

position.

Monocots—Among extant angiosperms, monocotyledons

represent the earliest-appearing major clade. Using a molecular

clock, K. Bremer (2000) dated the origin of the monocot clade

to be 134 mya, older than the oldest angiosperm fossils. Al-

though their exact age is unclear from the fossil record (but

see Gandolfo et al., 2002), monocots clearly represent an early

lineage of angiosperms. There are approximately 52000 spe-

cies of monocots (Mabberley, 1993), representing 22% of all

angiosperms. Half of the monocots can be found in the two

largest families, Orchidaceae and Poaceae, which comprise

34% and 17%, respectively, of all monocots.

Phylogenetic studies of nonmolecular data (Donoghue and

Doyle, 1989; Loconte and Stevenson, 1991; Doyle and Don-

oghue, 1992) have identiﬁed 13 putative synapomorphies for

the monocots, including, among others, a single cotyledon,

parallel-veined leaves, sieve cell plastids with several cuneate

protein crystals, scattered vascular bundles in the stem, and an

adventitious root system. An often-overlooked synapomorphy

for monocots is their sympodial growth; although there are

other angiosperms with sympodial growth, monocots are near-

ly exclusively so. These synapomorphies are covered in detail

in the paper by Chase in this issue (2004; see also Judd et al.,

2002; Soltis et al., in press-b).

Recognition of the monocots as a distinct group within the

angiosperms dates from Ray (1703) and was largely based on

their possession of a single cotyledon relative to the two cot-

yledons typical of the dicotyledons or ‘‘dicots.’’ As reviewed

earlier, the latter group is now known to be nonmonophyletic,

and the term ‘‘dicot’’ should be abandoned. There is, however,

a great diversity of form in monocot seedlings (Tillich, 1995)

and not all possess an obvious single cotyledon.

Another major, distinctive trait of the monocots is their vas-

cular system, which is characterized by vascular bundles that

are scattered throughout the medulla and cortex and are closed

(i.e., do not contain an active cambium; reviewed in Tomlin-

son, 1995). In contrast, basal angiosperms formerly considered

dicots (e.g., members of the magnoliid clade) and eudicots

possess open vascular bundles arranged in a ring.

Another widely cited character of the monocots is their par-

ticular form of sieve cell plastids (Behnke, 1969), which are

triangular with cuneate proteinaceous inclusions. Similar sieve

cell plastids are found in Aristolochiaceae (Dahlgren et al.,

1985). This similarity between monocots and Aristolochiaceae

apparently represents convergence, not shared ancestry, be-

cause phylogenetic studies of DNA sequences from all three

genomes (Qiu et al., 1999; Zanis et al., 2002, 2003) have dem-

onstrated a strongly supported relationship of Aristolochiaceae

to other Piperales within the magnoliid clade.

Other traits characteristic of the monocots include parallel

venation without free vein-endings (vs. reticulate venation

with free vein-endings), intercalary meristem, adventitious

roots, and roots without secondary growth. Adventitious roots

are found elsewhere in the angiosperms, in both Piperaceae

and Nymphaeaceae.

Trimerous ﬂowers have long been considered a uniting fea-

ture of the monocots, but it is not an exclusive one because

there are many other basal angiosperms, including Nymphae-

aceae and magnoliids, that also exhibit trimery. In fact, char-

acter-state reconstructions of the angiosperms indicate that tri-

mery arose early in the angiosperms; it may be ancestral for

all angiosperms except Amborella (Ronse De Craene et al.,

2003; Zanis et al., 2003; Soltis et al., in press-b), or perhaps

all angiosperms, if the shift away from trimery in Amborella

occurred along the lineage leading to Amborella. Trimery ap-

pears, therefore, to be a symplesiomorphic feature for mono-

cots and other angiosperms and is not a ‘‘monocot character.’’

Our understanding of monocot phylogenetics has greatly

improved over the past decade, aided greatly by the foci pro-

vided by the international monocot symposia held in 1993,

1998, and 2003. These meetings have focused attention both

on what was known and, more importantly, on which groups

needed additional research. As a result, we now know more

about monocots than any other group of angiosperms of com-

parable size, a situation that is remarkable given the paucity

of information available in 1985 (Dahlgren et al., 1985). This

model should be adopted for the other large groups of angio-

sperms (e.g., rosids, asterids) so that attention is likewise fo-

cused on integration of research programs and gaps in the

database.

There have been several recent analyses of relationships

among the monocots, including the three-gene analyses of

Chase et al. (2000) and D. Soltis et al. (2000) and the seven-

gene analysis of Chase et al. (in press). The ﬁrst two studies

are based on the same three genes (rbcL, atpB, 18S rDNA);

however, Chase et al. (2000) focused only on the monocots

and employed a larger number of taxa than used in D. Soltis

et al. (2000). The analysis by Chase et al. (2004) included

those three genes, plus partial nuclear 26S rDNA, plastid matK

and ndhF, and mitochondrial atpA. The paper in this issue by

Chase (2004) provides greater detail on monocot phylogeny,

and our coverage will therefore be brief.

All but two molecular phylogenetic analyses of monocots

have placed Acorus alone as sister to all other monocots. The

ﬁrst exception to this statement was the 18S rDNA analysis

of Bharathan and Zimmer (1995), in which Acorus was placed

outside of the monocots altogether, a result that has to be con-

sidered spurious. Combination of 18S rDNA sequence data

with sequences from rbcL and atpB (Chase et al., 2000; D.

Soltis et al., 2000) resulted in strong support for the mono-

phyly of monocots, as well as strong support for the mono-

phyly of all monocots excluding Acorus. A recent analysis of

two of the seven genes used in Chase et al. (in press), rbcL

and atpA (Davis et al., in press), retrieved an alismatid clade

that included Acorus. This deviating result is perplexing be-

cause neither rbcL (Chase et al., 1993; Duvall et al., 1993)

nor atpA (Davis et al., 1998) analyzed alone produced such a

position for Acorus. In contrast, studies of basal angiosperm

relationships that have employed more genes (six to 11) have

consistently found Acorus sister to the remaining monocots

with strong support (e.g., Qiu et al., 1999, 2000; Zanis et al.,

2002, 2003). A recent angiosperm-wide analysis of matK se-

quence data (Hilu et al., 2003), an analysis of ndhF in mono-

cots (Givnish et al., in press), and a seven-gene analysis of

monocots (Chase et al., in press) found moderate to strong

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support for the placement of Acorus as sister to other mono-

cots. Hence, most analyses agree on the placement of Acorus

as sister to all other monocots.

Following Acorus, the monophyly of the remaining mono-

cots is strongly supported. Alismatales are sister to the re-

maining monocots, which themselves are strongly supported.

