6
Evolution of
Flowering Plants
ANGIOSPERM APOMORPHIES . . . . . . . . . . . . . . . . . . . . 121
Flower . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .121
Stamens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .124
Reduced Male Gametophyte . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .126
Carpel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .127
Two Integuments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .130
Reduced Female Gametophyte . . . . . . . . . . . . . . . . . . . . . . . . . . . . .130
Endosperm Formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .130
The owering plants, or angiosperms (also called Angiosper-
mae, Magnoliophyta, or Anthophyta), are a monophyletic
group currently thought to be the sister group to the gymno-
sperms (Chapter 5). Angiosperms are by far the most numer-
ous, diverse, and successful e xtant plant group, containing
well over 95% of all land plant species alive today. Flowering
plants grow in virtually every habitable region and are domi-
nant in some aquatic and most terrestrial ecosystems, the
notable exception to the latter being coniferous forests.
Angiosperms comprise the great bulk of our economically
important plants, including our most valuable food crops
(Chapter 1).
Several apomorphies distinguish the angiosperms from all
other land plants (Figure 6.1): (1) the ower, usually with an
associated perianth; (2) stamens with two lateral thecae, each
composed of two microsporangia; (3) a reduced, 3-nucleate
male gametophyte; (4) carpels and fruit formation; (5) ovules
with two integuments; (6) a reduced, 8-nucleate female game-
tophyte; (7) endosperm formation; and (8) sieve tube members.
Some of these apomorphic features, which represent the prod-
uct of a unique evolutionary event, have become further modi-
ed in particular lineages of angiosperms (see Chapters 7, 8).
Figure 6.1 shows a simpli ed cladogram of the major
groups of anigosperms. The diversity and classi cation of
these groups are discussed in Chapter 7 (Amborellales,
Nymphaeales, Austrobaileyales, Magnoliids, Ceratophyllales,
and Monocots) and Chapter 8 (Eudicots). The following is
121
Sieve Tube Members . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .132
Angiosperm Specializations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .132
Vessels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .133
ORIGIN OF ANGIOSPERMS . . . . . . . . . . . . . . . . . . . . . . . 133
REVIEW QUESTIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
EXERCISES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
REFERENCES FOR FURTHER STUDY . . . . . . . . . . . . . . . 136
a review of owering plant apomorphies and general evolu-
tionary history.
ANGIOSPERM APOMORPHIES
FLOWER
Perhaps the most obvious distinguishing feature of angio-
sperms is the ower (Figure 6.2; see Chapter 9 for detailed
terminology of ower parts). A ower can be de ned as
a modi ed, determinate shoot system bearing one or more
stamens, collectively called the androecium, and/or one or
more carpels (making up one or more pistils), collectively
called the gynoecium (see later discussion). Most angiosperm
owers are bisexual (perfect), containing both stamens and
carpels, but some are unisexual (imperfect), having only sta-
mens or carpels. In addition, most (but not all) owers have a
perianth, consisting of modi ed leaves at the base of the
shoot system.
The perianth of a ower both protects the other oral parts
during oral development and functions as an attractant for
pollination (see later discussion and Chapter 13). Most ow-
ers have a perianth of two discrete whorls or series of parts:
an outer calyx and an inner corolla (Figure 6.3A). The calyx
is generally green and photosynthetic, composed of leaf-like
sepals or (if these are fused) of calyx lobes. The corolla is
typically colorful, showy, and odoriferous and is composed
122 CHAPTER 6 evolution of flowering plants
Magnoliophyta - Angiosperms
Austrobaileyales
Chloranthaceae
Nymphaeales
Amborellales
Magnoliids
sieve tube members with companion cells
endosperm and double fertilization
female gametophyte 8-nucleate
ovules with 2 integuments
carpel and fruit
male gametophyte 3-nucleate
stamens with 2 lateral thecae
flowers (generally with perianth)
Figure 6.1 Cladogram of the angiosperms, showing apomorphies and major taxonomic groups, the latter after APG II (2003).
of individual petals or (if these are fused) of corolla lobes.
However, in some owering plants, there are two whorls of
parts, but the outer and inner whorl of perianth parts are not
otherwise differentiated, resembling one another in color and
texture. The term tepal is often used for such similar perianth
parts, and one may refer to outer tepals and inner tepals for
the two whorls (Figure 6.3B). More rarely, the perianth may
consist of a single whorl (this usually called the calyx, by
tradition) or of three or more discrete whorls (see Chapter 9).
Finally, the perianth of some owers consists of spirally
arranged units that grade from sepal-like structures on the
outside to petal-like structures on the inside, but with no clear
point of differentiation between them; in this case, the units
may be termed tepals, perianth parts, or perianth segments
(Figure 6.3C).
The components of a ower develop in a manner very sim-
ilar to leaves. In early oral development actively dividing
regions of cells grow, forming bumplike mounds of tissue,
the primordia. Typically, the primordia develop in whorls
from outside to inside, in sequence as sepal (or outer tepal)
primordia rst, petal (or inner tepal) primordia second,
stamen primordia third (often in two or more whorls), and
carpel primordia last (Figure 6.4A C). Each primordium
typically becomes innervated by one or more vascular bun-
dles (veins); primordia may also transform into a attened, or
dorsiventral (having a dorsal and ventral side) shape,
Monocotyledons
Eudicots
resembling leaves. Fusion of oral parts may occur after they
form, termed postgenital fusion. Alternatively, oral parts
may appear to be fused at maturity but may actually develop
as a single structure. For example, the basal tube of a corolla
in which the petals are fused (known as a sympetalous
corolla; see Chapter 9) may form by vertical expansion of a
ring of actively dividing tissue that develops beneath discrete
primordia; only the upper corolla lobes may develop from
discrete primordia. Overall, the resemblance of oral organs
to leaves in terms of initiating lik e leaf primordia of a veg-
etative shoot, being innervated by veins, and often having a
dorsiventral shape is why these or gans sepals, petals,
stamens, and carpels are thought to be homologous to
leaves (Chapter 2).
Ongoing studies of the molecular basis of development in
plants, especially those using the species Arabidopsis thali-
ana (termed the Drosophila of the plant world ), ha ve helped
to elucidate the genetic basis of oral development and the
nature of these presumed homologies. Research in this eld
is summarized in the ABC model of oral development, in
which gene products of the so-called A, B, and C classes
combine to produce the four major oral organs: sepals,
petals, stamens, and carpels (Figure 6.5). In this model, sepals
are expressed by A activity alone; petals by a combination of
A and B activities, stamens by a combination of B and C
activities, and carpels by C activity alone (Figure 6.5).
 Unit II evolution and diversity of plants 123

