Developmental Biology 8e Ch20

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[From Developmental Biology, Eighth Edition,
20
by Scott F. Gilbert, published by Sinauer Associates, Inc.]
An Overview of Plant
Development
Susan R. Singer
Laurence McKinley Gould Professor of the Natural Sciences, Carleton College
The search for differences or fun-

THE DEVELOPMENTAL STRATEGIES OF PLANTS have evolved separately from those
of the animals over millions of years. The two kingdoms have many common-
“damental contrasts … has occupied
alities (and the land plants are sometimes referred to as “embryophytes,” call- many men’s minds, while the search
ing attention to the significance of the embryo in their life histories), but some
for commonality of principle or
of the challenges and solutions found in plants are sufficiently unique to war-
rant separate discussion in this chapter. What are the fundamental differences essential similarities, has been pur-
between development in animals and development in the land plants? sued by few; the contrasts are apt to
• Plant cells do not migrate. Plant cells are trapped within rigid cellulose loom too large, great though they
may be.
walls that generally prevent cell and tissue migration. Plants, like most
metazoan animals, develop three basic tissue systems (dermal, ground, and ” D’ARCY THOMPSON (1942)
vascular), but do not rely on gastrulation to establish this layered system of
tissues. Plant development is highly regulated by the environment, a strate-
gy that is adaptive for a stationary organism. “andDoyournotimagination;
quench your inspiration
do not
• Plants have sporic meiosis rather than gametic meiosis. That is, meiosis in
become the slave of your model.
plants produces spores, not gametes. Plant gametes are produced by mitotic
divisions following meiosis.
VINCENT VAN GOGH”
• The life cycle of land plants (as well as many other plants) includes both
diploid and haploid multicellular stages. This type of life cycle is referred
to as alternation of generations and results in two different multicellular body
plans over the life cycle of an individual.
• Plant germ cells are not set aside early in development. While this is also
the case in several animal phyla, it is the case for all plants.
• Plants undergo extended morphogenesis. Clusters of actively dividing cells
called meristems, which are similar to stem cells in animals, persist long
after maturity. Meristems allow for iterative development and the formation
of new structures throughout the life of the plant.
• Plants have tremendous developmental plasticity. Many plant cells are
highly plastic. While cloning in animals also demonstrates plasticity, plants
depend far more heavily on this developmental strategy. For example, if a
shoot is grazed by herbivores, meristems in the leaf often grow out to replace
the lost part. (This strategy has similarities to the regeneration seen in some
animals.) Whole plants can be regenerated from some single cells. In addition,
a plant’s form (including branching, height, and relative amounts of vegeta-
tive and reproductive structures) is greatly influenced by environmental fac-
tors such as light and temperature, and a wide range of morphologies can
result from the same genotype (see Figure 2.15). The amazing level of plastici-
ty found among the plants may help compensate for their lack of mobility.
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628 CHAPTER 20
• Developmental mechanisms evolved independently Diploid generation Haploid generation

in plants and animals. The last common ancestor of
plants and animals was a single-celled eukaryote. MEIOSIS
Genome-level comparisons indicate that there is mini- 1n
mal homology between the genes and proteins used to Mitosis
establish body plans in plants and animals (Meyerowitz
2002). While both homeobox and MADS box genes were Path D Path A
Path C Path B
present in the last common ancestor of plants and ani- 2n 1n
mals, the MADS box family controls major developmen- organism organism
tal regulatory processes in plants, but not in animals.
Mitosis 1n
Despite the major differences among many plants and ani-
2n
mals, developmental genetic studies are revealing some FERTILIZATION Gametes
commonalities in the logic of their pattern formation, along
with evolutionarily distinct solutions to the problem of cre- 1n
ating three-dimensional form from a single cell.
The green plants include many organisms, from algae
to flowering plants (angiosperms). Recent phylogenetic FIGURE 20.1 Plants have haplodiplontic life cycles that
studies show a common lineage for all green plants, dis- involve mitotic divisions (resulting in multicellularity) in both
tinct from the red and brown plants. While comparisons the haploid and diploid generations (paths A and D). Most ani-
mals are diplontic and undergo mitosis only in the diploid gen-
of developmental strategies among diverse plants is both eration (paths B and D). Multicellular organisms with haplontic
fascinating and informative, this chapter focuses primari- life cycles follow paths A and C.
ly on the flowering plants (angiosperms). The goal is to
examine plant development within the larger context of
developmental biology. W E B S I T E 20.1 Plant life cycles. In plants there is an
evolutionary trend from sporophytes that are
Gamete Production in Angiosperms nutritionally dependent on autotrophic gameto-
phytes to the opposite—gametophytes that are
Plants have both multicellular haploid and multicellular dependent on autotrophic sporophytes. This
diploid stages in their life cycles, and embryonic develop- trend is exemplified by comparing the life cycles
ment is seen only in the diploid generation. The embryo, of mosses and ferns to that of angiosperms.
however, is produced by the fusion of gametes, which are [Note: This Web topic is included at the end of this chapter.]
formed only by the haploid generation. Understanding the
relationship between the two generations is important in bers of the animal kingdom deliver the male gameto-
the study of plant development. phyte—pollen—to the female gametophyte. Mitotic divi-
sions within the gametophytes are required to produce
gametes. The diploid sporophyte results from the fusion
Gametophytes of two gametes. Among land plants, the gametophytes and
Unlike animals, plants have multicellular haploid and mul- sporophytes of a species have distinct morphologies, and
ticellular diploid stages in their life cycles (see Chapter 2). how a single genome can be used to create two unique
Gametes develop in the multicellular haploid gametophyte morphologies is an intriguing puzzle.
(from the Greek phyton, “plant”). Fertilization gives rise to At first glance, angiosperms may appear to have diplon-
a multicellular diploid sporophyte, which produces hap- tic life cycles because the gametophyte generation has been
loid spores via meiosis. This type of life cycle is called a reduced to just a few cells (Figure 20.2). However, mitotic
haplodiplontic life cycle (Figure 20.1). It differs from the division follows meiosis in the sporophyte, resulting in a
diplontic life cycle of animals, in which only the gametes multicellular gametophyte, which produces eggs or sperm.
are in the haploid state. All of this takes place in the organ that is characteristic of
In a haplodiplontic life cycle, gametes are not the direct the angiosperms: the flower.
result of a meiotic division. Diploid sporophyte cells under-
go meiosis to produce haploid spores. Each spore goes POLLEN The pollen grain is an extremely simple multicel-
through mitotic divisions to yield a multicellular, haploid lular structure (Figure 20.3). The outer wall of the pollen
gametophyte. There are two types of spores in angio- grain, the exine, is composed of resistant material provid-
sperms. Megaspores produce female gametophytes, while ed by both the tapetum (sporophyte generation that pro-
microspores produce male gametophytes. Male and female vides nourishment for developing pollen) and the
gametophytes have distinct morphologies. Wind or mem- microspore (gametophyte generation). The inner wall, the
AN OVERVIEW OF PLANT DEVELOPMENT 629
Diploid sporophyte generation Haploid gametophyte generation
Petals Flower Microsporangium

Pollen
(2n)
Sporophyte (2n)
Microspores (1n) Gametophyte
Anther Carpel
MEIOSIS Mitosis
Stamen
Filament
Ovary
Seed Ovule
germination
Embryo sac
Megasporangium Megaspores (1n) Gametophyte
(2n)
Embryo
Endosperm Embryo sac FERTILIZATION