Within this remaining large clade are several component sub-

clades: commelinids, Dioscoreales, Petrosaviaceae, Pandana-

les, Liliales, and Asparagales. Although many of these com-

ponent subclades receive moderate to strong support, relation-

ships among these subclades have been generally poorly re-

solved. In the strict consensus of Chase et al. (2000), the

branching order above Alismatales is Dioscoreales, Pandana-

les, Liliales, and Asparagales 1 commelinids. The seven-gene

analysis of Chase et al. (in press) is consistent with this pat-

tern, except that Dioscoreales and Pandanales are sister taxa,

and most of these relationships received at least moderate

bootstrap support.

Chloranthaceae—Chloranthaceae, with their small, simple

ﬂowers, have an extensive fossil record, dating back 125 my

(e.g., Couper, 1958; Walker and Walker, 1984; Friis et al.,

2000). Chloranthaceae are clearly an isolated lineage separate

from the magnoliid clade (Fig. 2), but their phylogenetic po-

sition remains uncertain. In some analyses (e.g., Zanis et al.,

2002; Davies et al., 2004), they are sister to a clade of mag-

noliids 1 eudicots. Relationships and patterns of evolution

within Chloranthaceae have been addressed by Kong et al.

(2002), Doyle et al. (2003), Zhang and Renner (2003), and

Eklund et al. (2004).

Magnoliids—The magnoliid clade comprises most of those

lineages typically referred to as ‘‘primitive angiosperms’’ in

earlier works (e.g., Stebbins, 1974; Cronquist, 1981, 1988;

Takhtajan, 1997). Although the component families of the

magnoliid clade were loosely associated in previous classiﬁ-

cations, for example, as Cronquist’s (1981) subclass Magno-

liidae, relationships among the families and orders were not

clear. In addition, Magnoliidae contained groups that are not

part of the magnoliid clade as recognized by phylogenetic

analyses. Reconstructing relationships within this clade, and

even recognition of the clade itself, is challenging, given the

age of this clade (some putative members, such as Archaean-

thus, Dilcher and Crane, 1984, date to the early Cretaceous)

and presumably high levels of extinction. Although the major

lineages of the magnoliid clade were identiﬁed as well-sup-

ported clades in earlier studies (e.g., Soltis et al., 1999), com-

position and interrelationships of the magnoliid clade did not

become clear until data sets of at least ﬁve genes for a broad

sample of taxa were assembled to address these problems (e.g.,

Qiu et al., 1999, 2000; Zanis et al., 2002). Within the mag-

noliids, Magnoliales and Laurales are sisters, and Piperales and

Canellales are sisters (Fig. 2).

Magnoliales. This clade comprises six families (Myristica-

ceae, Degeneriaceae, Himantandraceae, Magnoliaceae, Eu-

pomatiaceae, and Annonaceae), relationships among which are

now clear (e.g., Sauquet et al., 2003; Fig. 2). This same clade

emerged in the nonmolecular analysis of Doyle and Endress

(2000). Apparent synapomorphies for the clade include re-

duced ﬁber pit borders, stratiﬁed phloem, an adaxial plate of

vascular tissue in the petiole, palisade parenchyma, astero-

sclereids in the leaf mesophyll, continuous tectum in the pol-

len, and multiplicative testa in the seed (Doyle and Endress,

2000). Furthermore, all members of this clade examined to

date have a characteristic deletion in their Apetala3 gene (Kim

et al., in press).

Laurales. Laurales, as currently circumscribed (APG II,

2003; see Renner, 1999), comprise seven families: Calycan-

thaceae (including Idiospermaceae), Monimiaceae, Gomorte-

gaceae, Atherospermataceae, Lauraceae, Sipurunaceae, and

Hernandiaceae. Amborellaceae and Trimeniaceae have also

occasionally been placed in Laurales (e.g., Cronquist, 1981,

1988); in fact, both Amborella and Trimenia have even been

considered part of Monimiaceae (Perkins, 1925). Chlorantha-

ceae have also occasionally been placed in Laurales (e.g.,

Thorne, 1974; Takhtajan, 1987, 1997). Laurales are united by

a perigynous ﬂower in which the gynoecium is frequently

deeply embedded in a ﬂeshy receptacle (Endress and Iger-

sheim, 1997; Renner, 1999). Other apparent synapomorphies

include the presence of inner staminodia, ascendant ovules,

and tracheidal endotesta (Doyle and Endress, 2000).

Piperales. Previous circumscriptions of Piperales have var-

ied (e.g., Dahlgren, 1980; Cronquist, 1981, 1988; Takhtajan,

1987, 1997; Thorne, 1992; Heywood, 1993), but molecular

studies clearly united Aristolochiaceae, Lactoridaceae, Piper-

aceae, and Saururaceae (e.g., Qiu et al., 1999; Soltis et al.,

1999; Barkman et al., 2000; D. Soltis et al., 2000; Zanis et

al., 2002). In addition, recent studies have placed Hydnora-

ceae, a family of parasitic plants often placed in Rosidae (e.g.,

Cronquist, 1981; Heywood, 1993), within Piperales, although

the exact position is not certain (Nickrent et al., 2002). Al-

though not recognized as a group prior to molecular analyses,

a number of morphological synapomorphies have been iden-

tiﬁed: distichous phyllotaxis, a single prophyll, and oil cells

(Doyle and Endress, 2000).

Canellales. The sister group of Canellaceae and Winteraceae

has been strongly supported in all multigene analyses (e.g.,

Qiu et al., 1999; Soltis et al., 1999; D. Soltis et al., 2000;

Zanis et al., 2002, 2003), and the clade was obtained in Doyle

and Endress’s (2000) nonmolecular analysis as well. However,

these two families have not typically been considered closely

related to each other, and neither was suspected of being re-

lated to any members of Piperales. For example, Winteraceae

have often been considered a close relative of Magnoliaceae

(e.g., Cronquist, 1981, 1988; Heywood, 1993), with Canella-

ceae close to Myristicaceae (e.g., Wilson, 1966; Cronquist,

1981, 1988). Furthermore, Winteraceae have often been re-

garded as perhaps the ‘‘most primitive’’ extant family of an-

giosperms (Cronquist, 1981; Endress, 1986). The phylogenetic

position of Winteraceae clearly indicates that the vesselless

xylem and plicate carpels found in members of the family are

secondarily derived (see also Young, 1981). Possible synapo-

morphies for Canellales are a well-differentiated pollen tube

transmitting tissue, an outer integument with only two to four

cell layers, and seeds with a palisade exotesta (Doyle and En-

dress, 2000). Additional synapomorphies may include an ir-

regular ‘‘ﬁrst-rank’’ leaf venation (Hickey and Wolf, 1975;

Doyle and Endress, 2000), stelar and nodal structure (Keating,

2000), and vascularization of the seeds (Deroin, 2000).

Eudicots—Eudicots comprise approximately 75% of all an-

giosperm species (Drinnan et al., 1994) and are strongly sup-

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Fig. 3. Summary of phylogenetic relationships among clades of eudicots,

based on Hoot et al. (1999), D. Soltis et al. (2000, 2003), and Kim et al.

(2004).

ported by molecular data. However, only a single morpholog-

ical synapomorphy—triaperturate pollen—has been identiﬁed.