pollen
pollen tubes

{
}
anther
stamen stigma
(of androecium) filament
style pistil
(of gynoecium)

ovary

{
(Pistil may
petal consist of
(of corolla) one or more
perianth receptacle (Perianth units carpels)
sepal ovules
termed tepals or
(of calyx) pedicel perianth se gments
if similar)
Figure 6.2 A typical (diagrammatic) ower, illustrating the parts.

In addition, genes of the so-called SEPALLATA class are
needed in combination with those of the A, B, and C classes
to effect proper oral organ identity (Figure 6.5). All of these
oral organ identity genes work by producing transcription
factors in the proper location of the ower, i.e., in the
outermost, second, third, and innermost oral whorls. The
transcription factors induce the expression of other genes that
bring about the development of the four oral organs. Devel-
opmental studies like these, in a wide range of species, will
help to understand both the molecular basis of homology and
the mechanisms of evolution that have given rise to the rich
diversity of oral forms.
The ower, with its typically showy and often scented peri-
anth, evidently evolved in response to selective pressure for
the transfer of pollen by animals. Animal pollination appears
to be the primitive condition in the angiosperms, separating
them from the predominantly wind-pollinated gymnosperms
(Chapter 5). Numerous, intricate pollination mechanisms have
evolved in various angiosperm lineages. These pollination
mechanisms have largely driven the evolution of innumerable