Pollen tube
Seed coat
FIGURE 20.2 Life cycle of an angiosperm, represented here sporangium, meiosis yields four megaspores—three small and
by a pea plant (genus Pisum). The sporophyte is the dominant one large. Only the large megaspore survives to produce the
generation, but multicellular male and female gametophytes female gametophtye (the embryo sac). Fertilization occurs
are produced within the flowers of the sporophyte. Cells of the when the male gametophyte (pollen) germinates and the
microsporangium within the anther undergo meiosis to pro- pollen tube grows toward the embryo sac. The sporophyte gen-
duce microspores. Subsequent mitotic divisions are limited, but eration may be maintained in a dormant state, protected by the
the end result is a multicellular pollen grain. Integuments and seed coat.
the ovary wall protect the megasporangium. Within the mega-
intine, is produced by the microspore. A mature pollen the pollen lands on the stigma of a female gametophyte.
grain consists of two cells: a tube cell, and a generative The generative cell divides to produce two sperm. One of
cell within the tube cell. The nucleus of the tube cell guides the two sperm will fuse with the egg cell to produce the
pollen germination and the growth of the pollen tube after next sporophyte generation. The second sperm will par-
(A) (B)
Exine
Intine FIGURE 20.3 (A) Pollen grains

have intricate surface patterns, as
Tube cell seen in this scanning electron
micrograph of aster pollen. (B) A
1n 1n pollen grain consists of a cell
Tube cell
nucleus within a cell. The generative cell
will undergo division to produce
Generative two sperm cells. One will fertilize
cell the egg, and the other will join
with the polar nuclei, yielding the
endosperm.
630 CHAPTER 20
Stigma surround the egg and the pollen tube enters the embryo
Style sac by penetrating one of the synergids. The central cell
contains two or more polar nuclei, which will fuse with the
Ovule second sperm nucleus and develop into the polyploid
Megasporangium
Ovary wall endosperm. Three antipodal cells form at the opposite end
(eventual fruit) Integuments of the embryo sac from the synergids and degenerate
before or during embryonic development. There is no
Megaspores known function for the antipodals. Genetic analyses of
Ovary
1n female gametophyte development in maize and Arabidop-
Placenta sis* are providing insight into the regulation of the specif-
Micropyle ic steps in this process (Pagnussat et al. 2005).
1n
1n
1n Pollination
Pollination refers to the landing and subsequent germina-
Sepals tion of the pollen on the stigma. Hence it involves an inter-
Placenta action between the gametophytic generation of the male
(the pollen) and the sporophytic generation of the female
FIGURE 20.4 The carpel consists of the stigma, the style, and (the stigmatic surface of the carpel). Pollination can occur
an ovary containing one or more ovules. Each ovule contains within a single perfect flower that contains both male and
megasporangia protected by two layers of integument cells. female gametophytes (self-fertilization), or pollen can land
The megasporangia divide meiotically to produce haploid on a different flower on the same or a different plant.
megaspores. All of the carpel is diploid except for the mega- About 96 percent of flowering plant species produce male
spores, which divide mitotically to produce the embryo sac
(the female gametophyte). and female gametophytes on the same plant. However,
about 25 percent of these produce two different types of
flowers on the same plant, rather than perfect flowers.
Staminate flowers lack carpels, while carpellate flow-
ers lack stamens. Maize plants, for example, have stami-
ticipate in the formation of the endosperm, a structure that nate (tassel) and carpellate (ear) flowers on the same plant.
provides nourishment for the embryo. Such species, which include the majority of the angio-
sperms, are considered to be monoecious (Greek mono,
THE OVARY The angiosperm ovary is part of the carpel of
a flower, which gives rise to the female gametophyte (Fig- *A small weed in the mustard family, Arabidopsis is used as a model
ure 20.4). The carpel consists of the stigma (where the organism because of its very small genome.
pollen lands), the style, and the ovary. Following fertiliza-
tion, the ovary wall will develop into the fruit. This unique
angiosperm structure provides further protection for the
developing embryo and also enhances seed dispersal by Antipodal cells
frugivores (fruit-eating animals). Within the ovary are one
or more ovules attached by a placenta to the ovary wall. Polar nuclei
Synergid
Fully developed ovules are called seeds.
The ovule has one or two outer layers of cells, called the
integuments. The integuments enclose the megaspo- Egg
rangium, which contains sporophyte cells that undergo
meiosis to produce megaspores (see Figure 20.2). There is
a small opening in the integuments called the micropyle,
through which the pollen tube will grow. The integuments
develop into the seed coat, a waterproof physical barrier Integuments
that protects the embryo. When the mature embryo dis- Micropyle
perses from the parent plant, diploid sporophyte tissue (pollen entry
accompanies the embryo in the form of the seed coat and point)
the fruit.
Within the ovule, meiosis and unequal cytokinesis yield FIGURE 20.5 The embryo sac is the product of three mitotic
divisions of the haploid megaspore; it comprises seven cells and
four megaspores. The largest of these megaspores under- eight haploid nuclei. The two polar nuclei in the central cell will
goes three mitotic divisions to produce the female game- fuse with the second sperm nucleus and produce the endo-
tophyte, a seven-celled embryo sac with eight nuclei (Fig- sperm that will nourish the egg. The other six cells, including
ure 20.5). One of these cells is the egg. Two synergid cells the egg, contain one haploid nucleus each.
“one”; oecos, “house”). The remaining 4 percent of species developing but stops before reaching the micropyle (Fig-
(e.g., willows, maples, and date palms*) produce stami- ure 20.6A). Sporophytic self-incompatibility occurs when one
nate and carpellate flowers on separate plants. These of the two S alleles of the pollen-producing sporophyte
species are considered to be dioecious (“two houses”). (not the gametophyte) matches one of the S alleles of the
Only a few plant species have true sex chromosomes, yet stigma (Figure 20.6B). Most likely, sporophyte contribu-
they arose several times in flowering plant evolution tions to the pollen exine are responsible for this type of self-
(Charlesworth 2002). The terms “male” and “female” are incompatibility.
most correctly applied only to the gametophyte genera- The S locus consists of several physically linked genes
tion, not to the sporophyte (Cruden and Lloyd 1995). that regulate recognition and rejection of pollen. An S gene
has been cloned that codes for an RNase (called S RNase)
SELF-INCOMPATIBILITY The arrival of a viable pollen grain that is sufficient, in the gametophytically self-incompati-
on a receptive stigma does not guarantee fertilization. ble petunia pistil, to recognize and reject self-pollen (Lee
Interspecific incompatibility refers to the failure of pollen et al. 1994). The pollen component of gametophytic self-
from one species to germinate and/or grow on the stigma incompatibility in the petunia, SLF (S-locus, F-box), is an
of another species. Intraspecific incompatibility is incom- F-box gene† within the S locus (Sijacic et al. 2004).
patibility that occurs within a species. Self-incompatibil- A different, more rapid gametophytic response to self-
ity—incompatibility between the pollen and the stigmas incompatibility has been investigated in poppies, a rela-
of the same individual—is an example of intraspecific tive of the more basal flowering plants. Calcium ions accu-
incompatibility (see Kao and Tsuikamoto 2004). Self-incom- mulate in the tip of the pollen tubes, where open calcium
patibility blocks fertilization between two genetically sim- channels are concentrated (Jaffe et al. 1975; Trewavas and
ilar gametes, increasing the probability of new gene com- Malho 1998). There is direct evidence that pollen tube
binations by promoting outcrossing (pollination by a growth in the poppy is regulated by a slow-moving Ca2+
different individual of the same species). Groups of close- wave controlled by the phosphoinositide signaling path-
ly related plants can contain a mix of self-compatible and way (Figure 20.7; Franklin-Tong et al. 1996). Ca2+ influx
self-incompatible species. occurs at both the tip of the pollen tube and on the shanks.
Several different self-incompatibility systems have Altered calcium influx is observed when the pollen tube is
evolved. Recognition of self depends on the multiallelic self-incompatible with the style, which leads to F-actin
self-incompatibility (S) locus (Nasrallah 2002). Gametophyt- depolymerization, destabilization of the pollen cytoskele-
ic self-incompatibility occurs when the S allele of the pollen ton, and cessation of pollen tube growth (Franklin-Tong et
grain matches either of the S alleles of the stigma (remem- al. 2002; Franklin-Tong and Franklin 2003). The incompat-
ber that the stigma is part of the diploid sporophyte gen- ible pollen tube then undergoes programmed cell death
eration, which has two S alleles, while a single pollen grain (Thomas and Franklin-Tong 2004).
carries one S allele). In this case, the pollen tube begins In sporophytic self-incompatibility, a ligand on the
pollen is thought to bind to a membrane-bound kinase
receptor in the stigma, starting a signaling process that
*The discovery that plants had sexes was important to the economy
of date palms in the ancient Near East over two thousand years
†
ago. Since only the female trees bore fruit, date farmers planted just Members of the F-box family of genes share a common “F-box
a few male trees, then hand-pollinated the many female trees. This domain” for binding transcription factors. Although some F-box
practice greatly increased the fruit yield per acre, and such pollina- genes have been found in other eukaryote groups, most of these
tion events became associated with spring fertility festivals. genes are unique to the plants.
(A)–Gametophytic self-incompatibility (B)–Sporophytic self-incompatibility
Pollen S1 S2 Pollen S1 S2 FIGURE 20.6 Self-incompatibility.