This pollen type is clearly distinct from the uniaperturate pol-

len of basal angiosperms, monocots, and all other seed plants,

allowing easy assignment of fossil pollen to the eudicots. The

fossil pollen record indicates that the eudicots appeared 125

mya, shortly after the origin of the angiosperms themselves.

The extensive fossil pollen collections worldwide, coupled

with solid dates, make it unlikely that the eudicots arose much

before this time. Although triaperturate pollen is a synapo-

morphy for this clade, not all eudicots have triaperturate pollen

due to subsequent changes in pollen structure. The eudicots

(referred to instead as tricolpates) are covered in greater detail

by Judd and Olmstead (2004).

Basal lineages—A basal grade of ﬁve lineages (Ranuncu-

lales, Proteales, Sabiaceae, Trochodendraceae, and Buxaceae)

subtends the large clade of core eudicots (Hoot et al., 1999;

D. Soltis et al., 2000; Kim et al., 2004; Fig. 3). Although

Ranunculales are supported as the sister to all other eudicots,

the relative placements of the remaining four lineages of basal

eudicots are not clear and require additional study.

Core eudicots—The core eudicots comprise the vast major-

ity of eudicot species. Seven major clades (Gunnerales, ‘‘Ber-

beridopsidales,’’ Saxifragales, Santalales, Caryophyllales, ros-

ids, and asterids) have been recognized, but the relationships

among these clades are not clear (Figs. 1, 3; D. Soltis et al.,

2000). The topology indicates a rapid radiation, but additional

data are needed to evaluate this hypothesis. Recent studies

have identiﬁed Gunnerales as the sister to all other core eu-

dicots (Hilu et al., 2003; Soltis et al., 2003). Several important

changes in ﬂoral genes appear to coincide with the origin of

core eudicots, including duplication of AP3 yielding the

euAP3 lineage (Kramer et al., 1998) and the origin of Apetala1

(Litt and Irish, 2003).

Gunnerales. Gunnerales comprise two small families, Gun-

neraceae (Gunnera with approximately 40 species) and My-

rothamnaceae (Myrothamnus with two species) (or Gunnera-

ceae s.l. sensu APG II, 2003). This relationship had not pre-

viously been suggested on the basis of morphology because

the two genera differ substantially, although molecular support

for their relationship is very strong. Gunneraceae have a dim-

erous perianth (Drinnan et al., 1994), as do many of the basal

eudicot lineages; dimery probably typiﬁes Buxaceae, Trochod-

endraceae, and Proteaceae (but perhaps not the Platanus lin-

eage) and is common and perhaps ancestral in Ranunculales

(van Tieghem, 1897; Drinnan et al., 1994; Douglas and Tucker,

1996). The placement of Gunnerales as sister to the rest of the

core eudicots implies that the pentamerous perianth typical of

most core eudicots was derived from dimerous ancestors

(Ronse De Craene et al., 2003; Soltis et al., 2003).

‘‘Berberidopsidales’’. Like Gunnerales, ‘‘Berberidopsida-

les’’ comprise two small and morphologically disparate fami-

lies: Berberidopsidaceae (Berberidopsis and Streptothamnus,

which is sometimes included in Berberidopsis) and Aextoxi-

caceae (Aextoxicon, one species). Although this clade has not

been recognized at the ordinal level by APG (hence the quo-

tation marks), it is strongly supported by molecular data and

is isolated from all other clades. Furthermore, both families

have encyclocytic stomata, a rare character and an apparent

synapomorphy for this clade (Soltis et al., in press-b).

Saxifragales. Saxifragales are a morphologically eclectic

clade of annual and perennial herbs, succulents, aquatics,

shrubs, vines, and large trees. Prior to molecular phylogenetics

(Morgan and Soltis, 1993; Fishbein et al., 2001), members of

this clade were classiﬁed in three of Cronquist’s (1981) six

subclasses of dicots (see also Takhtajan, 1997). Possible syn-

apomorphies for this clade include a partially fused bicarpel-

late gynoecium, a hypanthium, and glandular leaf teeth (Judd

et al., 2002); aspects of leaf venation and wood anatomy are

similar in the woody members of the clade. The best known

of the 13 families in this clade are Saxifragaceae, Crassula-

ceae, Grossulariaceae, Paeoniaceae, and Hamamelidaceae.

Molecular studies continue to reveal new, unexpected mem-

bers of this clade, such as Peridiscaceae (Davis and Chase,

2004), a family placed in Malpighiales in APG II (2003).

Monophyly of Saxifragales is strongly supported, but the

position of this clade relative to other core eudicots remains

uncertain. Some analyses have placed it as sister to the rosids,

although with weak support (e.g., D. Soltis et al., 2000). The

simple, pentamerous ﬂowers have long been thought to indi-

cate a relationship with Rosaceae and other rosids, but whether

these ﬂoral features are synapomorphies for Saxifragales 1

rosids or symplesiomorphies (i.e., shared ancestral features) is

unclear. Despite the fairly constant general ﬂoral structure of

Saxifragales, certain aspects of ﬂoral evolution within this

clade appear to be quite labile, especially ovary position (e.g.,

Kuzoff et al., 2001). Additional research is needed to resolve

the relationship of Saxifragales within the core eudicots.

Santalales. The seven families of Santalales are united by

molecular characters and aspects of their parasitic habit and

are a strongly supported clade of core eudicots. However, re-

lationships of Santalales to other core eudicots are not clear,

although they occasionally appear near the asterids in at least

some shortest trees. Furthermore, relationships within this

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clade have not yet been resolved, and the monophyly of some

of the currently recognized families has not been supported by

molecular evidence. The lack of resolution within Santalales

may be explained in part by apparently rapid rates of molec-

ular evolution in all three plant genomes (e.g., Nickrent and

Starr, 1994; Nickrent et al., 1998). Aerial hemiparasites (mis-

tletoes) have evolved multiple times in Santalales.

Caryophyllales. The core of Caryophyllales sensu APG II

(2003) was considered a closely related group of families as

long ago as the mid-nineteenth century (e.g., Braun, 1864;

Eichler, 1876) and was formally recognized as the Centro-

spermae by Harms (1934) based on morphological and em-

bryological characters. Recent molecular studies have identi-

ﬁed a larger clade (Caryophyllales sensu APG II) that includes

the Caryophyllidae of Cronquist (1981; i.e., Caryophyllales,

Polygonales, and Plumbaginales) plus a number of families

previously considered distantly related to Caryophyllales, in-

cluding the carnivorous sundews and Venus’ ﬂytrap (Droser-

aceae) and Old World pitcher plants (Nepenthaceae).

Relationships of Caryophyllales to other core eudicots are

not clear, although Dilleniaceae are sister to Caryophyllales in

some analyses, although with low support (e.g., Chase and

Albert, 1998; D. Soltis et al., 2000; Fig. 3), and some shortest

trees have indicated a possible relationship with the asterids.

