11 The Diversification of Flowering Plants

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Pamela S. Soltis

Douglas E. Soltis

Mark W. Chase

Peter K. Endress

Peter R. Crane

154

In this chapter, we provide an overview of the phylogeny of

flowering plants, with special emphasis on the root and major

clades of the angiosperms, and patterns of radiation in the

evolutionary history of angiosperms. Given the size of the

angiosperm clade, we will not examine relationships within

major clades in any detail; instead, we refer the reader to

publications that focus on those clades or grades [e.g., basal

angiosperms (Zanis et al. 2002), monocots (Chase et al.

2000), early-diverging eudicots (Hoot et al. 1999), asterids

(Albach et al. 2001, Bremer et al. 2002)]. After this overview,

we use the phylogeny to examine patterns of evolution in

three important features of flowering plants: double fertilization

and endosperm formation, closed carpels, and perianth

structure and organization.

The flowering plants are one of five clades of extant seed

plants, and they are by far the largest, most diverse, and most

important ecologically of all living embryophytes (land

plants). There are at least 260,000 (Takhtajan 1997) species

of flowering plants (i.e., five to six times the number of living

species of vertebrates), classified in approximately 450

families (e.g., 453, as listed in Angiosperm Phylogeny Group

II 2003). The clade has a fossil history that extends back at

least to the early Cretaceous, conservatively approximately

130 million years ago (Mya).

Several features have been identified as synapomorphies

of angiosperms (see Doyle and Donoghue 1986). Perhaps

foremost among these is double fertilization, with its joint

processes of zygote production, endosperm formation, and

angiospermy (i.e., presence of closed carpels). In angiosperms,

one sperm unites with the egg to form a diploid

zygote. Then, typically a second sperm unites with two additional

nuclei, the polar nuclei, to produce a triploid endosperm.

Endosperm tissue provides a source of nutrients

for the developing embryo. Although double fertilization has

also been reported in the gnetophytes (Friedman 1990,

Carmichael and Friedman 1996), the process of double fertilization

and its consequent formation of endosperm are

unique to angiosperms. We examine variation on the basic

theme of fertilization and endosperm formation in angiosperms

later in this chapter.

A second synapomorphy of the angiosperms is the carpel,

the floral structure that contains the ovule(s), which after

fertilization will become the seed(s). The closure of the carpel

provides additional protection for the seeds and may be

accomplished by secretion or fusion of the carpel margins

or flanks. We consider the evolution of the closed carpel later

in this chapter.

Additional synapomorphies of flowering plants include

phloem tissue composed of sieve tubes and companion cells,

stamens with two pairs of pollen sacs, and aspects of gametophyte

development and structure. Although important

characteristics, we do not examine these features further in

this chapter.

Relationships among clades of extant seed plants remain

unclear, despite considerable recent attention (see Pryer et al.,

ch. 10 in this vol.). Nearly all morphological analyses of seed

The Diversification of Flowering Plants 155

plants place the gnetophytes (or at least some of them) as

the sister group to the angiosperms (e.g., Crane 1985, Doyle

and Donoghue 1986, 1992, Loconte and Stevenson 1990,

Nixon et al. 1994, Rothwell and Serbet 1994; for reviews, see

Doyle 1996, 1998, Donoghue and Doyle 2000); however,

molecular analyses have found a variety of topologies,

depending on the gene(s) used and the taxa sampled

(e.g., Hamby and Zimmer 1992, Hasebe et al. 1992, Albert

et al. 1994, Chaw et al. 1997, 2000, Goremykin et al. 1996,

Malek et al. 1996, Hansen et al. 1999, Winter et al. 1999,

Soltis et al. 1999b, Bowe et al. 2000, Sanderson et al. 2000,

Rydin et al. 2002, D. Soltis et al. 2002). Most multigene

analyses have found a clade of extant gymnosperms, consisting

of cycads, Ginkgo, conifers, and gnetophytes, as the

sister to the angiosperms. However, given that the number

of extinct seed plant lineages nearly equals the number of

extant groups, analyses of living seed plants only are likely

to provide inadequate inferences of phylogeny. Resolution

of seed plant relationships, including the sister group of the

angiosperms, will require careful phylogenetic analyses that

integrate data for fossil and extant groups (see Donoghue

and Doyle 2000).

Overview of Angiosperm Phylogeny

The phylogenetic overview of flowering plants that follows

(summarized in fig. 11.1) is drawn from several sources. The

backbone of the tree comes from the collaborative study by

Soltis et al. (2000), which included 560 species of angiosperms,

seven gymnosperms as outgroups, and data from two

plastid genes (rbcL and atpB) and one nuclear gene (18S ribosomal

DNA), for a total of more than 4700 aligned nucleotides.

The rbcL analysis of nearly all families of eudicots

(Savolainen et al. 2000) helped to place several groups not

sampled in the three-gene analysis. In addition, analyses of

specific groups provided information on relationships of

basal angiosperms (Zanis et al. 2002), monocots (Chase et al.

2000), core eudicots (D. Soltis et al. 2002), and asterids

(Albach et al. 2001, Bremer et al. 2002).