S1, S2, and S3 are different alleles of
the self-incompatibility (S) locus. (A)
Plants with gametophytic self-incom-
patibility reject pollen only when the
genotype of the pollen (i.e., the
gametophyte) matches either one of
the carpel’s two alleles. (B) In sporo-
phytic self-incompatibility, the geno-
type of the pollen parent (i.e., the
sporophyte), not just that of the hap-
S1/S2 S2/S3 S2/S3 S1/S2 S2/S3 S2/S3 loid pollen grain, can trigger an
Stamen Carpel Carpel Stamen Carpel Carpel incompatibility response.
632 CHAPTER 20
POLLEN GERMINATION If the pollen and the stigma are com-

patible, the pollen takes up water (hydrates) and the pollen
tube emerges. The pollen tube grows down the style of the
carpel toward the micropyle (Figure 20.9). The tube nucle-
us and the sperm cells are kept at the growing tip by bands
of callose (a complex carbohydrate). It is possible that this
Embryo may be an exception to the “plant cells do not move” rule,
sac Ovule
as the generative cell(s) appear to move forward via adhe-
Callose sive molecules (Lord 2000). Pollen tube growth is quite
plug slow in gymnosperms (up to a year), while in some
angiosperms the tube can grow as rapidly as 1 cm per hour.
e
Pollen
wav
Genetic approaches have been useful in investigating

tube
a +
how the growing pollen tube is guided toward unfertil-

fC 2
ized ovules. In Arabidopsis, the pollen tube appears to be

no
guided by a long-distance signal from the ovule (Hul-

tio
skamp et al. 1995; Wilhelmi and Preuss 1999). Analysis of

rec
pollen tube growth in ovule mutants of Arabidopsis indi-

Di
cates that the haploid embryo sac is particularly important

Sperm in the long-range guidance of pollen tube growth. Mutants
cells
Tube (A) Self-pollination (B) Cross-pollination

Ca2+ channels nucleus (self-self) (self-nonself)
FIGURE 20.7 Calcium and pollen tube tip growth. After com- å å
patible pollen germinates, the pollen tube grows toward the S1 S1
micropyle. Waves of calcium ions play a key role in this growth
of the tube. (After Franklin-Tong et al. 1996.) S2 S2
× ×
ç ç
S1 S3
leads to pollen rejection. In Brassica, one of the genes of the
S locus encodes a transmembrane serine-threonine kinase S2 S4
(SRK) that functions in the epidermis of the stigma and
binds a cysteine-rich peptide (SCR) from the pollen (Fig-
ure 20.8; Kachroo et al. 2001).
Pollen coat Stigma cell wall
There are numerous examples of plant populations that
have switched from self-incompatible to self-fertilizing sys-
tems. Changes in the S locus, specifically the SKR and SCR
genes, could account for these evolutionary changes. The
SRK-SCR NO
Nasrallahs (2002) created self-incompatible Arabidopsis
binding SRK-SCR
thaliana plants (which are normally self-compatible) by binding
introducing the SKR and SCR genes that encode self-recog-
nizing proteins from A. lyrata (a self-incompatible species).
This experiment demonstrates that A. thaliana still has all
SRK NO SRK
of the downstream components of the signal cascade that activation activation
can lead to pollen degradation. The mechanism of pollen
degradation is unclear, but appears to be highly specific.
Pollen tube inhibition Pollen tube growth
FIGURE 20.8 Receptor-ligand self-recognition is the key to

self-incompatibility in Brassicas. Allelic variability in both the SRK
and SRC genes leads to a variety of possible combinations of lig-
and and receptor proteins. Unlike the common self-recognition
systems of animals, including immunity and mating, self-incom-
patibility results from the binding of SRK and SRC proteins of
self (from allelic S loci) rather than nonself. (After Nasrallah 2002;
photographs courtesy of J. Nasrallah.)
(A) (B)
Style cells
Pollen tubes
Tube cell
Pollen nucleus
tube
Sperm nuclei
FIGURE 20.9 Pollen tube germination. (A) Scanning electron micrograph of an

Arabidopsis pollen tube en route to the ovule for fertilization. (B) Lily pollen tubes
grown in vivo and removed from the ovary. Each green strand is an individual pollen
tube and contains two sperm nuclei (bright blue stain) and a fainter (lighter blue) tube
cell nucleus. Note the huge number of pollen tubes, all “racing” to fertilize a single
egg. (Photographs courtesy of E. Lord.)
with defective sporophyte tissue in the ovule but a normal which nourishes the developing embryo. This second event
haploid embryo sac appear to stimulate normal pollen tube is not true fertilization in the sense of male and female
development. gametes undergoing syngamy (fusion)—that is, it does not
While the evidence points primarily to the role of the result in a zygote, but in nutritionally supportive endo-
gametophyte generation in pollen tube guidance, diploid derm. When you eat popcorn, you are actually eating
cells may make some contribution. The Arabidopsis gene “popped” endosperm. The other accessory cells in the
POP2 encodes an enzyme that degrades γ-amino butyric embryo sac degenerate after fertilization.
acid (GABA) and establishes a gradient of GABA in the The zygote of the angiosperm produces only a single
style up to the micropyle (Palanivelu et al. 2003). The pop2 embryo.* Double fertilization, first identified a century ago,
mutant has misguided pollen tube growth, presumably is generally restricted to the angiosperms, but it has also
because there is no GABA gradient. POP2 is expressed in been found in the gymnosperm genera Ephedra and Gne-
both the pollen and the style, which may explain why tum, although no endosperm forms. Friedman (1998) has
wild-type pollen tubes find their way to the micropyle suggested that endosperm may have evolved from a sec-
when the style has a pop2 genotype. The wild-type enzyme ond zygote “sacrificed” as a food supply in an early gym-
in the pollen tube may degrade GABA and create a suffi- nosperm lineage with double fertilization.
cient gradient to guide itself to the micropyle. Investigations of Amborella, the most closely related
As the final step in pollen guidance, the two synergid extant relative of the basal angiosperm (Figure 20.10A), is
cells in the embryo sac may attract the pollen tube. In Tore- providing information on the evolutionary origin of the
nia fournieri (wishbone flower), the embryo sac protrudes endosperm (Brown 1999). It is probable that the first
from the micropyle and can be cultured. In vitro, it can angiosperm had a four-nucleus embryo sac (Williams and
attract a pollen tube. Higashiyama and colleagues (2001) Friedman 2002, 2004). The critical cell to consider is the
used a laser beam to destroy individual cells in the embryo central cell, which is fertilized by the second sperm to cre-
sac and then tested whether or not pollen tubes were still ate the endosperm. In eight-nuclei embryo sacs, there are
attracted to the embryo sac. A single synergid was suffi- seven cells. The central cell contains two nuclei and, when
cient to guide pollen tubes; however, when both synergids fertilized, produces a triploid endosperm. In Nuphar, a
were destroyed, pollen tubes were not attracted to the sac. basal angiosperm, the embryo sac consists of four nuclei,
and the central cell has a single nucleus that, when fertil-
Fertilization ized, develops into a 2n endosperm (Figure 20.10B). The
2n endosperm provides convincing evidence that the four-
The growing pollen tube enters the embryo sac through celled embryo sac in Nuphar does not result from the degra-
the micropyle and grows through one of the synergids. The dation of four nuclei. If other cells had degraded, a 3n
two sperm cells are released, and a double fertilization endosperm would be predicted.
event occurs (see Southworth 1996). One sperm cell fuses
with the egg, producing the zygote that will develop into *The gymnosperm zygote, on the other hand, produces two or
the sporophyte. The second sperm cell fuses with the bi- more embryos after cell division begins, by a process known as
or multinucleate central cell, giving rise to the endosperm, cleavage embryogenesis.
634 CHAPTER 20
(A) (B) Synergids
FIGURE 20.10 Ancestral angiosperms.