Within Caryophyllales, there are two large clades, core and

noncore Caryophyllales (Cue´noud et al., 2002), that corre-

spond to Caryophyllales and Polygonales sensu Judd et al.

(2002). The core Caryophyllales clade generally corresponds

to Caryophyllales of recent classiﬁcations (e.g., Cronquist,

1981; Takhtajan, 1997) and comprises 19 families, although

some currently recognized families (e.g., Portulacaceae, Phy-

tolaccaceae) are poly- or paraphyletic and require recircum-

scription (Cue´noud et al., 2002). Synapomorphies for this

clade include unilacunar nodes, stems with concentric rings of

xylem and phloem, phloem sieve tubes with plastids with a

peripheral ring of proteinaceous ﬁlaments and a central protein

crystal, betalains (rather than anthocyanins), loss of the intron

in the plastid gene rpl2, a single perianth whorl, free central

to basal placentation, an embryo curved around the seed, and

presence of perisperm with little or no endosperm (Judd et al.,

2002 and references therein). The noncore clade has been

identiﬁed on the basis of molecular data and comprises fami-

lies classiﬁed in Cronquist’s (1981) Rosidae and Dilleniidae.

Most surprising is the inclusion in this clade of the carnivorous

Droseraceae and Nepenthaceae. Synapomorphies for the non-

core clade are scattered secretory cells containing plumbagin,

an indumentum of stalked, gland-headed hairs, basal placen-

tation, and starchy endosperm (Judd et al., 2002).

Many Caryophyllales are adapted to harsh environments,

such as high-alkaline soils, high-salt conditions, extreme arid-

ity, and nutrient-poor soils (see descriptions of component

families in Heywood, 1993; Judd et al., 2002). Various adap-

tations, such as Crassulacean acid metabolism and C

photo-

synthesis, succulence, carnivory, and salt secretion, have

evolved multiple times (e.g., Juniper et al., 1989; Meimberg

et al., 2000; Pyankov et al., 2001; Cameron et al., 2002) and

have allowed Caryophyllales to exploit these habitats.

Rosids. The rosid clade is broader than the traditional sub-

class Rosidae (Cronquist, 1981; Takhtajan, 1980, 1997), also

encompassing many families formerly classiﬁed in the poly-

phyletic subclasses Magnoliidae, Dilleniidae, and Hamameli-

dae. The rosids comprise 140 families and close to one-third

of all angiosperm species. Clear synapomorphies for the rosids

have not been identiﬁed, although most rosids share several

morphological and anatomical features, such as nuclear en-

dosperm development, reticulate pollen exine, generally sim-

ple perforations of vessel end-walls, alternate intervessel pit-

ting, mucilaginous leaf epidermis, and two or more whorls of

stamens, plus ellagic acid (Hufford, 1992; Nandi et al., 1998).

Relationships within rosids are not clearly resolved. Vita-

ceae may be sister to the rosids, but this relationship is not

strongly supported (Fig. 3; Savolainen et al., 2000a, b; D. Sol-

tis et al., 2000), and Saxifragales may be sister to the Vitaceae

1 rosids clade, but this relationship is not strongly supported

either (D. Soltis et al., 2000). Two large subclades of rosids,

eurosids I (fabids) and II (malvids), have been identiﬁed

through molecular analyses (e.g., Chase et al., 1993; Savolai-

nen et al., 2000a, b; D. Soltis et al., 2000; Fig. 1). However,

some orders and families (e.g., Crossosomatales, Geraniales,

Myrtales) do not ﬁt into either eurosid I or eurosid II. The

eurosid I clade comprises Celastrales, Cucurbitales, Fabales,

Fagales, Zygophyllales, Malpighiales, Oxalidales, and Ro-

sales. Of these, Cucurbitales, Fabales, Fagales, and Rosales

form the ‘‘nitrogen-ﬁxing clade,’’ a clade that contains all an-

giosperms known to have symbiotic relationships with nodu-

lating nitrogen-ﬁxing bacteria (see D. Soltis et al., 1995, 1997,

2000). The placements in previous classiﬁcations of the spe-

cies that exhibit this symbiosis indicated that symbiotic rela-

tionships with nodulating bacteria must have occurred multiple

times. Current phylogenetic evidence instead indicates a single

origin of the predisposition for symbiosis, with perhaps both

gains and losses of the symbiotic relationship within the nitro-

gen-ﬁxing clade itself (Soltis et al., 1995; Swensen, 1996).

Multiple gains of this association may be more parsimonious

than a single gain followed by multiple losses (Swensen,

1996). The smaller eurosid II clade is composed of Brassi-

cales, Malvales, Sapindales, and Tapisciaceae. Brassicales in-

clude all angiosperms known to produce glucosinolates, a

form of chemical defense, except Drypetes and Putranjiva of

the distantly related rosid family Putranjivaceae of Malpighi-

ales (e.g., Rodman, 1991; Rodman et al., 1993, 1998). Previ-

ous classiﬁcations led to the conclusion that glucosinolate pro-

duction had evolved several times in the angiosperms; current

phylogenetic evidence indicates instead only two such origins.

In addition to the large eurosid I and II clades, additional

smaller clades have been recognized (Crossosomatales, Myr-

tales, Geraniales, and Picramniaceae), but their relationships

to each other and to eurosids I and II are not clear. Further-

more, relationships within eurosids I and II are not fully re-

solved, and much additional work is needed to reconstruct

relationships within the rosid clade. In fact, the rosids repre-

sent the largest remaining problematic group of angiosperms.

Several factors may have contributed to the lack of resolu-

tion of relationships within the rosids. The clade is old, dating

at least to the late Santonian to Turonian (approximately 84–

89.5 mya; Crepet and Nixon, 1998; Magallo´n et al., 1999),

and possibly to 94 mya, based on an unnamed apparently rosid

ﬂower from the Dakota Formation in Nebraska (Basinger and

Dilcher, 1984). Furthermore, molecular-based age estimates of

Myrtales using penalized likelihood (Sanderson, 2002) placed

the crown radiation of Myrtales at approximately 110 mya

(Sytsma et al., in press), implying an even older age for the

rosids. The age of the rosid clade is therefore sufﬁcient to have

allowed substantial morphological and molecular diversiﬁca-

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OLTIS AND

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tion and speciation, although the similar age of the monocots

has not similarly obscured relationships within that clade. The

rosid clade may have diversiﬁed via a series of radiations (P.

Soltis et al., 2004), resulting in a pattern of polytomies (see

Remaining Problems and Future Prospects). Furthermore, sub-

tle nonmolecular features that could potentially unite large

groups of families within the rosids have not generally been

identiﬁed because, until the results of molecular analyses,

many families of rosids were not suspected of being closely

related, having been placed in four subclasses of dicots (Mag-

noliidae, Hamamelidae, Dilleniidae, and Rosidae), and were

therefore not included together in most previous analyses and

treatments. Gaps in morphological data sets across the rosids

have likewise made it difﬁcult to identify synapomorphies for

groups of families.