A B C
sepal

petal

outer perianth
inner parts
tepal tepal
Figure 6.3 Various perianth types in owers. A. Perianth of two whorls, dissimilar in appearance: a calyx of sepals and a corolla of
petals (Ruta). B. Perianth of two whorls, similar in appearance: outer tepals and inner tepals (Lilium). C. Perianth undifferentiated, spiral
(Nymphaea).
124 CHAPTER 6 evolution of flowering plants

se/ot
pe/it
pe/it
st st st
st

se/ot st c
se/ot
pe/it
A B C st

Figure 6.4 Flower development. A. Early development of sepal/outer tepal (se/ot) primordia and petal/inner tepal (pe/it) primordia.
B. Later formation of stamen (st) primordia. C. More mature stamens and early initiation of carpel (c) primordia.

oral forms, accounting in large part for the distinctiveness then opens to the outside by a speci c dehiscence mecha-
of many angiosperm families (see Chapter 13 for oral nism, releasing the pollen (Figure 6.7E). (Note that anthers of
syndromes related to pollination biology). Animal pollina- some angiosperms are secondarily reduced to a single theca,
tors may include bees (Figure 6.6A), butter ies and moths known as monothecal or bisporangiate, a distinctive sys-
(Figure 6.6B), ies (Figure 6.6C), bats (Figure 6.6D,E), tematic character; see Chapters 7 9.)
and birds (Figure 6.6F). However, owers of many groups The adaptive value of the stamens of angiosperms over the
are quite reduced in size or structural complexity, often lack- microsporophylls of gymnosperms is likely connected with
ing a perianth altogether; these may be water pollinated selective pressures for the ower itself. Stamens are generally
(Figure 6.6G) or wind pollinated (Figure 6.6H). smaller and lighter than gymnosperm microsporophylls, and
stamens generally occur in bisexual owers, rather than in
STAMENS more massive, unisexual cones. Modi cations of the stamen
A distinctive apomorphy for the angiosperms is the stamen,
the male reproductive organ of a ower. Stamens are inter-
preted as modi ed microsporophylls, modi ed leaves that bears sepals petals stamens carpels
microsporangia (see Chapter 5). Microsporangia produce micro-
spores, which develop into pollen grains (Chapter 5; see later
discussion). Some stamens have a laminar (leaf-like) structure,
to which the anther is attached or embedded (Figure 6.7A).
However, the stamens of most owering plants have two
parts: a stalk, known as a lament, and the pollen bearing
part, known as the anther (Figure 6.7B). Some stamens lack
B
AP3 PI
a lament (or lamina), in which case the anther is sessile,
directly attached to the rest of the ower. A C
The angiosperm anther is a type of synangium, a fusion AP1 AP2 AG
product of sporangia. Anthers are unique in (ancestrally) con-
taining two pairs of microsporangia arranged in a bilateral
SEPALLATA
symmetry (i.e., having two mirror image halves). Each pair SEP1 SEP2
of microsporangia is typically located within a discrete half SEPALLATA
of the anther called a theca (plural, thecae; Figure 6.7C).
SEP3
Thus, such an anther consists of two thecae (termed bithecal),
each theca having two microsporangia for a total of four Figure 6.5 The ABC model of oral development. Within
(termed tetrasporangiate; Figure 6.7D). At maturity, the two each gene class are speci c genes (AP1, AP2, AP3, AG, PI, SEP1,
microsporangia of a theca typically coalesce into a single, SEP2, SEP3), identi ed in mutant forms in Arabidopsis thalliana.
contiguous chamber, called the anther locule; each theca (Diagram after Jack, 2001.)
 Unit II evolution and diversity of plants 125