(A) Amborella trichopoda. This plant is
more closely related to the first Egg
angiosperm than any other extant
species. (B) Ancestral angiosperms prob-
ably had 2n endosperms. The embryo
sac of the basal angiosperm Nuphar (yel-
low water lily) has a single nucleus in its
central cell , which when fertilized will
produce a 2n endosperm. DAPI staining
shows that the DNA content is 1n , not n.
Because this is a section of tissue, the
egg cell is hidden behind the two syn-
ergids and is shown in the insert.
(A photograph courtesy of Sandra K.
Floyd; B photograph courtesy of William
Freidman.)
Fertilization is not an absolute prerequisite for angi- Central cell

osperm embryonic development (Mogie 1992). Embryos
can form within embryo sacs from haploid eggs and from
cells that did not divide meiotically. This phenomenon is
called apomixis (Greek, “without mixing”), and results in
viable seeds. The viability of the resulting haploid sporo-
phytes indicates that ploidy alone does not account for the
morphological distinctions between the gametophyte and
the sporophyte. Embryos can also develop from cultured
sporophytic tissue. These embryos develop with no associ- MATERNAL EFFECTS IN EARLY EMBRYOGENESIS Maternal effect
ated endosperm, and they lack a seed coat. genes play a key role in establishing embryonic patterns
in animals (see, for example, the discussion of Drosophila
in Chapter 9). The extent of extrazygotic gene involvement
Embryonic Development in plant embryogenesis is an open question, complicated
by at least three potential sources of influence: sporophytic
Embryogenesis tissue, gametophytic tissue, and the polyploid endosperm.
In plants, the term embryogenesis covers development from All of these tissues are in close association with the egg/
the time of fertilization until dormancy occurs. The basic zygote (Ray 1998). Endosperm development could also be
body plan of the sporophyte is established during embryo- affected by maternal genes. Sporophytic and gametophyt-
genesis; however, this plan is reiterated and elaborated ic maternal effect genes have been identified in Arabidop-
after dormancy is broken. The major challenges of plant sis, and it is probable that the endosperm genome influ-
embryogenesis are: ences the zygote as well.
The first maternal effect gene identified, SHORT
•To establish the basic body plan. Radial patterning pro-
INTEGUMENTS 1 (SIN1), must be expressed in the sporo-
duces three tissue systems (dermal, ground, and vascu-
phyte for normal embryonic development to occur (Ray et
lar), and axial patterning establishes the apical-basal
al. 1996). Two transcription factors (FBP7 and FBP11) are
(shoot-root) axis.
needed in the petunia sporophyte for normal endosperm
•To set aside meristematic tissue for postembryonic elab-
development (Columbo et al. 1997). A female gametophyt-
oration of the body structure (leaves, roots, flowers, etc.).
ic maternal effect gene, MEDEA,* has protein domains sim-
•To establish an accessible food reserve for the germinating
ilar to those of a Drosophila maternal effect gene (Gross-
embryo until the embryo becomes autotrophic.
niklaus et al. 1998). Curiously, MEDEA is in the Polycomb
Embryogenesis is similar in all angiosperms in terms of the gene group (see Chapter 9), whose products alter chro-
establishment of the basic body plan. There are differences matin, directly or indirectly, and affect transcription.
in pattern elaboration, however, including differences in MEDEA affects an imprinted gene (see Chapter 5) that is
the precision of cell division patterns, the extent of
endosperm development, cotyledon development, and the
extent of shoot meristem development (Esau 1977; Steeves *Another name from Greek mythology, after Euripides’ Medea,
and Sussex 1989; Johri et al. 1992). who killed her own children.
(A) (B) FIGURE 20.11 Axis formation in the

brown alga Pelvetia compressa. (A) An F-
actin patch (orange) is first formed at the
point of sperm entry; the blue spot marks
the sperm pronucleus. (B) Later, light was
Direction of light
shone in the direction of the arrow. The
sperm-induced axis was overridden, and
an F-actin patch formed on the dark side,
where the rhizoid will later form. (Pho-
tographs courtesy of W. Hables.)
expressed by the female gametophyte and by maternally the rhizoid (root homologue) and anchor the rest of the
inherited alleles in the zygote, but not by paternally inher- plant, and one larger cell, which gives rise to the thallus
ited alleles (Vielle-Calzada et al. 1999). The significance of (the main body of the sporophyte). The point of sperm
maternal effect genes in establishing the sporophyte body entry fixes the position of the rhizoid end of the apical-
plan has been highlighted by Pagnussat and co-workers’ basal axis. This axis is perpendicular to the plane of the
(2005) screen of 130 female gametophytic mutants. Near- first cell division. F-actin accumulates at the rhizoid pole
ly half the mutations were in a maternal gene, further (Figure 20.11A; Kropf et al. 1999). However, light or grav-
implicating the female gametophyte or maternal genome ity can override this fixing of the axis and establish a new
in embryo development. position for cell division (Figure 20.11B; Alessa and Kropf
1999). Once the apical-basal axis is established, secretory
FIRST ASYMMETRIC DIVISION: BROWN ALGAE Polarity is estab- vesicles are targeted to the rhizoid pole of the zygote (Fig-
lished in the first cell division following fertilization. ure 20.12). These vesicles contain material for rhizoid out-
Because angiosperm embryos are deeply embedded in growth, with a cell wall of distinct macromolecular com-
multiple layers of tissue, the establishment of polarity is
also investigated in brown algae, a model system with
external fertilization (Belanger and Quatrano 2000; Brown- FIGURE 20.12 Asymmetrical cell division in brown algae.
lee 2004). The zygotes of these plants are independent of Time course from 8 to 25 hours after fertilization, showing algal
other tissues and are amenable to manipulation. The ini- cells stained with a vital membrane dye to visualize secretory
tial cell division results in one smaller cell, which will form vesicles, which appear first, and the cell plate, which begins to
appear about halfway through this sequence. (Photographs
courtesy of K. Belanger.)
8 hours after fertilization
Secretory
vesicles
Cell
plate
25 hours after fertilization
636 CHAPTER 20
Root Shoot Cotyledons

meristem meristem
Embryo
Terminal cell
2-Cell embryo
Suspensor
Zygote Basal cell Suspensor Hypophysis
FIGURE 20.13 Angiosperm embryogenesis. A representative Globular stage Heart stage Torpedo stage
dicot is shown; a monocot would develop only a single cotyle- embryo embryo embryo
don. The embryo proper forms from the terminal cell; the basal
cell divides to form the suspensor, which will degenerate as
development progresses. The point of interface between the
suspensor and the embryo is the hypophysis. While there are et al. 1994). In these mutants, abnormalities in the embryo
basic patterns of embryogenesis in angiosperms, there is proper appear prior to suspensor abnormalities.† Earlier
tremendous morphological variation among species. experiments in which the embryo proper was removed
also demonstrated that suspensors could develop like
embryos (Haccius 1963). A signal from the embryo prop-
er to the suspensor may be important in maintaining sus-
position. Targeted secretion may also help orient the first pensor identity and blocking the development of the sus-
plane of cell division. Maintenance of rhizoid versus thal- pensor as an embryo. Molecular analyses of these and
lus fate early in development depends on information in other genes are providing insight into the mechanisms of
the cell walls (Brownlee and Berger 1995). Such cell wall communication between the suspensor and the embryo
information also appears to be important in angiosperms proper (Figure 20.14C).
(see Scheres and Benfey 1999). The SUS1 gene has been renamed DCL1 (DICER-LIKE1)
because its predicted protein sequence is structurally like
FIRST ASYMMETRIC DIVISION: ANGIOSPERMS The basic body plan that of Dicer in Drosophila melanogaster and DCR-1 in
of the angiosperm laid down during embryogenesis also Caenorhabditis elegans (Schauer et al. 2002). These proteins
begins with an asymmetrical* cell division, giving rise to may control the translation of developmentally important
a terminal cell and a basal cell (Figure 20.13). The terminal mRNAs. This is an exciting discovery that will lead to a bet-
cell gives rise to the embryo proper. The basal cell forms ter understanding of the regulation of development beyond
closest to the micropyle and gives rise to the suspensor. the level of transcriptional control. Intriguingly, DCL1 has
The hypophysis is found at the interface between the sus- several alleles that were originally assumed to be complete-
pensor and the embryo proper. In some species it gives rise ly different genes regulating very different developmental
to a portion of the root cells. (The suspensor cells divide to processes in plants. DCL1 alleles include sin1 alleles. These
form a filamentous or spherical organ that degenerates mutants affect ovule development (discussed in the next
later in embryogenesis.) In both gymnosperms and section) and the transition from vegetative to reproductive
angiosperms, the suspensor orients the absorptive surface development (discussed later in the chapter). The carpel fac-
of the embryo toward its food source; in angiosperms, it tory (caf1) allele of DCL1 causes indeterminancy in floral
also appears to serve as a nutrient conduit for the devel- meristems leading to extra whorls of carpels. Extrapolat-
oping embryo. ing from Drosophila Dicer function, DCL1 protein may be
The study of embryo mutants in maize and Arabidopsis involved in cleaving small, noncoding RNAs into even
has been particularly helpful in sorting out the different smaller, 21- to 25-nucleotide, single-stranded RNA prod-
developmental pathways of embryos and suspensors. ucts that could cleave to mRNAs and affect translation.
Investigations of suspensor mutants (sus1, sus2, and rasp- Many questions about the role of microRNAs as possi-
berry1) of Arabidopsis have provided genetic evidence that ble developmental signals are arising from the work being
the suspensor has the capacity to develop embryo-like done on DCL1 alleles and on leaf asymmetry genes, which
structures (Figure 20.14A,B; Schwartz et al. 1994; Yadegari will be discussed later (Kidner and Martienssen 2005).
†
*Asymmetrical cell division is also important in later angiosperm Another intriguing characteristic of these mutants is that cell differ-
development, including the formation of guard cells of leaf stomata entiation occurs in the absence of morphogenesis. Thus, cell differen-
and of different cell types in the ground and vascular tissue systems. tiation and morphogenesis can be uncoupled in plant development.
(A) (B) (C)
Signals from
Signals from
embryo
suspensor
suppress
cells promote
embryonic
embryonic
development
development
in suspensor
cells
FIGURE 20.14 The SUS gene (a DCL1 allele) suppresses