Asterids. Like rosids, asterids are a large clade, encompass-

ing nearly one-third of all angiosperm species (80000 species)

and classiﬁed in 114 families (Albach et al., 2001b). However,

unlike the rosids, a group of families corresponding closely to

the asterids has been recognized on morphological grounds for

over 200 years (de Jussieu, 1789; Reichenbach, 1828; Warm-

ing, 1879), and several morphological and chemical features

appear to unite all or most asterids. Most notable are iridoid

chemical compounds (e.g., Jensen, 1992), sympetalous corol-

las, unitegmic and tenuinucellate ovules, and cellular endo-

sperm development; however, it is still unclear which of these

features are actually synapomorphies for asterids (cf. Albach

et al., 2001a; Judd et al., 2002). The asterid clade is broader

than Asteridae of recent classiﬁcations (e.g., Cronquist, 1981;

Takhtajan, 1980, 1997) and includes also members of the poly-

phyletic subclasses Hamamelidae, Dilleniidae, and Rosidae

(Olmstead et al., 1992, 1993, 2000; Chase et al., 1993; D.

Soltis et al., 1997, 2000; Soltis et al., 1999; Savolainen et al.,

2000a, b).

Many relationships within asterids were resolved by angio-

sperm-wide analyses, but asterids have also been analyzed in

greater detail with extensive taxon sampling and data from

four (Albach et al., 2001b) and six (Bremer et al., 2002) loci.

These studies conﬁrmed earlier results of four major clades

within asterids (Fig. 1): Cornales are sister to all other asterids,

with Ericales sister to a clade of euasterids I 1 euasterids II.

The families of Cornales and Ericales were not considered

closely related to those of Asteridae in previous classiﬁcations

and were placed instead mostly in Rosidae and Dilleniidae,

respectively. Euasterids are mostly united by ﬂowers with epi-

petalous stamens that equal the number of corolla lobes and a

gynoecium of two fused carpels.

Within the euasterids, the euasterid I (or lamiid, Bremer et

al., 2002) and euasterid II (or campanulid, Bremer et al., 2002)

clades are sisters and can be distinguished both morphologi-

cally and molecularly (Albach et al., 2001b; Bremer et al.,

2001; Bremer et al., 2002). Most members of euasterids I have

opposite leaves, entire leaf margins, hypogynous ﬂowers,

‘‘early sympetaly’’ with a ring-shaped primordium, fusion of

stamen ﬁlaments to the corolla tube, and capsular fruits (Bre-

mer et al., 2001). The euasterid I clade comprises Garryales,

Gentianales, Solanales, and Lamiales, plus Boraginaceae, Vah-

liaceae, and Oncothecaceae 1 Icacinaceae (APG II, 2003).

Most taxa of euasterids II have alternate leaves, serrate-dentate

leaf margins, epigynous ﬂowers, ‘‘late sympetaly’’ with dis-

tinct petal primordia, free stamen ﬁlaments, and indehiscent

fruits (Bremer et al., 2001). It is unclear which of the char-

acters that distinguish euasterids I and II are truly synapo-

morphies for these clades and which are symplesiomorphies;

both reversals and parallelisms have contributed to complex

patterns of morphological evolution in the asterids (Albach et

al., 2001a; Bremer et al., 2001). The euasterid II clade is com-

posed of Dipsacales, Aquifoliales, Apiales, and Asterales, plus

Bruniaceae 1 Columelliaceae, a small clade of Tribelaceae,

Polyosmaceae, Escalloniaceae, and Eremosynaceae, and pos-

sibly Paracryphiaceae. The euasterid II clade includes families

previously classiﬁed in Asteridae and Rosidae (Cronquist,

1981, 1988).

The supertree approach—The relationships described in

this paper are all based on analyses that use the ‘‘supermatrix’’

approach, that is, a taxon-by-character data matrix is assem-

bled and analyzed, directly producing a tree or set of trees. A

problem with this approach is that comprehensive data sets

become extremely large, and analyses become increasingly

computationally complex and time-consuming. In addition,

different gene sets have not always sampled the same taxa,

requiring assumptions of generic or familial monophyly in the

formation of ‘‘mosaic’’ taxa and/or leading to large amounts

of missing data. An alternative to the supermatrix approach is

the supertree approach (e.g., Baum, 1992; Ragan, 1992; Purv-

is, 1995; Ronquist, 1996; Bininda-Emonds and Bryant, 1998;

Sanderson et al., 1998), in which trees that overlap in at least

a single taxon may be joined together algorithmically. Al-

though less satisfying than the supermatrix approach in relat-

ing support or conﬂict for a topology to speciﬁc characters,

the supertree approach is a viable alternative when multiple

data sets overlap in only a small fraction of the taxa or when

the number of taxa to be analyzed is very large. Furthermore,

the two approaches seem to give similar results (e.g., Salamin

et al., 2002).

The supertree approach has not been applied extensively to

angiosperms, but it offers an opportunity for representation of

greater numbers of taxa than the supermatrix analyses con-

ducted to date. A recent supertree analysis combined trees that

included all angiosperm families and produced the ﬁrst com-

prehensive family-level phylogenetic tree for angiosperms

(Davies et al., 2004). The basic framework of the angiosperm

supertree is largely consistent with the results of large, mul-

tigene analyses of exemplar taxa (e.g., D. Soltis et al., 2000)

on which it was based. Amborella is sister to all other angio-

sperms, followed by Nymphaeaceae, Austrabaileyales, a clade

of monocots 1 Ceratophyllaceae, Chloranthaceae, and a clade

of magnoliids 1 eudicots. Relationships within monocots,

magnoliids, and eudicots are also mostly consistent with the

results of the supermatrix analyses. This congruence indicates

that the placement of those taxa not included in the super-

matrix analyses may be correct, inasmuch as the data set can

convey. Furthermore, some clades that have been difﬁcult to

place appear in resolved locations. For example, Caryophyl-

lales are sister to the asterids, and Saxifragales are sister to the

rosids, positions they occupy in some of the shortest trees ob-

tained in other analyses but not in the strict consensus trees

(e.g., D. Soltis et al., 2000). Although the best methods of

supertree construction remain under debate, supertree ap-

proaches seem a viable alternative to supermatrix analyses as

data sets continue to grow.

1622 [Vol. 91A

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REMAINING PROBLEMS AND FUTURE PROSPECTS

Despite tremendous progress in angiosperm phylogenetics

during the past 10 years, several difﬁcult problems remain.

Most prominent are (1) relationships among monocots, Chlor-

anthaceae, magnoliids, and eudicots, (2) branching order

among basal eudicots, (3) relationships among the major

clades of core eudicots, (4) relationships within rosids, (5) re-

lationships of the many lineages of parasitic plants (although

this problem has been addressed recently by Barkman et al.,

2004), and (6) integration of fossils with extant taxa into a

comprehensive tree of angiosperm phylogeny. Solving these

problems will require coordinated efforts among angiosperm

systematists and paleobotanists and a large amount of molec-

ular (and other, where appropriate) data.