A B

C D

E F

styles

G H
Figure 6.6 Flower modi cations. A. Ranunculus sp., buttercup, insect-pollinated. B. Calonyction sp., moon ower, moth-pollinated.
C. Stapelia sp., star ower, y-pollinated. D. Selenicereus, night-blooming cereus, bat-pollinated. E. Couroupida guianensis, cannonball
tree, bat-pollinated. F. Strelitzia reginae, bird of paradise, bird-pollinated. G. Phyllospadix torreyi, surf-grass, water-pollinated. H. Grass,
wind-pollinated.
126 CHAPTER 6 evolution of flowering plants
theca
anther
lamina
lament
A B C E
Figure 6.7 Stamen morphology. A. Laminar stamen, Nymphaea. B,C. Filamentous stamen, Aloe. Note anther composed of two thecae,
each with two microsporangia. D. Young anther in cross-section, showing four microsporangia. E. Cross-section of older anther at time of
dehiscence. Note that walls between adjacent microsporangia of each theca have broken down. Dehiscence line indicated by arrows.
have enabled the evolution of specialized pollination mecha-
nisms, such as those involving stamens of the proper length
or orientation to transfer pollen to a speci c pollinator, ower
heteromorphism (associated with stamens at different levels
in the ower relative to differing style/stigma lengths),
trigger devices, and very modi ed stamens such as pollinia
(see Chapters 12 and 13 for more details).
REDUCED MALE GAMETOPHYTE
Another apomorphy for the angiosperms is a reduced, three-
celled male gametophyte (Figure 6.8). No other plant group
has a male gametophyte so reduced in cell number. After each
microspore is formed by meiosis within the microsporangium,
its single nucleus divides mitotically to form two cells: a tube
cell and a generative cell (Figure 6.8A,B). When this happens,
the microspore is transformed to an immature, endosporic male
gametophyte or pollen grain (Chapter 5). The generative cell
divides one time, producing two sperm cells (Figure 6.8A).
Pollen grains are shed in either a two- or three-celled condi-
tion, depending on whether the generative cell division occurs
before or after the pollen grains are released. If pollen is
released as two-celled, then the generative cell divides within
the pollen tube as it travels down the style (Figure 6.8A).
Whether pollen grains are 2- or 3-nucleate at release can be an
important taxonomic character (Chapter 11).
The pollen grains of angiosperms, like those of gymno-
sperms, germinate during development, meaning that an
microsporangia
theca
D
anther locules
micro-
sporangia
pollen
elongate pollen tube grows out of the pollen grain wall, a
condition known as siphonogamy (Figure 6.8A,C,D). In
gymnosperms the pollen tube develops after the pollen grains
enter the micropyle of the ovule and functions as a haustorial
device (feeding from the tissues of the nucellus) for a long
period of time (see Chapter 5). In contrast, the pollen tube of
angiosperms forms immediately after transfer of pollen to the
stigma. The pollen tube of angiosperms elongates through
(and feeds upon) the tissues of the stigma and style of the
carpel and soon reaches the ovule, where it penetrates the
micropyle and transports the two sperm cells directly to
the female gametophyte (see later discussion). The sperm
cells of angiosperms lack agella or cilia and are thus non-
motile, a derived condition among the land plants. The loss of
motility may be a function of the direct transport of the sperm
cells to the micropyle of the ovule. The only other land plants
with nonmotile sperm cells are the gymnospermous conifers
(including the Gnetales), which lost sperm motility indepen-
dently of owering plants.
The adaptive signi cance of the reduced male gameto-
phytes of angiosperms is probably correlated with the evolu-
tion of a reduced female gametophyte and relatively rapid
seed development (discussed later). In gymnosperms fertil-
ization of sperm and egg occurs long after pollination, some-
times as long as a year; the male gametophytes must persist
during this long period, feeding off the tissues of the nucel-
lus. In angiosperms, however, fertilization occurs very soon
 Unit II evolution and diversity of plants 127

tube cell tube nucleus

mitosis
2 sperm cells

tube nucleus
generative cell
2 sperm cells

pollen grain
(immature male pollen tube mature male
gametophyte) gametophyte
A

tube nucleus

nuclei

B generative
cell C D
Figure 6.8 Angiosperm male gametophyte. A. Development of reduced 3-nucleate male gametophyte from pollen grain. B. Mature
binucleate pollen grain, with tube nucleus and generative cell. C. Germinating pollen grain, forming pollen tube. D. Tip of pollen tube,
housing nuclear material (nuclei types unclear in this image).