The Root of the Angiosperms

Phylogeny of Extant Angiosperms

Most analyses focusing on the root of the angiosperms concur

in finding Amborella as the sister to all other extant flowering

plants (D. Soltis et al. 1997, 2000, P. Soltis et al. 1999a,

Qiu et al. 1999, Mathews and Donoghue 1999, Graham and

Olmstead 2000, Zanis et al. 2002; fig. 11.1). Nymphaeaceae

(water lilies) and Austrobaileyales (composed of Austrobaileya,

Trimenia, Schisandra, Kadsura, and Illicium) occupy

the next branches in this basal grade; all other angiosperm

species form a clade that is sister to Austrobaileyales. This

large clade of all other angiosperms has been referred to as

the euangiosperms (Qiu et al. 1999), but no consensus has

yet been reached on a name for this clade. In contrast to those

studies that show Amborella as the sister group to the rest

of the angiosperms, a few analyses have found alternative

rootings, the more strongly supported of which shows

Amborella together with the water lilies as the sister to all other

living flowering plants (e.g., Barkman et al. 2000). Statistical

analyses of alternative rootings, however, generally favor

the tree with Amborella as sister to the rest of the angiosperms,

although the Amborella + water lilies tree cannot be conclusively

rejected (Zanis et al. 2002). However, more recent

analyses of rapidly evolving genes also place Amborella alone

as sister to all other extant flowering plants (Borsch et al.

2003, Hilu et al. 2003). Furthermore, Amborella is unequivocally

reconstructed as the sister group to all other angiosperms

based on both sequence and structural features

of the floral genes AP3 and PI (S. Kim et al., unpubl. obs.).

Regardless of which rooting is correct, tremendous progress

has been made in a short time, due in large part to large-scale

collaborations among angiosperm systematists.

Although Amborella has received considerable attention

since its noteworthy position was reported, we summarize

some of its basic attributes here. Amborella is monotypic, and

A. trichopoda is restricted to cloud forests on New Caledonia.

The plants are dioecious shrubs with vesselless xylem (but

see Feild et al. 2000). The flowers, although functionally

unisexual, have a bisexual organization: at least in the female

flowers, sterile stamens are present between tepals and carpels

(Endress and Igersheim 2000b; for additional studies

of floral development in A. trichopoda, see Posluszny and

Tomlinson 2003). The small (generally <0.5 cm in diameter)

flowers are composed of a moderate number of spirally arranged

floral organs. The perianth is undifferentiated; that

is, there is no clear distinction into sepals and petals (described

below). The carpels are completely ascidiform (i.e.,

without a conduplicate part) and are closed by secretion and

Figure 11.1. Overview of angiosperm phylogeny, showing

eudicots and major clades of basal angiosperms. The branch

uniting the eudicots with the magnoliids is only weakly

supported.

156 The Relationships of Green Plants

Figure 11.4. Archaefructus sinensis from the Early Cretaceous

(courtesy of D. L. Dilcher). (A) Reproductive shoots showing

numerous carpels and dissected leaves; note the fossil fish

skeleton at top left, indicating aquatic habitat of Archaefructus.

(B) Reconstruction, clearly showing dissected leaves and paired

stamens subtending carpels.

not by postgenital fusion (Endress and Igersheim 2000b; (see

section below titled Closed Carpels).

The Fossil Record of Early Angiosperms

The fossil record of angiosperms from the early Cretaceous

portrays tremendous diversity in size, structure, and organization

of flowers. For example, the fossil Archaeanthus from

the mid-Cretaceous (uppermost Albian to mid-Cenomanian)

supported the long-standing view (e.g., Cronquist 1968) that

the first flowers were large and Magnolia-like in size and structure

(Dilcher and Crane 1984; fig. 11.2). This view of the

early angiosperm flower prevailed among most paleobotanists

and systematists for at least the latter half of the twentieth

century.

During the past several years, views of early flowers have

changed dramatically, because of new paleobotanical techniques

of studying charcoalified mesofossils from new fossil

sites, most notably in Portugal and eastern North America

(for review, see Friis et al. 2000). These fossil deposits harbor

abundant diversity in floral morphology. Furthermore,

many extant lineages of flowering plants were established by

100–90 Mya (see Magallуn and Sanderson 2001), and many

fossils that do not appear to fit into extant groups were also

present. Despite this morphological and phylogenetic diversity,

these fossils are uniformly small, all less than 1 cm in

diameter. Among these fossils is a water lily from approximately

125 Mya (Friis et al. 2001; fig. 11.3), consistent with

the near-basal position of the extant water lily clade in molecular

phylogenetic trees.

Recent discoveries of two species described in the fossil

genus Archaefructus, A. sinensis and A. liaoningensis, have

provided new information on early angiosperms (Sun et al.

1998, 2002). The recently discovered fossils of A. sinensis are

beautifully preserved specimens at reproductive maturity

(fig. 11.4) and come from the lower part of the Yixian Formation

in Beipiao and Lingyuan of western Liaoning, China,

dated to the early Cretaceous. Although the date for this site

is not clear, the minimum age certainly places Archaefructus

as one of the oldest unambiguous angiosperm fossils. Archaefructus

sinensis has spirally arranged to whorled carpels and

paired stamens. From the dissected leaf morphology and

the abundance of fish fossils found in the same deposit,

Archaefructus is inferred to have been aquatic (Sun et al.

2002). A phylogenetic analysis that included Archaefructus

and 173 extant taxa, molecular characters from three genes

(taken from Soltis et al. 2000), and 17–108 morphological

characters (taken from Doyle and Endress 2000) concluded

that Archaefructus is the sister to all extant angiosperms (Sun

et al. 2002). However, a reanalysis of the data, including

additional material, suggests other potential placements (Friis

et al. 2003).