At least some of those nodes that remain poorly resolved

(e.g., basal eudicots, core eudicots, rosids) may be the results

of rapid radiations (see P. Soltis et al., 2004). If so, increased

sampling of molecular characters coupled with inclusion of

additional taxa (if a clade has not yet been thoroughly sam-

pled) may help to resolve at least some of the remaining po-

lytomies. For example, the addition of 26S rDNA sequences

to the three-gene data set of D. Soltis et al. (2000) for a subset

of eudicots provided evidence for Gunnerales as the sister to

the remaining lineages of core eudicots (D. Soltis et al., 2003),

and increased character sampling for data sets of more than

100 taxa improved relationships among basal angiosperms

(Zanis et al., 2002) and within monocots (e.g., Chase et al., in

press). However, if the lack of resolution is due to a true ra-

diation, it may not be possible to resolve these nodes. Like-

wise, if poor resolution has resulted from other factors, such

as extinction, inadequate sampling of extant lineages, ancient

reticulation, horizontal gene transfer, or unequal evolutionary

rates among lineages, then the prospects for resolution, using

currently available data and methods of analysis, are also poor.

Estimates of the age of the angiosperms and the timing of

important divergences based on molecular data do not gener-

ally agree with each other (ranging from ;125 to .400 mya)

or with dates determined from the fossil record (see e.g., San-

derson and Doyle, 2001; P. Soltis et al., 2002; Sanderson et

al., 2004). Although most molecular-based ages for angio-

sperms, and other groups of organisms (e.g., Heckman et al.,

2001), are much older than the fossil record suggests, many

recent estimates based on methods that do not assume equal

rates of evolutionary change among lineages are similar to, if

slightly older than, dates inferred from the fossil record (San-

derson et al., 2004). Furthermore, estimated ages for speciﬁc

angiosperm clades are generally older than inferences from the

fossil record (e.g., Wikstro¨m et al., 2001, compared with Ma-

gallo´n et al., 1999), but these discrepancies are much smaller

than those reported for the age of the angiosperms. However,

room for further reconciliation of age estimates inferred from

fossils and molecular data remains. For example, given the

numerous diverse fossils reported from as early as 115–125

mya, perhaps the earliest angiosperms were older than the con-

servative estimate of ;130 mya. Conversely, molecular meth-

ods tend to overestimate ages (Rodrı´guez-Trelles et al., 2002),

so reﬁnement of dating approaches is needed to compensate

for this bias.

Many of the large clades identiﬁed through analysis of mo-

lecular data are not easily recognized morphologically. Al-

though possible synapomorphies for many clades have been

proposed by Doyle and Endress (2000) and Judd et al. (2002),

the identiﬁcation of nonmolecular synapomorphies is still

needed for many clades. This task will require new morpho-

logical and molecular data for many groups, including both a

search for new characters and ﬁlling in data for many families.

Finally, all of this new information—sequences, trees, mor-

phological data—will need to be managed in such a way as

to make it easily accessible to all who are interested via public

databases. The development and maintenance of informatics

tools and resources are therefore also major challenges that lie

ahead for angiosperm systematics. Informatics issues may be-

come particularly important as new methods are needed to

analyze large amounts of sequence data for more taxa than

have yet been analyzed together and to develop algorithms and

methods for constructing supertrees to link new trees with

those that have been archived.

The phylogenetic information currently available for angio-

sperms, and that to come, is fundamentally important for or-

ganizing all that is known about the angiosperm branch of the

tree of life. However, this phylogenetic information is also a

prerequisite for addressing basic questions in a number of oth-

er ﬁelds, ranging from genomics to ecology.

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Angiosperm‐wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits

Article

Full-text available

Feb 2024
J INTEGR PLANT BIOL

Fruit functions in seed protection and dispersal and belongs to many dry and fleshy types, yet their evolutionary pattern remains unclear in part due to uncertainties in the phylogenetic relationships among several orders and families. Thus we used nuclear genes of 502 angiosperm species representing 231 families to reconstruct a well supported phylogeny, with resolved relationships for orders and families with previously uncertain placements. Using this phylogeny as a framework, molecular dating supports a Triassic origin of the crown angiosperms, followed by the emergence of most orders in the Jurassic and Cretaceous and their rise to ecological dominance during the Cretaceous Terrestrial Revolution. The robust phylogeny allowed an examination of the evolutionary pattern of fruit and ovary types, revealing a trend of parallel carpel fusions during early diversifications in eudicots, monocots, and magnoliids. Moreover, taxa in the same order or family with the same ovary type can develop either dry or fleshy fruits with strong correlations between specific types of dry and fleshy fruits; such associations of ovary, dry and fleshy fruits define several ovary‐fruit “modules” each found in multiple families. One of the frequent modules has an ovary containing multiple ovules, capsules and berries, and another with an ovary having one or two ovules, achenes (or other single‐seeded dry fruits) and drupes. This new perspective of relationships among fruit types highlights the closeness of specific dry and fleshy fruit types, such as capsule and berry, that develop from the same ovary type and belong to the same module relative to dry and fleshy fruits of other modules (such as achenes and drupes). Further analyses of gene families containing known genes for ovary and fruit development identified phylogenetic nodes with multiple gene duplications, supporting a possible role of whole‐genome duplications, in combination with climate changes and animal behaviors, in angiosperm fruit and ovary diversification.

Polycotyly: How Little Do We Know?

Article

Full-text available

Apr 2024

Yong-Bi Fu

Polycotyly, an interesting characteristic of seed-bearing dicotyledonous plants with more than two cotyledons, represents one of the least explored plant characters for utilization, even though cotyledon number was used to classify flowering plants in 1682. Gymnosperm and angiosperm species are generally known to have one or two cotyledons, but scattered reports exist on irregular cotyledon numbers in many plant species, and little is known about the extent of polycotyly in plant taxa. Here, we attempt to update the documentation of reports on polycotyly in plant species and highlight some lines of research for a better understanding of polycotyly. This effort revealed 342 angiosperm species of 237 genera in 80 (out of 416) families and 160 gymnosperm species of 26 genera in 6 (out of 12) families with reported or cited polycotyly. The most advanced research included the molecular-based inference of the phylogeny of flowering plants, showing a significant departure from the cotyledon-based classification of angiosperm plants, and the application of genetic cotyledon mutants as tools to clone and characterize the genes regulating cotyledon development. However, there were no reports on breeding lines with a 100% frequency of polycotyly. Research is needed to discover plant species with polycotyly and to explore the nature, development, genetics, evolution, and potential use of polycotyly.