embryonic development in the suspensor. (A) Wild-type
embryo and suspensor. (B) The suspensor of a sus mutant devel-
The globular shape of the embryo is lost as cotyledons
ops like an embryo (arrow). (C) Model showing how the embryo (“first leaves”) begin to form. Dicots have two cotyledons,
proper suppresses embryonic development in the suspensor which give the embryo a heart-shaped appearance as they
and the suspensor provides feedback information to the form. In monocots, such as maize, only a single cotyledon
embryo. (Photographs courtesy of D. Meinke.) emerges.The axial body plan is evident by this heart stage
of development (Figure 20.15B). Hormones (specifically,
auxins) may mediate the transition from radial to bilateral
RADIAL AND AXIAL PATTERNING Radial and axial patterns symmetry (Liu et al. 1993).
develop as cell division and differentiation continue (Fig-
ure 20.15). The cells of the embryo proper divide in trans- AUXIN AND THE APICAL-BASAL AXIS The hormone auxin plays
verse and longitudinal planes to form a globular stage a key role in establishing the apical-basal axis of the
embryo with several tiers of cells. Superficially, this stage embryo. Very early in embryogenesis, the family of pin-
bears some resemblance to cleavage in animals, but the formed (PIN) auxin efflux carriers are asymmetrically dis-
nucleus/cytoplasm ratio does not necessarily increase. The tributed (Figure 20.16A; Friml et al. 2003, 2004). The pinoid
emerging shape of the embryo depends on regulation of (PID) protein kinase aids in the asymmetric localization of
the planes of cell division and expansion, since the cells PIN proteins. At the 4-cell stage, auxin moves apically, but
are not able to move and reshape the embryo. Cell division by the globular stage, the efflux carriers direct the flow of
planes in the outer layer of cells become restricted, and this auxin to the hypophysis, which organizes as the root meris-
layer, called the protoderm, becomes distinct. Radial pat- tem (Figure 20.16B). Disruption of the auxin morphogenet-
terning emerges at the globular stage as the three tissue ic gradient, either through mutation or overexpression of
systems (dermal, ground, and vascular) of the plant are
initiated (Figure 20.15A). The dermal tissue (epidermis)
will form from the protoderm and contribute to the outer (A) Radial patterning
protective layers of the plant. Ground tissue (cortex and
Protoderm (B) Axial patterning
pith) forms from the ground meristem, which lies beneath
layer Cotyledon
the protoderm. The procambium, which forms at the core
of the embryo, gives rise to the vascular tissue (xylem and Ground layer
phloem), which will function in support and transport. The Procambium Shoot
differentiation of each tissue system is at least partially (vascular meristem
independent. For example, in the keule mutant of Arabidop- layer) Root–shoot
axis Procambium
sis, the dermal system is defective while the inner tissue
systems develop normally (Mayer et al. 1991). Root meristem
Globular stage
FIGURE 20.15 Radial and axial patterning. (A) Radial patterning in angiosperms begins in
the globular stage and results in the establishment of three tissue systems. (B) The axial pat-
tern (shoot-root axis) is established by the heart stage. Heart stage
638 CHAPTER 20
(A) (B) Wild type (C) PID overexpression
Embryo
Embryo
Suspensor Concentration No PIN 1

Suspensor of PIN1 auxin auxin efflux
efflux carriers carriers
Auxin transport via PIN family

auxin efflux carriers
Cells accumulating auxin
Cells producing auxin
FIGURE 20.16 An auxin gradient specifies the shoot-root axis. Auxin-induced

(A) A family of PIN auxin efflux carriers are responsible for the gene expression
early apical flow of auxin in the embryo and the shift to basal Auxin-induced
auxin flow as the apical end of the globular stage embryo gene expression
begins to produce auxin. (B,C) The PID protein kinase localizes
the PIN auxin efflux carriers. (B) In wild-type globular embryos,
PID expression leads to the accumulation of PIN1 at the basal
end of the embryo. When an auxin-response gene is fused with
GFP and expressed, basal accumulation and normal embryonic
development occur. (C) Ectopic overexpression of the PID gene
(induced by fusion to a viral promoter) eliminates basal accumu- tion (although those of some species never emerge from
lation of PIN1. The GFP-labeled auxin response gene is then the ground). In some cases—peas, for example—the food
expressed throughout the embryo proper rather than in the reserve in the endosperm is used up before germination,
basal portion of the embryo. and the cotyledons serve as the nutrient source for the ger-
minating seedling.* Even in the presence of a persistent
endosperm (as in maize), the cotyledons store food
reserves such as starch, lipids, and proteins. In many
PID allows auxin to accumulate more apically and root monocots, the cotyledon grows into a large organ pressed
development is abnormal or inhibited (Figure 20.16C). against the endosperm and aids in nutrient transfer to the
Although auxin accumulation is necessary for apical-basal seedling. Upright cotyledons can give the embryo a torpe-
polarity, an extensive study of the PIN proteins reveals that do shape. In some plants, the cotyledons grow sufficient-
auxin alone may not be sufficient to establish polarity in ly long that they must bend to fit within the confines of the
the embryo (Weijers and Jürgens 2005). seed coat. The embryo then looks like a walking stick. By
The discovery of the auxin receptor provided a link this point, the suspensor is degenerating.
between the asymmetric distribution of auxin and the The Arabidopsis LEAFY COTYLEDON1 (LEC1) gene, first
expression of auxin-induced genes (Dharmasiri et al. 2005; identified by a mutant with leaflike cotyledons (Meinke
Kipinski and Leyser 2005). In the absence of auxin, the 1994), is necessary to maintain the suspensor early in devel-
auxin response factors (ARF) are in a repressed state (Fig- opment, to specify cotyledeon identity, to initiate matura-
ure 20.17A). These genes form a heterodimer with tion, and to prevent early germination of the seed. LEC1
Aux/IAA protein, which inhibits the transcription of belongs to a gene class that is unique among the embryo-
auxin-induced genes. In the presence of auxin, the enzyme genesis genes in acting throughout the course of embryo
SCF binds Aux/IAA, catalyzing Aux/IAA ubiquitination development (Harada 2001; Kwong et al. 2003).
(Figure 20.17B). Ubiquitination targets Aux/IAA for degra-
dation by the 26S proteosome. Freed from the Aux/IAA MERISTEM ESTABLISHMENT The shoot apical meristem and
repressor, ARF can act on its own to stimulate transcrip- root apical meristem are clusters of stem cells that will per-
tion or form a homo/heterodimer with another ARF to fur-
ther modulate gene expression.
*Mendel’s famous wrinkled-seed mutant (the rugosus or r allele)
has a defect in a starch branching enzyme that affects starch, lipid,
COTYLEDONS In many plants, the cotyledons aid in nour- and protein biosynthesis in the seed and leads to defective cotyle-
ishing the plant by becoming photosynthetic after germina- dons (Bhattacharyya et al. 1990).
sist in the postembryonic plant and give rise to most of the shoot development is less tractable. The TOPLESS gene in
sporophyte body (see Jurgens 2001 for a review of apical- Arabidopsis may provide some clues. A single gene muta-
basal pattern formation). The root meristem is partially tion has been identified that converts a shoot into a root,
derived from the hypophysis in some species (see Figure but how the wild-type gene functions is still a puzzle (Long
20.15B). All other parts of the sporophyte body are derived et al. 2002).
from the embryo proper. The shoot apical meristem will initiate leaves after ger-
Genetic evidence indicates that the formation of the mination and, ultimately, the transition to reproductive
shoot and root meristems is regulated independently. From development. In Arabidopsis, the cotyledons are produced
an evolutionary perspective, this is not surprising. One of from general embryonic tissue, not from the shoot meris-
the major adaptations to terrestrial life involved the evo- tem (Barton and Poethig 1993). In many angiosperms, a
lution of a root system.* This independence is demonstrat- few leaves are initiated during embryogenesis. In the case
ed by the dek23 maize mutant and the shootmeristemless of Arabidopsis, clonal analysis points to the presence of
(STM) mutant of Arabidopsis, both of which form a root leaves in the mature embryo, even though they are not
meristem but fail to initiate a shoot meristem (Clark and morphologically well developed (Irish and Sussex 1992).
Sheridan 1986; Barton and Poethig 1993). The STM gene, Clonal analysis has demonstrated that the cotyledons and
which has a homeodomain, is expressed in the late globu- the first two true leaves of cotton plants are derived from
lar stage, before cotyledons form. Genes have also been embryonic tissue rather than an organized meristem
identified that specifically affect the development of the (Christianson 1986).
root axis during embryogenesis. Mutations of the HOBBIT Clonal analysis experiments provide information on cell
gene in Arabidopsis, for example, affect the hypophysis fates, but do not necessarily indicate whether or not cells
derivatives and eliminate root meristem function (Willem- are determined for a particular fate. Clonal analysis has
son et al. 1998). While it is clear that root and shoot devel- demonstrated that cells that divide in the wrong plane and
opmental programs are different, what triggers root or “move” to a different tissue layer often differentiate accord-
ing to their new position. Position, rather than clonal ori-
*It should be noted, however, that the nonvascular land plants, gin, appears to be the critical factor in embryo pattern for-
including the mosses, did not develop root systems. mation, suggesting some type of cell-cell communication
(Laux and Jürgens 1994).
Dormancy
(A) Auxin (Indole-3-acetic acid)
From the earliest stages of embryogenesis, there is a high
CH2COOH level of zygotic gene expression. As the embryo reaches
maturity, there is a shift from constructing the basic body
plan to creating a food reserve by accumulating storage
carbohydrates, proteins, and lipids. Genes coding for seed
N
storage proteins were among the first to be characterized
H by plant molecular biologists because of the high levels of
specific storage protein mRNAs that are present at differ-
ent times in embryonic development. The high level of
(B) No Auxin present
Aux/IAA (inhibitor) SCF (enzyme)