Based on early Cretaceous fossils such as Archaefructus

and the abundance of early to mid-Cretaceous fossils from

Portugal and eastern North America, the fossil record is most

consistent with a hypothesis of early flowers having been

fairly small. However, the diversity of form suggests an early

Figure 11.2. (A) Reconstruction of fossil genus Archaeanthus

from the mid-Cretaceous (Dilcher and Crane 1984). (B) Photograph

of modern Magnolia grandiflora. Note the similarity in floral

structure between Archaeanthus and Magnolia; Archaeanthus fits

contemporary models of the ancestral flower.

Figure 11.3. Fossil and modern water lilies. (A–C) Early

Cretaceous water lily fossils (from Friis et al. 2001); the flower

is inferred to have been no more than 1 cm in diameter. (A)

Lateral view, showing numerous scars from attachment of

stamens (24) and perianth parts (6). (B) Apical view, showing

12 carpels in the center, surrounded by rhomboidal stamen

scars and narrow elliptic perianth scars. (C) Monocolpate pollen

grain with reticulate pollen wall. (D) Modern Nuphar; note the

numerous stamens and four of six perianth parts (two additional

small, sepaloid perianth parts are not visible from this view).

The Diversification of Flowering Plants 157

radiation of angiosperms, with associated diversification in

floral structure (e.g., Friis et al. 2000). A more complete

understanding of early floral evolution will require integrated

phylogenetic analyses of extant and fossil species.

Molecular versus Fossil Ages of Angiosperms

Estimates of the age of the angiosperms and the timing of

important divergences based on molecular data do not generally

agree with each other or with dates determined from the

fossil record. For example, the age of the angiosperms has been

estimated as 350–420 Mya (Ramshaw et al. 1972), > 319 Mya

(Martin et al. 1989, 1993), 200 Mya (Wolfe et al. 1989), 160

Mya (Goremykin et al. 1996), 158–179 Mya (Wikstrцm et al.

2001), 140–190 Mya (Sanderson and Doyle 2001), and 126.9–

134.5 Mya (P. Soltis et al. 2002) using different genes and

different methods. Although some of these estimates fall close

to or slightly older than the age implied by the fossil record

(i.e., 125–135 Mya), many molecular-based estimates of the

age of the angiosperms published to date greatly exceed this

age. Many sources of error can lead to poor DNA-based estimates

of divergence times (e.g., Sanderson and Doyle 1991,

P. Soltis et al. 2002). Unequal rates of evolution among lineages,

especially when combined with inadequate sampling of

taxa, can distort estimates of divergence times based on molecular

data. A similar pattern of older molecular-based estimates

than fossil dates has been observed for other groups of

organisms, including fungi, animals, and the divergence of the

crown-group eukaryotes (e.g., Heckman et al. 2001). This

pattern has been attributed to a methodological bias such that

clock-based methods will overestimate ages (Rodrнguez-Trelles

et al. 2002). However, in at least the cases of angiosperms and

land plants (Sanderson and Doyle 2001, P. Soltis et al. 2002,

Sanderson 2003), sufficient data and appropriate sampling

have produced estimates that are generally in line with the fossil

record.

Within the angiosperms, estimated divergence times are

also generally older than indications from the fossil record

(e.g., molecular dates from Wikstrцm et al. 2001, compared

with fossil dates from Magallуn et al. 1999). However, these

discrepancies are on a much smaller scale than those reported

for the age of the angiosperms, typically differing by tens

rather than hundreds of millions of years. Further refinement

of analytical methods is needed to allow accurate estimation

of divergence times for those many groups of flowering plants

that lack a fossil record.

Major Clades of Angiosperms

Apart from the basal grade of Amborella, water lilies, and

Austrobaileyales, relationships among other basal clades of

angiosperms are less clear. The monocots and magnoliids

represent two large clades that diversified early in angiosperm

history, but their exact placements, as well as those of smaller

clades such as Ceratophyllaceae and Chloranthaceae, are not

well supported, even in analyses based on 11 genes and more

than 15,000 aligned nucleotides (Zanis et al. 2002). Ceratophyllaceae

and Chloranthaceae have fossil records that

extend back at least 125 Mya (e.g., Couper 1958, Walker and

Walker 1984, Friis et al. 2000, Dilcher 1989; for review, see

Endress 2001), placing them among the oldest angiosperm

fossils.

Monocots

The monocots are one of the largest clades of angiosperms,

with an estimated 65,000 or more species (Takhtajan 1997)

and approximately 20% of all angiosperms. Acorus is the sister

to all other monocots, and the alismatid families with a large

number of aquatic species follow Acorus as the next successive

sister group to the rest of the monocots. Key lineages

within monocots are the graminoid families (restios, sedges,

and grasses), palms, yams, gingers, lilies, and Asparagales, a

large clade that includes the orchids, irises, and hyacinths,

among other groups (fig. 11.5). Relationships among major

clades of monocots remain largely unresolved (e.g., Chase

et al. 2000), but only three genes have been sampled to infer

these relationships; ongoing collaborative research using

several additional genes should help resolve monocot phylogeny.

Based on both the fossil record and molecular clock

estimates, many lineages of monocots extend back in

the fossil record at least 80–100 Mya (e.g., Bremer 2000,

Wikstrцm et al. 2001, Gandolfo et al. 2002).