after pollination. Thus, angiospermous male gametophytes
are lean, apparently requiring a minimum number of cells
and nuclei; they function to deliver sperm cells to the female
gametophyte and effect fertilization very rapidly compared
with gymnosperms.
CARPEL
A major apomorphy of angiosperms is the carpel. According
to the most widely accepted hypothesis, the carpel constitutes
a modi ed, conduplicate megasporophyll bearing two, adax-
ial rows of ovules (Figure 6.9D). (Recall that a me gasporo-
phyll is a modi ed leaf that bears megasporangia, which
in the seed plants are components of the ovules and seeds;
see Chapter 5. Conduplicate means inw ardly folded longi-
tudinally and along the central margin; see Chapter 9.)
This megasporophyll is modi ed in that the margins by
virtue of the conduplicate folding come together and fuse
(Figures 6.9A D, 6.10A), with certain parts differentiating
into tissue for pollen reception and pollen tube growth,
typically forming an apical stigma and style (Figure 6.9D).
At maturity the carpel body completely encloses the ovules
and seeds, accounting for the name angiosperm (Gr. angio,
vessel + sperm, seed).
The sporophyll-like nature of the carpel is evident in that
(1) it may develop like a leaf, having an initially attened,
dorsiventral shape, with an adaxial (toward the top-center of
the ower) and abaxial (away from the top-center of the
ower) surface; and (2) it has veins, typically one in the middle
termed the dorsal (median) vein or bundle, corresponding to
the midvein of a leaf, and two others near the two carpel mar-
gins termed the ventral (lateral or placental) veins/bundles
(Figures 6.9D, 6.10A). Additional veins often occur between
the dorsal and ventral bundles (e.g., Figure 6.10B), and veins
will sometimes fuse together. The veins of a carpel are
128 CHAPTER 6 evolution of flowering plants

typically collateral (see Chapter 10), with xylem on the adax-
ial side and phloem on the abaxial side. The ventral veins
become inverted in orientation after carpel formation, with the
xylem and phloem disposed 180° from their original orienta-
tion, i.e., prior to conduplicate folding (Figure 6.9D).
The carpels of some angiosperm taxa show no evidence of
a conduplicate, lea ike nature during development. It is gen-
erally accepted that these have become secondarily modi ed
or specialized, particularly in compound pistils (see later
discussion). One type, known as an ascidiate carpel, develops
from a ring of tissue that grows upward, sometimes assuming
a somewhat peltate form. However, taxa that lack a condupli-
cate carpel development usually still have inverted ventral
veins, evidence of the ancestral condition.
A given ower can have one to many carpels. If two or
more carpels are present, they may be separate from one

A B C

abaxial
stigma
adaxial
TYPICAL LEAF
dorsal style
vein ovary wall
pistil
abaxial
locule
ovule
adaxial c.s. ovary
funiculus
c.s.
D ventral
c.s.
placenta
veins

c.s.
E c.s. c.s.

Figure 6.9 The carpel, an apomorphy of the angiosperms. A–C. Scanning electron micrographs of carpel development. A. Early
formation of three carpels, showing conduplicate formation. B. Intermediate developmental stage. Note lateral contact of the three carpels.
C. Mature stage, in which carpel margins have closed in and adjacent carpels have fused into a syncarpous gynoecium (compound pistil).
D. Diagram of carpel development from early stages to mature ovary, adaxial side below. Note dorsal and ventral veins (black=xylem;
white=phloem), the latter becoming inverted. E. Diagram illustrating evolutionary sequence of carpel fusion (dashed lines=carpel boundaries).