FIGURE 20.17 Mechanism of auxin action. (A) In the absence
ARF (transcription No transcription of auxin, auxin response factors (ARF) are in a repressed state.
factor) These genes form a heterodimer with Aux/IAA protein, which
inhibits the transcription of auxin-induced genes. (B) In the pres-
Promoter Auxin-induced gene ence of auxin, the enzyme SCF binds Aux/IAA, catalyzing
Aux/IAA ubiquitination. Ubiquitination targets Aux/IAA for
degradation by the 26S proteosome. Freed from the Aux/IAA
repressor, ARF can act on its own to stimulate transcription or
(C) Auxin present
form a homo or heterodimer with another ARF to further modu-
Auxin late gene expression.
SCF 26S proteosome
ARF Transcription Auxin-induced
Aux/IAA mRNA
+
Ubiquitin Promoter Auxin-induced gene
Protein
degradation
640 CHAPTER 20
FIGURE 20.18 Viviparous maize mutant. Each kernel on this

maize ear contains an embryo. Viviparous embryos do not go
through a dormant phase, but begin germinating while still on
the ear.
metabolic activity in the developing embryo is fueled by

continuous input from the parent plant into the ovule.
Eventually metabolism slows, and the connection of the
seed to the ovary is severed by the degeneration of the
adjacent supporting sporophyte cells. The seed desiccates
(loses water), and the integuments harden to form a tough
seed coat. The seed has entered dormancy, officially ending
embryogenesis. The embryo can persist in a dormant state
for weeks or years, a phenomenon that affords tremendous
survival value. There are even cases where seeds found
stored in ancient archaeological sites have germinated after
thousands of years of dormancy.
Maturation leading to dormancy is the result of a pre-
cisely regulated program. The viviparous mutation in maize,
for example, produces genetic lesions that block dorman-
cy (Steeves and Sussex 1989). The apical meristems of vivip-
arous mutants behave like those of ferns, with no pause
before producing postembryonic structures. The embryo
continues to develop, and seedlings emerge from the ker-
nels on the ear attached to the parent plant (Figure 20.18).
A group of plant genes have been identified that belong to
the Polycomb group, which regulates early development
in mammals, nematodes, and insects (Preuss 1999). These ground that they use up their food reserves before photo-
genes encode chromatin silencing factors, which may play synthesis is possible.
an important role in seed formation. Desiccated seeds may be only 5–20 percent water. Imbi-
Plant hormones are critical in dormancy, and linking bition is the process by which the seed rehydrates, soak-
them to genetic mechanisms is an active area of research. ing up large volumes of water and swelling to many times
The hormone abscisic acid is important in maintaining its original size. The radicle (primary embryonic root)
dormancy in many species. Gibberellins, another class of emerges from the seed first to enhance water uptake; it is
hormones, are important in breaking dormancy. protected by a root cap produced by the root apical meris-
tem. Water is essential for metabolic activity, but so is oxy-
Germination gen; a seed sitting in a glass of water will not survive. Some
species have such hard protective seed coats that they must
The postembryonic phase of plant development begins be scarified (scratched or etched) before water and oxy-
with germination. Some dormant seeds require a period gen can cross the barrier. Scarification can occur when the
of after-ripening, during which low-level metabolic activ- seed is exposed to the weather and other natural elements
ities continue to prepare the embryo for germination. High- over time, or by its exposure to acid as the seed passes
ly evolved interactions between the seed and its environ- through the gut of a frugivore (fruit eater). The frugivore
ment increase the odds that the germinating seedling will thus prepares the seed for germination, as well as dispers-
survive to produce another generation. ing it to a site where germination can take place.
Temperature, water, light, and oxygen are all key in During germination, the plant draws on the nutrient
determining the success of germination. Stratification is reserves in the endosperm or cotyledons. Interactions
the requirement for chilling (5°C) to break dormancy in between the embryo and endosperm in monocots use gib-
some seeds. In temperate climates, this adaptation ensures berellin as a signal to trigger the breakdown of starch into
that germination takes place only after the winter months sugar. As the shoot reaches the surface, the differentiation
have passed. In addition, seeds have maximum germina- of chloroplasts is triggered by light. Seedlings that germi-
tion rates at moderate temperatures of 25–30°C and often nate in the dark have long, spindly stems and do not pro-
will not germinate at extreme temperatures. Seeds such as duce chlorophyll. This environmental response allows
lettuce require light (specifically, the red light wavelengths) plants to use their limited resources to reach the soil sur-
for germination; thus seeds will not germinate so far below face, where photosynthesis will be productive.
Terminal AN OVERVIEW OF PLANT DEVELOPMENT 641

flower
Axillary
flower Inflorescence
elongation in more proximal cells. The root apical meris-
tem also gives rise to daughter cells that produce the three
tissue systems of the root (Figure 20.20A). New root api-
cal meristems are initiated from tissue within the core of
the root and emerge through the ground tissue and der-
mal tissue. Root meristems can also be derived secondari-
ly from the stem of the plant; in the case of maize, this is
Vegetative the major source of root mass.
axillary bud The shoot apical meristem produces stems, leaves, and
reproductive structures. In addition to the shoot apical
Internode meristem initiated during embryogenesis, axillary shoot
apical meristems (axillary buds; Figure 20.20B) derived
Node from the original one form in the axils (the angles between
Leaf leaf and stem). Unlike new root meristems, these arise from
blade the surface layers of the meristem.
Epicotyl
(A) Root meristems
Cotyledons Lateral root
Hypocotyl
Pericycle
Root hairs
Root apical Protoderm
meristem
Ground
FIGURE 20.19 Morphology of a generalized angiosperm
sporophyte. tissue
Procambium
Vegetative Growth
When the shoot emerges from the soil, most of the sporo- Apical
phyte body plan remains to be elaborated. Figure 20.19 meristem
shows the basic parts of the mature sporophyte plant, Root cap
which will emerge from meristems.
Meristems (B) Shoot meristems