Magnoliids

The magnoliid clade, which comprises fewer than 5% of all

living species of flowering plants, contains most of the groups

considered to be “primitive angiosperms” by many previous

authors (e.g., Cronquist 1981, 1988, Takhtajan 1997) and

consists of four subclades: Magnoliales and Laurales are sisters,

and Piperales and Canellales are sisters (fig. 11.1).

Figure 11.5. Summary of monocot phylogeny. Acorus (Acorales)

and Alismatales are successive sisters to the rest of the clade.

Despite intensive study, relationships among major clades of

monocots are mostly unresolved.

158 The Relationships of Green Plants

Figure 11.7. Summary of phylogenetic relationships among

major clades of core eudicots. (A) Basal eudicots. (B) Core

eudicots.

Magnoliales, long considered the most ancient group of living

angiosperms (although phylogenetic analyses now indicate

otherwise; see above), are composed of six families of

woody plants from tropical to warm-temperate habitats.

The Magnolia family, with the Magnolia and tulip poplar

(Liriodendron), may be the most familiar family in the

order, but Magnoliales also contain Annonaceae (paw

paw family), Myristicaceae (nutmeg family), and three

small families, Degeneriaceae, Himantandraceae, and Eupomatiaceae.

The largest family of Laurales is the laurel family

(Lauraceae), and the order also contains a number of small

families (Calycanthaceae, Monimiaceae, Gomortegaceae,

Atherospermataceae, and Hernandiaceae; for review of the

phylogeny of Laurales, see Renner 1999). Canellales consist

of only two families, Canellaceae and Winteraceae; and

Piperales contain only five, Aristolochiaceae, Lactoridaceae,

Piperaceae, Hydnoraceae (Nickrent et al. 2002), and Saururaceae.

The magnoliids are weakly supported as sister to

the eudicots (Zanis et al. 2002). Although phylogenetic

evidence argues against members of the magnoliid clade as

being among the most ancient extant flowering plants, this

clade does extend back into the mid-Cretaceous (Archaeanthus;

Dilcher and Crane 1984). Furthermore, this clade may represent

an early radiation in the history of flowering plants.

Despite the small number of extant species, floral diversity

in magnoliids is extensive, with flowers ranging from the

large, showy flowers of Magnolia to the simple, perianthless

flowers of Piperaceae.

Most clades of basal angiosperms are characterized by

generally uniaperturate or uniaperturate-derived pollen

grains (fig. 11.6; see Sampson 2000). This type of pollen is

also produced by all extant and fossil gymnosperms. In contrast,

triaperturate (or triaperturate-derived) pollen is produced

by a single large clade of angiosperms, the eudicots

(see below; Donoghue and Doyle 1989, Doyle and Hotton

1991). In fact, this single pollen character is the only nonmolecular

synapomorphy identified for this clade that contains

approximately 75% of all angiosperm species (Drinnan

et al. 1994). The distinction between uniaperturate and triaperturate

pollen is clear in the fossil record, making assignment

of fossil specimens to the eudicot clade unambiguous.

Furthermore, the pollen record clearly shows that the earliest

triaperturate pollen appeared 125 Mya. Moreover, the

richness of the pollen record makes the age of 125 Mya one

of the most secure dates in the paleobotanical record. The

origin of the eudicots at least 125 Mya indicates that this clade

arose early in angiosperm evolution and is nearly as old as

the angiosperms themselves.

Eudicots

The eudicot clade consists of a basal grade of five main lineages

and a large clade that contains most species of eudicots

(fig. 11.7). Ranunculales, which include Ranunculaceae (buttercups,

columbines, and larkspurs) and Papaveraceae (poppies),

among others, are the sister group to all other eudicots

(e.g., Hoot et al. 1999, Soltis et al. 2000, Kim et al. 2003).

Other basal lineages are Proteales (proteas, sycamores, and

the water lotus, Nelumbo), Sabiaceae, Trochodendraceae, and

Buxaceae (boxwoods), but relationships among these groups

and their relationships to the core eudicots are not completely

clear.

Most eudicots fall in the core eudicot clade (fig. 11.7).

Within the core eudicots, Gunnerales are sister to the rest of

the clade (Soltis et al. 2003), but the interrelationships among

Figure 11.6. (A) Typical uniaperturate pollen grains

of gymnosperms and noneudicots; note the single groove.

(B) Triaperturate pollen grains of eudicots; note three grooves.

The Diversification of Flowering Plants 159

the remaining six main clades of core eudicots are not resolved.

The most prominent clades of core eudicots are the

rosids and asterids, each with thousands of species, along

with the smaller Caryophyllales, Santalales, and Saxifragales

clades and the very small clade of Berberidopsis and Aextoxicon.

Because the core eudicots contain more than 70%

of all angiosperm species and most of the morphological and

physiological diversity of flowering plants, resolution of relationships

among major clades of core eudicots is needed to

clarify major patterns of evolution.

Eudicots: Gunnerales. Gunnerales consist of only two

families, Gunneraceae with the single genus Gunnera (40

species) and Myrothamnaceae with only two species of

Myrothamnus. Despite strong molecular support for the relationship

between the two families, they were not previously

considered to be close relatives, because they differ

dramatically in morphology. Plants of Myrothamnus are small,

xerophytic shrubs, whereas plants of Gunnera are small or

immense perennial herbs often from moist or humid habitats

in the Southern Hemisphere.