Unique Jurassic Fruits Shed a New Light on the Nature of Carpels

Preprint

Full-text available

Jun 2024

Carpels are a reproductive feature restricted to angiosperms, therefore they are a focus of many botanical studies. However, there are controversies over the nature of carpels. A reason underly-ing these controversies is mixing implications given by conflicting interpretations on fossil carpels in early fossil angiosperms from the Cretaceous. These controversies hinder a clear understanding of angiosperm evolution and systematics. A key to these questions is older fossil fruits bearing concerned information. Here we report a new fossil fruit, Xenofructus dabuensis gen. et sp. nov, from the Middle Jurassic of Liaoning, China. Unlike previously reported fruits of early angio-sperms that were interpreted as bearing seeds either on adaxial or abaxial margin by various au-thors, our fossil demonstrates clearly that the seeds in Xenofructus are neither borne on the adaxial nor abaxial margin of the fruit, instead the seeds of Xenofructus are borne on an axis positioned between two margins. This new feature implies that a placenta in carpels is an ovule/seed-bearing axis, a carpel is a composite organ comprising an enclosing leaf (fruit wall) and an axis (placenta). The adaxial or abaxial position of ovules/seeds frequently seen in fossil and extant angiosperms is a consequence derived through long time evolution (coalescence of placenta with either margin of fruits). Carpels can be taken as foliar structures enclosing their associated ovulate branches.

The potential of flowering plant diversity in local fruit thematic garden of Indrokilo Botanic Garden of Boyolali as a biology learning resource

Conference Paper

Full-text available

Jan 2024

A method and application for the integration of geology, geochronology, and paleontology

Chapter

Jan 2024

Was Charles Darwin right in his explanation of the ‘abominable mystery’?

Article

Full-text available

Mar 2018

The site and time of origin of angiosperms are still debated. The co-occurrence of many of the early branching lineages of flowering plants in a region somewhere between Australia and the SW Pacific islands suggests a possible Gondwanan origin of angiosperms. The recent recognition of Zealandia, a 94% submerged continent in the east of Australia, could explain the discrepancy between molecular clocks and fossil records about the age of angiosperms, supporting the old Darwinian hypothesis of a “lost continent” to explain the “abominable mystery” regarding the origin and rapid radiation of flowering plants.

Characterization of the Complete Mitochondrial Genome of Wintersweet (Chimonanthus praecox) and Comparative Analysis within Magnoliids

Article

Full-text available

Jan 2024

Mitochondrial genome sequencing is a valuable tool for investigating mitogenome evolution, species phylogeny, and population genetics. Chimonanthus praecox (L.) Link, also known as “La Mei” in Chinese, is a famous ornamental and medical shrub belonging to the order Laurales of the Calycanthaceae family. Although the nuclear genomes and chloroplast genomes of certain Laurales representatives, such as Lindera glauca, Laurus nobilis, and Piper nigrum, have been sequenced, the mitochondrial genome of Laurales members remains unknown. Here, we reported the first complete mitogenome of C. praecox. The mitogenome was 972,347 bp in length and comprised 60 unique coding genes, including 40 protein-coding genes (PCGs), 17 tRNA genes, and three rRNA genes. The skewness of the PCGs showed that the AT skew (−0.0096233) was negative, while the GC skew (0.031656) was positive, indicating higher contents of T’s and G’s in the mitochondrial genome of C. praecox. The Ka/Ks ratio analysis showed that the Ka/Ks values of most genes were less than one, suggesting that these genes were under purifying selection. Furthermore, there is a substantial abundance of dispersed repeats in C. praecox, constituting 16.98% of the total mitochondrial genome. A total of 731 SSR repeats were identified in the mitogenome, the highest number among the eleven available magnoliids mitogenomes. The mitochondrial phylogenetic analysis based on 29 conserved PCGs placed the C. praecox in Lauraceae, and supported the sister relationship of Laurales with Magnoliales, which was congruent with the nuclear genome evidence. The present study enriches the mitogenome data of C. praecox and promotes further studies on phylogeny and plastid evolution.

Holomorphology, Space, and Time to Shed Light on the Evolution and Distributional Pattern of the Endemic Flowering Plants of Brazil

Article

Full-text available

Nov 2023
EVOL BIOL

The disparity in species richness among clades of angiosperms is partly explained by differences in evolutionary and biogeographic processes; however, part of this imbalance remains elusive. The relationships between species diversification and key innovations, as well as the impact of clade age, are also predicted to explain such disparities. This relationship has not been examined using phylogeny-based approaches based on holomorphology, i.e., concatenated morphological and molecular datasets. Despite some large-scale evolutionary studies that have contributed to the knowledge of Brazilian flora, the evolutionary history of angiosperms endemic to Brazilian provinces has not yet been elucidated. Therefore, this study had two principal targets. First, we investigated the species richness and distribution patterns of endemic angiosperm genera. Secondly, we perform a phylogenetic analysis based on holomorphology to examine the relationship between species diversification and putative key innovations (by homology assessments) and the effects of clade age on diversification in species-rich genera. We identified the occurrence of 341 exclusive genera (45% monotypic) in 61 families. Our results indicate a positive correlation between diversification and the number of putative key innovations per order but a negative or non-existent one per family. Furthermore, our findings contradict the idea that clade age is associated with species-rich genera, challenging the notion that clade age is a determining factor in species richness. The results showed that 14 traits are closely associated with diversification, and the confluence between biotic and abiotic factors drove the diversification of species-rich genera in the Atlantic Forest, Caatinga, Cerrado, and Parana provinces.

Advancements in balancing glucosinolate production in plants to deliver effective defense and promote human health

Article

May 2024

Some Palynological Considerations in the Environmental History

Chapter

Apr 2024

Environmental history and Quaternary botany have long been interconnected by palynological methods. In this context, pollen morphology and some aspects of pollen systematics can inform on adaptations to different environmental conditions in short- and long-term approaches. In this chapter, we show that some topics such as pollen aperture evolution, exine ultrastructure, and pollen wall development are critical for past environments. In addition, the inclusion of some niche construction ideas improves palaeoecological reconstructions for cross-scale interactions such as historical legacies, climate change, and microenvironmental conditions. For these reasons, we provide this framework and promising future lines of research in ecology and archaeology. Finally, the environmental history represents a mosaic of methods in pollen morphology and local and regional reconstructions for past societies.

The Diversification of Flowering Plants

Chapter

Jul 2004

This edited volume is provides an authoritative synthesis of knowledge about the history of life. All the major groups of organisms are treated, by the leading workers in their fields. With sections on: The Importance of Knowing the Tree of Life; The Origin and Radiation of Life on Earth; The Relationships of Green Plants; The Relationships of Fungi; and The Relationships of Animals. This book should prove indispensable for evolutionary biologists, taxonomists, ecologists interested in biodiversity, and as a baseline sourcebook for organismic biologists, botanists, and microbiologists. An essential reference in this fundamental area.