Axillary Apical meristem
As has been mentioned, meristems are clusters of cells that
meristem
allow the basic body pattern established during embryoge-
Leaf Protoderm
nesis to be reiterated and extended after germination.
primordium
Meristematic cells are similar to stem cells in animals.* They
divide to give rise to one daughter cell that continues to be
meristematic and another that differentiates. Meristems fall Leaf
into three categories: apical, lateral, and intercalary. primordium
Apical meristems occur at the growing shoot and root
tips. Root apical meristems produce the root cap, which Ground
consists of lubricated cells that are sloughed off as the tissue
meristem is pushed through the soil by cell division and Procambium
FIGURE 20.20 Both shoots and roots develop from apical
*The similarities between plant meristem cells and animal stem meristems, with undifferentiated cells clustered at their tips.
cells may extend to the molecular level, indicating that stem cells (A) The root meristem is protected by the root cap as it pushes
existed before plants and animals pursued separate phylogenetic through the soil. Lateral roots are derived from pericycle cells
pathways. Homology has been found between genes required for deep within the root. (B) The lateral organs of the shoot (leaves
plant meristems to persist and genes expressed in Drosophila germ and axillary branches) have a superficial origin in the shoot api-
line stem cells (Cox et al. 1998). cal meristem.
642 CHAPTER 20
(A) (B) tity in the cells positioned above,

Apical meristem
and the CLV signaling pathway is
L1 proposed to negatively feed back
L2 on WUS expression to control the
L3 size of the meristem. It is possible
that POL expression is a target in
CLV1 signal transduction. STM, like
POL and WUS, plays an important
role in maintaining an undifferenti-
ated population of meristematic
cells, and STM may positively reg-
ulate WUS (Clark and Schiefelbein
1997). The interactions of these gene
products balance the rate of cell
FIGURE 20.21 Organization of the shoot apical meristem. (A) Angiosperm meristems division (which enlarges the meri-
have two or three outer layers of cells that are histologically distinct (L1, L2, and L3). While stem) and the rate of cell differenti-
cells in certain layers tend to have certain fates, they are not necessarily committed to ation in the periphery of the meri-
those fates. If a cell is shifted to a new layer, it generally develops like the other cells in stem (which decreases meristem
that layer. (B) The fates of the cell layers can be seen in a chimeric tobacco plant. One por-
tion of the meristem contains three layers of wild-type cells, while the other portion has
size) (Meyerowitz 1997).
an L2 that lacks chlorophyll. This section of the meristem has given rise to the variegated Lateral meristems are cylindri-
leaves. In wild-type plants, the L1 layer always lacks chlorophyll (except in guard cells), cal meristems found in shoots and
but in this plant the L2, too, is genetically unable to produce chlorophyll; the L3 remains roots that result in secondary
green. The L3 does not contribute to the outer edges of leaves, which is why they appear growth (an increase in stem and
white in this plant. (Photograph courtesy of M. Marcotrigiano.) root girth by the production of vas-
cular tissues). Monocots do not
have lateral meristems, but often
have intercalary meristems insert-
Angiosperm shoot apical meristems are composed of ed in their stems between mature tissues. The popping
up to three layers of cells (labeled L1, L2, and L3) on the sound you can hear in a cornfield on a summer night is
plant surface (Figure 20.21A). One way of investigating the caused by the rapid increase in stem length due to inter-
contributions of different layers to plant structure is by con- calary meristems.
structing chimeras (Figure 20.21B). Plant chimeras are com-
posed of layers having distinct genotypes with discernible
markers. When L2, for example, has a different genotype
than L1 or L3, all pollen will have the L2 genotype, indi-
cating that pollen is derived from L2. Chimeras have also
been used to demonstrate classical induction in plants, in
Stem cell
which (as in animal development) one layer influences the population
developmental pathway of an adjacent layer.
The size of the shoot apical meristem is precisely con- CLV3 CLV3
trolled by intercellular signals, most likely between layers STM STM
of the meristem (see Bäurle and Laux 2003). Mutations in
the Arabidopsis CLAVATA (CLV) genes, for example, lead to Cell Cell
differentiation WUS differentiation
increased meristem size and the production of extra
organs. CLV1, CLV2, and CLV3 all limit the number of CLV1/2
undifferentiated, stem cells in both vegetative and floral L1 L2 L3
meristems (Figure 20.22). CLV1 is a serenine-threonine
kinase that, along with the receptor-like transmembrane
CLV2 protein, form a receptor for CLV3, which is localized FIGURE 20.22 The WUS and STM proteins act to keep meris-
in the extracellular space between cell layers of the meri- tem cells in an undifferentiated state, while the products of the
stem (Clark et al. 1997; Jeong et al. 1999; Rojo et al. 2002). CLAVATA genes CLV1, CLV2, and CLV3 all limit the number of
Reddy and Meyerowitz (2005) have demonstrated that undifferentiated meristem cells. The presence of WUS indirectly
CLV3 restricts its own domain of expression to the central induces expression (upward arrow) of CLV3 in L1 and L2. CLV3 is
a ligand that binds to the CLV1/CLV2 receptor in L3 cells. This
zone by preventing the differentiation of surrounding cells. binding triggers a negative feedback signal cascade that
POLTERGEIST (POL) and WUSCHEL (WUS) are redun- inhibits WUS expression and regulates the number of undiffer-
dant in function and appear to keep genes in an undifferentiated cells in the meristem, thus counterbalancing the roles
entiatied state (Yu et al. 2000). WUS specifies stem cell iden- of STM and WUS in keeping cells undifferentiated and dividing.
Positional information
Root development (A)
Radial and axial patterning in roots begins during embryo-
genesis and continues throughout development as the pri-
mary root grows and lateral roots emerge from the pericy-
cle cells deep within the root. Both clonal analyses and laser
ablation experiments that elilminate single cells have Daughter Cortex Endo-
cell cell dermal
demonstrated that cells are plastic, and that position is the cell
primary determinant of fate in early root development.
Analyses of mutations in root radial organization have Cortex/ Cortex/ Cortex/
revealed genes with layer-specific activity (Scheres et al. endodermal endodermal endodermal
1995; Scheres and Heidstra 1999). We will illustrate these initial initial initial
findings by looking at two Arabidopsis genes that regulate
ground tissue fate.
In wild-type Arabidopsis, there are two layers of root
ground tissue. The outer layer becomes the cortex while the
inner layer becomes the endodermis, which forms a tube
around the vascular tissue core. The SCARECROW (SCR) (B) Root (C) Shoot
and SHORT-ROOT (SHR) genes have mutant phenotypes
with only a single layer of root ground tissue (Benfey et al.
1993). The SCR gene is necessary for an asymmetrical cell
division in the initial layer of cells, yielding a smaller endo-
dermal cell and a larger cortex cell (Figure 20.23). The scr
mutant expresses markers for both cortex and endodermal
cells, indicating that differentiation progresses in the
absence of cell division (Di Laurenzio et al. 1996). SHR is
responsible for endodermal cell specification. Cells in the
shr mutant do not develop endodermal features.
Axial patterning in roots may be morphogen-depend-
ent, paralleling some aspects of animal development. A (D) Wild type (E) scr mutant
variety of experiments have established that the distribu-
tion of the plant hormone auxin organizes the axial pat- Ep
C
tern. A peak in auxin concentration at the root tip must be
perceived for normal axial patterning (Sabatini et al. 1999; En V
Ueda et al. 2005).
M V P
As discussed earlier, distinct genes specifying root and
shoot meristem formation have been identified; however, Ep
root and shoot development may share common groups of
genes that regulate cell fate and patterning (Benfey 1999). P
This appears to be the case for the SCR and SHR genes. In
the shoot, these genes are necessary for the normal gravit- (F) shr mutant
ropic response, which is dependent on normal endodermis
formation (a defect in mutants of both genes; see Figure
20.29C). It is important to keep in mind that there are a FIGURE 20.23 SCR and SHR
number of steps between establishment of the basic pattern regulate endodermal differ-
and elaboration of that pattern into anatomical and mor- entiation in root radial devel- Ep
opment. (A) Diagram of nor-
phological structure. Uncovering the underlying control V
mal cell division yielding
mechanisms is likely to be the most productive strategy in cortical and endodermal cells.
understanding how roots and shoots develop. SCR regulates this asymmetri- M
cal cell division. (B,C) SCR P
expression in root and shoot.
Shoot development The SCR promoter is linked to
the gene for GFP (green fluo-
The unique aboveground architectures of different plant
rescent protein). (D–F) Cross sections of primary roots of (D)
species have their origins in shoot meristems. Shoot archi- wild-type Arabidopsis, (E) scr mutant, and (F) shr mutant. Ep, epi-
tecture is affected by the amount of axillary bud outgrowth. dermis; C, cortex; En, endodermis; M, mutant layer; P, pericycle;
Branching patterns are regulated by the shoot tip—a phe- V, vascular tissue; St, stele. (A after Scheres and Heidstra 1999;
nomenon called apical dominance—and plant hormones B–F photographs courtesy of P. Benfey.)
644 CHAPTER 20
appear to be the regulating factors. Auxin is produced by shapes. Culture experiments have assessed when leaf pri-
young leaves and transported toward the base of the leaf. mordia become determined for leaf development. Research
It can suppress the outgrowth of axillary buds. Grazing on ferns and angiosperms indicates that the youngest vis-
and flowering often release buds from apical dominance, ible leaf primordia are not determined to make a leaf;
at which time branching occurs. Cytokinins can also rather, these young primordia can develop as shoots in cul-
release buds from apical dominance. Axillary buds can ini- ture (Steeves 1966; Smith 1984). The programming for leaf
tiate their own axillary buds, so branching patterns can get development occurs later. The radial symmetry of the leaf
quite complex. Branching patterns can be regulated by primordium becomes dorsal-ventral, or flattened, in all
environmental signals so that an expansive canopy in an leaves. Two other axes, the proximal-distal and lateral axes,
open area maximizes light capture. Asymmetrical tree are also established.
crowns form when two trees grow very close to each other. The unique shapes of leaves result from regulation of
In addition to its environmental plasticity, shoot architec- cell division and cell expansion as the leaf blade develops.
ture is genetically regulated. In several species, genes have There are some cases in which selective cell death (apop-
now been identified that regulate branching patterns. tosis) is involved in the shaping of a leaf, but differential
Leaf primordia (clusters of cells that will form leaves) cell growth appears to be a more common mechanism (Gif-
are initiated at the periphery of the shoot meristem (see ford and Foster 1989).
Figure 20.20). The union of a leaf and the stem is called a
node, and stem tissue between nodes is called an intern- DORSAL-VENTRAL PATTERNING IN LEAVES Plant biologists refer
ode (see Figure 20.19). In a simplistic sense, the mature to the surface of the leaf that is closest to the stem as the
sporophyte is created by stacking node/internode units adaxial side and the more distant surface is the abaxial side.
together. Phyllotaxy, the positioning of leaves on the stem, As the leaf begins to form, the Arabidopsis genes PHABU-
involves communication among existing and newly form- LOSA (PHB) and PHAVOLUTA (PHV) initially have uni-
ing leaf primordia. Leaves may be arranged in various pat- formly expressed RNA throughout the primordium (Fig-
terns, including a spiral, 180º alternation of single leaves, ure 20.24A). The PHB and PHV proteins are postulated to
pairs, and whorls of three or more leaves at a node (Jean be receptors for an adaxial signal, which leads to the accu-
and Barabé 1998). Experimentation has revealed a number mulation of PHB and PHV on the adaxial leaf surface
of mechanisms for maintaining geometrically regular spac- (McConnell et al. 2001; Byrne 2005). Exclusion of PHB and
ing of leaves on a plant, including chemical and physical PHV from the abaxial side is caused by microRNA binding
interactions of new leaf primordia with the shoot apex and to the transcripts of the two genes, which leads to their
with existing primordia (Steeves and Sussex 1989). degradation (Kidner and Martienssen 2005). In addition,
It is not clear how a specific pattern of phyllotaxy gets the PHB- and PHV-specific microRNAs appear to increase
started. Descriptive mathematical models can replicate the methylation of their complementary PHB and PHV DNA
observed patterns, but reveal nothing about the mecha- sequences, suppressing transcription (Bao et al. 2004). Dom-
nism. Biophysical models (e.g., of the effects of stress or inant gain-of-function mutants have disrupted microRNA
strain on deposition of cell wall material, which affects cell binding sites such that these genes are expressed on both
division and elongation) attempt to bridge this gap. Devel- sides of the primordium, leading to a leaf with two adaxial
opmental genetics approaches are promising, but few phyl- sides. The sequences of PHB and PHV make it likely that
lotactic mutants have been identified.* Currently there is they are activated by a lipid ligand and that this activation
much interest in the role of local auxin maxima and mini- is followed by the development of adaxial cells.
ma in determining where the next leaf primordium will KANADI (KAN) genes initiate abaxial cell differentia-
form on a meristem. The PIN gene family that plays an tion in Arabidopsis (Kerstetter et al. 2001). In situ hybridiza-
important role in embryo axis formation has also been tion shows that KAN is transiently expressed on the abax-
implicated in phyllotaxy because of the correlation between ial side of cotyledons, leaves, and initiating floral organ
localization of PIN auxin efflux carriers and primordia sit- primordia (Figure 20.24B). KAN contains a GARP domain
ing (Fleming 2005). found in transcription factors. KAN and PHB/PHV mutual-
ly suppress each other to maintain abaxial and adaxial
fates, respectively.
Leaf development Abaxial fate also appears to be specified by three mem-
Leaf development includes the cells’ commitment to bers of the YABBY gene family (Siegfried et al. 1999). The
become a leaf; establishment of the leaf axes; and morpho- exact mechanism of YABBY genes in leaf polarity is
genesis, which gives rise to a tremendous diversity of leaf unknown, although promoter deletion experiments reveal
that FILAMENTOUS, a gene in the YABBY family, is active-
ly excluded from the adaxial side of the primordium. KAN
*One candidate phyllotactic mutant is the terminal ear mutant
in maize, which has irregular phyllotaxy. The wild-type gene is
and YABBY likely have redundant functions. KAN gene
expressed in a horseshoe-shaped region, with a gap where the leaf expression is restricted to the abaxial side by PHB and
will be initiated (Veit et al. 1998). The plane of the horseshoe is per- PHV, while KAN restricts PHB and PHV expression to the
pendicular to the axis of the stem. adaxial side (Figure 20.24C).
(A) Leaf Adaxial