Eudicots: “Berberidopsidales.” This clade also contains

only two small families, Berberidopsidaceae with the genera

Berberidopsis from South America and Streptothamnus from

southeastern Australia (although Streptothamnus is sometimes

considered part of Berberidopsis) and Aextoxicaceae with a

single species of Aextoxicon. Again, despite strong molecular

support, no obvious morphological characters unite these

groups, and this clade is recognized solely on the basis of

molecular data. Both families have encyclocytic stomata, a

rare feature in angiosperms and an apparent synapomorphy

for these families. The clade has not been formally recognized

as an order (Angiosperm Phylogeny Group II 2003), despite

its strong molecular support.

Eudicots: Santalales. This clade consists of seven families,

many species of which are parasites, although some

plants photosynthesize during part of their life cycle and

obtain mostly water and dissolved nutrients from their hosts.

Untangling the relationships of parasitic plants has long been

difficult because they often exhibit morphologies that appear

to have been highly modified by their adaptation to the parasitic

habit. For example, many parasites appear to have lost

leaves, perianth parts, integuments, and chlorophyll relative

to their nonparasitic relatives (see Nickrent et al. 1998). Aerial

parasites, such as mistletoes, appear to have arisen multiple

times independently in Santalales.

Eudicots: Caryophyllales. The limits of Caryophyllales

extend beyond those of previous circumscriptions (e.g.,

Cronquist 1988, Takhtajan 1987, 1997). “Traditional Caryophyllales”

include several well-known families such as

Cactaceae (cactus family), Caryophyllaceae (pink family), and

Amaranthaceae (spinach family). The sister clades to this traditional

group include carnivorous plants in Droseraceae (sundews)

and Nepenthaceae (Old World pitcher plants) and are

now also included in Caryophyllales (Angiosperm Phylogeny

Group II 2003). Many members of Caryophyllales are

adapted to extremely harsh environmental conditions, such

as high-alkaline soils, high-salt conditions, extreme aridity,

and nutrient-poor soils. They have conquered these habitats

through a variety of adaptations, such as unusual photosynthetic

pathways [Crassulacean Acid Metabolism (CAM) and

C4], unusual morphologies (e.g., succulence), unusual methods

of nutrient uptake (e.g., carnivory), and secretion of

excessive salt by special glands.

Eudicots: Rosids. The rosids and asterids are by far the

two largest clades of core eudicots. The rosids are a clade of

extremely well-supported groups, the interrelationships of

which are not clear. This pattern is true at both the deep

nodes within the rosids and within the two large eurosid I

and II clades (fig. 11.8). Eurosid I consists of the large order

Malpighiales (examples of which are poplars, willows, passion

flowers, violets, St. John’s wort, and flax), Oxalidales

(e.g., Oxalis), and orders corresponding to the melon, oak/

hickory/walnut, legume, and rose clades. Eurosid II contains

Malvales (mallows, cotton, basswood, chocolate), Sapindales

(citrus, maples, horse chestnuts), and Brassicales (mustards,

capers, papaya, nasturtium). Three additional orders form

part of a basal split in the rosids: Myrtales (myrtles), Geraniales

(geranium), and Crossosomatales.

Despite the lack of resolution among major groups of

rosids, the rosids offer some interesting cases of chemical and

physiological evolution. One of these concerns the origin

of symbioses with nitrogen-fixing bacteria. The legumes

(Fabaceae), a prominent clade in eurosid I, are well known

for their symbiotic associations with rhizobial bacteria. However,

nodular symbioses with nitrogen-fixing bacteria are also

found in nine other families of angiosperms, and nearly all

of these symbioses are with actinomycetes rather than rhizobia.

Traditional classifications of angiosperms indicated that

these 10 families were distantly related. This inference in turn

led crop geneticists and breeders to view the genetic machin-

Figure 11.8. Pattern of radiation in the rosids. Myrtales,

Geraniales, and Crossosomatales are basal branches of rosids.

Eurosids I and II are large clades, each of which consists of

multiple lineages, shown diagrammatically to the right. Note

repeated pattern of radiation, from basal relationships in rosids

to basal relationships within eurosids I and II to additional

radiations nearer the tips.

160 The Relationships of Green Plants

ery for nitrogen-fixing symbioses to be quite simple, and

perhaps transferable among distantly related species, for

example, from a bean to cereal grasses. Early molecular phylogenetic

studies (e.g., Chase et al. 1993) indicated, however,

that these families might be fairly closely related, and more

focused analyses confirmed these ideas (Soltis et al. 1995,

1997, 2000). In fact, all of the 10 families with nodular symbiotic

associations fall in a single clade within the eurosid I

clade, along with several families that lack these symbioses.

The focused placement of all 10 families within a single clade

supports the hypothesis that there was likely a single origin

of the predisposition for symbiotic associations with nitrogen-

fixing bacteria followed by multiple refinements of symbiosis

within this clade. This finding suggests, contrary to

previous hypotheses, that the genetic transfer of the needed

machinery from a legume to a cereal may be difficult.

A second example of complex chemical evolution in the

rosids involves the origin and diversification of glucosinolate

compounds. These compounds are generally considered to be

important plant defense compounds and are perhaps best

known in the mustards and their close relatives, all classified

in Brassicaceae. However, as with nitrogen-fixing symbioses,

glucosinolates have been reported in families outside Brassicaceae,

and these groups were considered distantly related

based on traditional classifications. On the contrary, phylogenetic

analyses, based initially on morphology and ultimately

molecular data (e.g., Rodman 1991, Rodman et al.