Duplication and Diversification in the APETALA1/FRUITFULL Floral Homeotic Gene Lineage: Implications for the Evolution of Floral Development

Article

Oct 2003
GENETICS

Phylogenetic analyses of angiosperm MADS-box genes suggest that this gene family has undergone multiple duplication events followed by sequence divergence. To determine when such events have taken place and to understand the relationships of particular MADS-box gene lineages, we have identified APETALA1/FRUITFULL-like MADS-box genes from a variety of angiosperm species. Our phylogenetic analyses show two gene clades within the core eudicots, euAP1 (including Arabidopsis APETALA1 and Antirrhinum SQUAMOSA) and euFUL (including Arabidopsis FRUITFULL). Non-core eudicot species have only sequences similar to euFUL genes (FUL-like). The predicted protein products of euFUL and FUL-like genes share a conserved C-terminal motif. In contrast, predicted products of members of the euAP1 gene clade contain a different C terminus that includes an acidic transcription activation domain and a farnesylation signal. Sequence analyses indicate that the euAP1 amino acid motifs may have arisen via a translational frameshift from the euFUL/FUL-like motif. The euAP1 gene clade includes key regulators of floral development that have been implicated in the specification of perianth identity. However, the presence of euAP1 genes only in core eudicots suggests that there may have been changes in mechanisms of floral development that are correlated with the fixation of floral structure seen in this clade.

Variation and Evolution in Plants

Book

Dec 1950

G. Ledyard Stebbins

Flowering Plants of the World

Article

May 1986

An Integrated System of Classification of Flowering Plants

Article

Jan 1984

The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm

Article

Nov 1994

William E. Friedman

For almost a century, the formation of endosperm from a second and distinctive fertilization event has been viewed as a unique feature of flowering plants. However, until recently, the evolutionary origin of this unique embryo-nourishing entity remained a mystery. Based upon comparative developmental analysis of reproduction among basal angiosperms and their closest extant relatives, the Gnetales (Ephedra, Gnetum, and Welwitschia), it is possible to construct an explicit hypothesis of the events that led to the evolutionary establishment of double fertilization and endosperm. The formulation of this historical record is derived entirely from and dependent upon the determination of reproductive features that are likely to have characterized the common ancestors of angiosperms and Gnetales. Current evidence is most congruent with the concept that a process of double fertilization first evolved in a common ancestor of the Gnetales and angiosperms. Initially, however, the second fertilization product was diploid and yielded a supernumerary embryo. Subsequent to the divergence of the angiosperm lineage from its closest relatives (which include the Gnetales), modification of the development of the supernumerary embryo (derived from the second fertilization event) led to the establishment of an embryo-nourishing endosperm. Comparative analysis of patterns of embryogeny within Gnetales and angiosperms establishes that embryo development in the ancestors of flowering plants (with a rudimentary process of double fertilization) was ab initio cellular, and not free nuclear, as had previously been assumed. Thus, it is likely that the earliest flowering plants displayed an ab initio cellular pattern of endosperm development, whose expression was inherited from that of the supernumerary embryo of the ancestors of flowering plants.

The evolution of actinorhizal symbioses: Evidence for multiple origins of the symbiotic association

Article

Nov 1996

Susan M. (Swensen) Witherup

According to morphologically based classification systems, actinorhizal plants, engaged in nitrogen-fixing symbioses with Frankia bacteria, are considered to be only distantly related. However, recent phylogenetic analyses of seed plants based on chloroplast rbcL gene sequences have suggested closer relationships among actinorhizal plants. A more thorough sampling of chloroplast rbcL gene sequences from actinorhizal plants and their nonsymbiotic close relatives was conducted in an effort to better understand the phylogenetic relationships of these plants, and ultimately, to assess the homology of the different actinorhizal symbioses. Sequence data from 70 taxa were analyzed using parsimony analysis. Strict consensus trees based on 24 equally parsimonious trees revealed evolutionary divergence between groups of actinorhizal species suggesting that not all symbioses are homologous. The arrangement of actinorhizal species, interspersed with nonactinorhizal taxa, is suggestive of multiple origins of the actinorhizal symbiosis. Morphological and anatomical characteristics of nodules from different actinorhizal hosts were mapped onto the rbclL-based consensus tree to further assess homology among rbcL-based actinorhizal groups. The morphological and anatomical features provide additional support for the rbcL-based groupings, and thus, together, suggest that actinorhizal symbioses have originated more than once in evolutionary history.

Comparative floral ontogenies among Persoonioideae including Bellendena (Proteaceae)

Article

Dec 1996

Floral ontogeny is described and compared in five species and four genera of the hypothetically basal proteaceous subfamily Persoonioideae sensu Johnson and Briggs. The hypotheses surrounding the origin of the peculiar proteaceous flower and homologous structures within the flowers are examined using ontogenetic morphological techniques. Ontogenetic evidence reveals that the proteaceous flower is simple, composed of four tepals, each tepal initiated successively with the lateral tepals being initiated first and second followed by the successive initiation of the sagittal tepals. Each of four stamens is initiated opposite a tepal in a similar sequence to tepal initiation. A single carpel develops terminally from the remaining floral meristem. In taxa of Persoonieae, nectaries are initiated from a broadened receptacle in alternistamenous sites after zonal growth beneath and between the tepals and stamens has begun. The nectaries are interpreted as secondary organs, not reduced homologues of a “lost” petal or stamen series. Developmental variation is present among the examined taxa in several forms including the development of a Vorlaüferspitze (spine) on the upper portion of the tepals, adnation between the anthers and tepals, and formation of the carpel. In Placospermum the early formation of the carpel cleft extends to the floral receptacle and in the other taxa, the carpel cleft is distinctly above the receptacle. Different developmental pathways result in similar mature morphologies of the carpel in Persoonia falcata and Placospermum coriaceum. Bellendena montana is unique relative to the other taxa in having free stamens, a punctate stigma, reduced (not lost) floral bracts, and the floral and bract primordia are initiated from a common meristem. This study provides a foundation for future studies of the developmental basis of floral diversity within Proteaceae.

THE COMPARATIVE MORPHOLOGY OF THE CANELLACEAE. IV. FLORAL MORPHOLOGY AND CONCLUSIONS

Article

Apr 1966

Thomas K. Wilson

The morphology and anatomy of 105 flowers representing 13 species and 6 genera of the Canellaceae are summarized. The flowers are borne in axillary or terminal racemes, cymes, or small groups, or solitary, in an axillary or terminal position. The flowers are characterized as follows: bisexual, hypogynous; sepals 3, thick and leathery; petals, 5–12, free or united into tube at base, rather thick, in 1 or 2 whorls and/or spirals; androecium of 6–12 stamens united by their filaments forming a tube, anthers with longitudinal extrorse dehiscence; gynoecium of 2–6 carpels fused by their ventral margins; 2–6 placentae. There are 2 vascular bundles (rarely 3) to each sepal, 3 to each petal (some of the inner petals have only 1), 1 to each stamen and 1 trace to each carpel. The petal and stamen bundles have a common origin. All the data accumulated in this series on the Canellaceae indicate that the correct systematic placement of the Canellaceae is in the woody Ranales, perhaps in a complex with the Myristicaceae.

A Phylogenetic Classification of the Annoniflorae

Article

Jan 1974

Robert Thorne

The origin and diversification of angiosperms

Abstract

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