1993, 1998), found that all but one of these families form a

single clade, now referred to as Brassicales (Angiosperm Phylogeny

Group 1998, Angiosperm Phylogeny Group II 2003),

nested well within the eurosid II clade. The only exception is

Putranjivaceae; Drypetes and Putranjiva are both reported to

produce glucosinolates. Putranjivaceae are also in the rosids,

but distantly related to Brassicales; this phylogenetic placement

suggests that glucosinolate production in Drypetes and Putranjiva

arose independently from that in Brassicales and that

glucosinolates in Putranjivaceae may be produced through

a different biosynthetic pathway (Rodman et al. 1998).

Eudicots: Saxifragales. The sister group to the rosids may

be Saxifragales, a clade of 14 families—including Saxifragaceae

(containing coral bells), Crassulaceae (stonecrops),

Grossulariaceae (gooseberries, currants), and several groups

previously not considered at all closely related to these families,

such as Altingiaceae (sweet gum), Cercidiphyllaceae,

Daphniphyllaceae, Hamamelidaceae (witch hazel), and

Paeoniaceae (peonies). These families were previously classified

in three different subclasses of angiosperms (e.g.,

Cronquist 1981, Takhtajan 1997), reflecting their morphological

diversity in habit, size, life history, and flowers. For

example, the clade includes trees, shrubs, lianas, annual and

perennial herbs, succulents, and aquatics, with further differences

in number of floral parts and the degree of fusion

of floral organs. Because of this morphological diversity,

nonmolecular synapomorphies have not yet been identified,

although features of wood anatomy and leaf venation are

similar in the woody members of the clade.

Despite strong support for Saxifragales as a clade of core

eudicots, their position is uncertain. They have variously

appeared as sister to the rosids or sister to the rest of (or most

of) the core eudicots. The diversification of Saxifragales appears

to have been contemporaneous with the initial radiations

of the eudicots, magnoliids, and monocots (Fishbein

et al. 2001). Furthermore, the oldest confirmed fossils of

Saxifragales are dated to 89.5 Mya, which is comparable with

the oldest fossils of core eudicots (Magallуn et al. 1999).

Eudicots: Asterids. The final clade of core eudicots is the

asterids, a huge clade consisting of nearly 80,000 species

classified into approximately 4700 genera and 100 families

(Thorne 1992). This clade is composed of four subclades

(e.g., Albach et al. 2001, Bremer et al. 2002): Cornales (dogwoods

and hydrangeas), Ericales (blueberries, cranberries,

azaleas, camellias, and phlox), euasterids I (= lamiids; see

Bremer et al. 2002; e.g., mints, snapdragons, tomato, and

potato), and euasterids II (= campanulids; Bremer et al. 2002;

e.g., sunflowers, carrot family, and honeysuckles and relatives).

Most analyses indicate that Cornales is a sister group

to a clade of Ericales and euasterids (e.g., Soltis et al. 2000,

Bremer et al. 2002). Relationships within clades of asterids

have been addressed by Xiang et al. (1998) for Cornales, Judd

and Kron (1993) and Anderberg et al. (2002) for Ericales,

B. and K. Bremer and their students (B. Bremer et al. 2002,

K. Bremer et al. 2001) for euasterids, Plunkett et al. (1997)

and Plunkett and Lowrey (2001) for Apiales, and Donoghue

et al. (2001, 2003) for Dipsacales.

Radiations in Angiosperm Phylogeny

A recurrent pattern in the angiosperm trees is that of radiations.

This pattern is clearly evident in the rosids, but it is

also present within the asterids, within the core eudicots, near

the base of the eudicots, within the magnoliids, within the

monocots, and even earlier in angiosperm phylogeny. Undoubtedly,

some of these radiations may be resolved by additional

data, as for basal angiosperms (e.g., Zanis et al. 2002),

but some of these starburst patterns remain even after the

analysis of several genes totaling several thousand nucleotides

(e.g., Saxifragales; Fishbein et al. 2001). Given that the eudicots

themselves originated shortly after the fossil record discloses

the origin of angiosperms as a whole, many of these

radiations actually trace back to an early point in angiosperm

history. The evolutionary history of flowering plants seems

to be one of repeated radiations, perhaps associated with

innovations and the opening up of new habitats.

Gaps in Our Knowledge of Angiosperm Phylogeny

Although many aspects of angiosperm phylogeny have been

clarified, areas of uncertainty remain. For example, are the

radiations described above true radiations, or do they simply

appear as radiations because we lack the information to

discriminate the true branching patterns of history? Additional

study should be devoted to those putative points of

The Diversification of Flowering Plants 161

major radiation, such as the core eudicots, the rosids, the

asterids, and the lilioid monocots. Relationships among the

basal nodes of the eudicot clade also need clarification. Thus,

although many of the major lineages of angiosperms and their

interrelationships have been identified in recent studies, further

study is required to resolve the topology of the angiosperm

branch of the Tree of Life and to interpret patterns of

diversification across the angiosperm clade.

Evolution of Key Angiosperm Features

The major traits that distinguish angiosperms from their

gymnospermous ancestors are all characters that have presumably

made the reproductive process more efficient in

angiosperms. Modifications occurred both in the structure

of the reproductive organs and in the set of processes that

collectively result in sexual reproduction. In this section, we

examine the evolution of three of these important features:

double fertilization and endosperm formation, closed carpels,

and the structure and organization of the perianth.

Double Fertilization and Endosperm Formation

The typical process of double fertilization in angiosperms

involves (1) the union of an egg and a single sperm nucleus

to form the zygote and (2) the union of two polar nuclei

and a second sperm nucleus to form triploid endosperm,

the nutritive material for the developing embryo (fig. 11.9).

This process involves the formation of an eight-nucleate

embryo sac.

Although double fertilization and embryo formation

occur in this manner in the vast majority of angiosperms,

some species show variation on this general theme. One important

variant is the formation of endosperm through the

union of the second sperm nucleus with a single haploid

central cell of the embryo sac, producing a diploid endosperm.

This process involves a four-nucleate embryo sac

rather than the typical eight-nucleate embryo sac produced

by most flowering plants. This variation on the general process

of sexual reproduction has been documented in detail

in Nuphar, a water lily, one of the basal lineages of flowering

plants (Williams and Friedman 2002). The same process

appears to occur in some other basal angiosperms, such as

Illicium (Friedman and Williams 2003). This phylogenetic

distribution of a four-nucleate embryo sac and diploid endosperm

formation suggests the possibility that these features

are ancestral in the angiosperms. However, there is at least

one report of an eight-nucleate embryo sac in Amborella,

which sits at the pivotal position of sister to all other angiosperms.

If Amborella indeed exhibits the typical angiosperm

processes of eight-nucleate embryo sac formation and

triploid endosperm production, then multiple changes in

embryo sac structure and endosperm formation occurred

early in the history of angiosperms. Possibilities include (1)

parallel development of the Nuphar-Illicium type of reproduction

in the water lilies and Austrobaileyales, (2) a reversion

to the Amborella type in the majority of angiosperms after the

Figure 11.9. Pattern of double fertilization and endosperm formation (redrawn from Williams

and Friedman 2002). (A and B) A seven-celled, eight-nucleate female gametophyte (embryo sac),

typical of most angiosperms. In double fertilization, one sperm unites with the egg to form a

diploid zygote, and a second sperm nucleus unites with the fused polar nuclei of the central cell

to form triploid endosperm. The three cells opposite the egg and its adjacent cells disintegrate.

(C) Four-celled female gametophyte of the water lily Nuphar. In Nuphar, and some other basal

angiosperms, one sperm fuses with the egg to form the zygote, and the second sperm unites with

the haploid nucleus of the central cell to form diploid endosperm. Redrawn and modified from

Williams and Friedman (2002).

Haploid

Egg Cell

Haploid

Egg Cell

Haploid

Egg Cell

Central Cell

Haploid

Polar Nuclei

Nuclear

Fusion

Cell Death

Diploid

Nucleus

Haploid

Nucleus

a b c

162 The Relationships of Green Plants

development of the Nuphar-Illicium type, or (3) parallel development

of the eight-nucleate type in Amborella and the

majority of angiosperms from a four-nucleate ancestor. This

fundamental aspect of angiosperm embryology requires further

study.

Closed Carpels

The closed carpel provides protection for both the ovule

before fertilization and the developing embryo and seed after

fertilization and thus represents a tremendously important

innovation in the history of plants. In addition, the closed

carpel allows for competition among pollen grains and thus

selection at the gametic level (Mulcahy 1979).

Numerous hypotheses have been presented for the origin

of the carpel, but most relate to the folding or tubular

development of a fertile leaf bearing ovules that become

tucked inside the new structure. The closure of the newly

formed carpel may have been initially by secretions. In fact,

a number of angiosperm groups have carpels that are closed

not by fusion of adjacent surfaces but by mucilaginous secretions

(Endress and Igersheim 2000a; fig. 11.10). The carpels

of Amborella, the small-flowered water lilies (Cabomba),

Austrobaileya, Trimenia, Schisandra, and Kadsura are fused

entirely by secretions, whereas those of Illicium and the largeflowered

water lilies (e.g., Nymphaea) have carpels that are

closed at least partly by fusion and partly by secretion. Within

the magnoliids, the degree of fusion increases, with less of a

role played by secretion. The carpels of the eudicots are nearly

all closed by fusion of adjacent tissues. Therefore, the ancestral

condition appears to have been closure by secretion, with

fusion evolving later, probably independently in a number

of lineages.

Evolution of a Differentiated Perianth:

Morphology and Floral Genes

Perianth is the collective term for the sepals and petals of a

flower (or the tepals, if sepals and petals are undifferentiated

from each other), and this structure plays a tremendously

important role in plant reproduction. Perianth parts provide

protection for the developing reproductive structures of the

flower when the flower is in bud. Further, a showy perianth,

typically the corolla (the collective term for the petals), is an

important attractant for pollinators. In most angiosperms, the

perianth is clearly differentiated into an outer whorl (series)

of typically green sepals and an inner whorl of typically colored

petals. However, many basal angiosperms and some

early-diverging eudicots lack a differentiated perianth, with

all perianth parts appearing identical. Multiple hypotheses

have been proposed to explain the origin of the differentiated,

or bipartite, perianth, with alternative hypotheses seeming

more likely for different groups of species (e.g., Takhtajan

1991). The form of the perianth of the original flower has

also been debated, with alternative hypotheses ranging from

a large, showy, undifferentiated perianth, as in Magnolia (e.g.,

Cronquist 1968), to a small, inconspicuous, or absent perianth

(e.g., Friis et al. 1986).

The distribution of differentiated and undifferentiated

perianths across the phylogenetic tree for angiosperms clearly

shows that a differentiated perianth arose multiple times in

the basal angiosperms and early eudicots (fig. 11.11; see also

Albert et al. 1998, Ronse DeCraene et al. 2003). Petals are

clearly not phylogenetically homologous across the angiosperms.

Furthermore, petals appear to have arisen via different

mechanisms in different groups (Takhtajan 1991) and thus

are not ontogenetically or structurally homologous either.

In contrast to stamens and carpels, sepals and petals cannot

be distinguished unambiguously by their structures and

functions; therefore, genetic data may be useful for clarifying

structural identities and homologies of perianth organs

among groups (see Kramer et al. 1998, Kramer and Irish

2000, Endress 2001, Theissen 2001). Floral organ identity

in the model angiosperm Arabidopsis thaliana (Brassicaceae)

is controlled by overlapping expression of three classes of

genes (A, B, and C class) in adjacent “whorls” of the flower

(Coen and Meyerowitz 1991; fig. 11.12). Most of the ABC

genes are members of the large MADS-box gene family that

occurs throughout plants, animals, and fungi. Expression of

A-class genes alone produces sepals, coexpression of A and

B genes yields petals, coexpression of B and C genes specifies

stamens, and C-class expression alone leads to carpel

formation (for modifications to the model, see Theissen and

Saedler 2001, Honma and Goto 2001; for review, see

Theissen 2001). This pattern of gene action in a core eudicot

with a clearly bipartite perianth can be used to evaluate the

genetic nature of undifferentiated perianth organs—tepals—

in other plant groups. Do tepals share expression patterns

with sepals or with petals, or do they exhibit their own combination

of MADS-box gene expression (e.g., Albert et al.

1998)? Conversely, can patterns of gene expression be used

Figure 11.10. Carpel closure in basal angiosperms (redrawn

from Endress and Igersheim 2001a). (1) Carpel is closed by

secretions only, as indicated by gray shading. This method of

carpel closure occurs in Amborella, the water lily Cabomba, and

Austrobaileya, Trimenia, and Schisandra of Austrobaileyales.

(2 and 3) Increasing role of congenital fusion (black shading)

and corresponding reduced role of secretions. (4) Complete

congenital fusion, as in Magnoliales, Canellales, monocots, and

eudicots.

The Diversification of Flowering Plants 163

to determine whether a structure is fundamentally a sepal

or a petal? To date, most studies of gene expression in flowers

with undifferentiated perianths (e.g., Kramer et al. 1998,

2003, Kramer and Irish 2000, Tzeng and Yang 2001, Kanno

et al. 2003) have focused on B-class genes because of their

role in petal formation in core eudicots. These studies have

generally demonstrated B-class gene expression throughout

the perianth, suggesting, perhaps, that these structures

are “petals.” However, this pattern of B-class expression

even extends to monocots such as lilies (Tzeng and Yang

2001) and tulips (van Tunen et al. 1993, Kanno et al. 2003)

with outer perianth segments that correspond positionally

to sepals. Thus, most authors agree on a “modified” ABC

model of floral organ identity in basal angiosperms, monocots,

and basal eudicots (Kramer et al. 1998, 2003, Kramer

and Irish 2000, Tzeng and Yang 2001, Kanno et al. 2003;

fig. 11.12) and suggest that gene expression patterns alone

cannot be used to infer homology of floral organs. Furthermore,

because B-class genes are expressed throughout the

perianths of both Amborella and Nuphar (a water lily; S. Kim

et al., unpubl. obs.), it appears that early angiosperms may

have exhibited diffuse expression of these organ-determining

genes throughout the flower. Later in angiosperm evolution,

expression of these genes became localized, resulting

in the uniform, predictable, synorganized flower of the core

eudicots.

Conclusions

The diversification of flowering plants has been phenomenal,

generating upward of 300,000 extant species in less than

150 million years. Flowering plants have thrived on all land

masses, and they continue to dominate, and form the basis

of, all terrestrial ecosystems. They also play crucial roles in

many aquatic, including some marine, habitats. Their evolution

has been closely tied to diversification in many other

groups of organisms, such as fungi, beetles, butterflies, flies,

and mammals. Clear understanding of all of these branches

of the Tree of Life will allow formulation and tests of hypotheses

of codiversification and coevolution.

Within angiosperms, information on phylogeny has already

guided research as diverse as ecology and genomics.

Phylogenetic information may also be crucial for conserving

rare species, eliminating invasive species, and improving crops.

Continued efforts to include all 300,000 “leaves” in the “Tree

of Flowering Plants” will ultimately generate unprecedented

and unforeseeable benefits to organismal biology and society.

Figure 11.11. Parsimony reconstruction of the evolution of differentiated versus undifferentiated

perianth in basal angiosperms using MacClade (Maddison and Maddison 1992) and a tree based

on analyses by Zanis et al. (2002), Renner (1999), Karol et al. (2000), Hoot and Crane (1995),

and Hoot (1995). A differentiated perianth has clearly distinguishable sepals and petals. Here,

“perianth differentiation” includes morphological and/or positional differentiation.

164 The Relationships of Green Plants

Acknowledgments

We thank Joel Cracraft and Michael Donoghue for inviting us to

participate in the Tree of Life Symposium and to contribute this

chapter. This work was supported in part by NSF grants DEB-

0090283 and PGR-0115684.

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IV

The Relationships of Fungi

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