primordium surface
Adaxial
development
Abaxial
surface
(B)
Abaxial
development
(C)
r face Adaxial signal
l su
a xia
ce
Ad rfa PHB, PHV

su
x ial Micro RNAs bind PHB and PHV RNA
Aba
Normal
KAN
development
YABBY
FIGURE 20.24 Patterning of adaxial and abaxial leaf surfaces

of Arabidopsis. (A) PHB and PHV proteins are uniformly distrib- gene in maize. Gain-of-function mutations of KN1 cause
uted throughout the leaf primordium. MicroRNAs expressed on meristem-like bumps to form on maize leaves. In wild-type
the abaxial side specifically degrade PHB and PHV, leading to plants, this gene is expressed in meristems. KNOX genes
degradation by DICER and blocking translation. In addition,
stimulate meristem initiation and growth. Although some
microRNAs increase methylation of the complementary regions
in PHB and PHV DNA, suppressing transcription. (B) Transient YABBY genes specify abaxial leaf identity (see Figure
expression of KAN on the abaxial side of the leaf leads to the 20.24), others function by downregulating KNOX genes,
expression of YABBY genes, which in turn lead to the transcrip-
tion of other abaxial genes. (C) PHB and PHV block KAN adaxial
activity. Expression of PHB, PHV, and KAN is transient and occurs
SIMPLE LEAF
early in leaf development.
Midrib
Leaves fall into two categories, simple and compound
(Figure 20.25; see review by Sinha 1999). There is much
variety in simple leaf shape, from smooth-edged leaves to
deeply lobed oak leaves. Compound leaves are composed
of individual leaflets (and sometimes tendrils) rather than Petiole Blade
a single leaf blade. Whether simple and compound leaves
develop by the same mechanism is an open question. One
perspective is that compound leaves are highly lobed sim- COMPOUND LEAF
ple leaves. An alternative perspective is that compound Vein
leaves are modified shoots. The ancestral state for seed
Stipule
plants is believed to be compound, but for angiosperms it
is simple. Compound leaves have arisen multiple times in
the angiosperms, and it is not clear if these are reversions to
the ancestral state. Tendril
Developmental genetic approaches are being applied to
Petiole Rachis Leaflet
leaf morphogenesis. The Class I KNOX genes are home-
obox genes that include STM and the KNOTTED 1 (KN1) FIGURE 20.25 Simple and compound leaves.
646 CHAPTER 20
development, however, is consistent with the hypothesis

(A) (B)
that compound leaves are modified shoots. Looking at pat-
terns of KN1 expression over a broad range of angiosperm
taxa, Bharathan et al. (2002) demonstrated that KN1 expres-
sion is associated with compound leaf primordia, but is not
present in the developing leaf primordia of simple leaves
(Figure 20.27). These data support the conclusion that com-
pound leaves maintain shootlike activity, at least for some
time. How KN1 works in meristems and in leaf primordia
is an area of active research. In tomato leaf, KN1 causes a
(A) (B) (C)
(C)
(D) (E) (F)
LP
LP
M LP
(G) (H) (I)

FIGURE 20.26 Overexpression of Class 1 KNOX genes in
tomato. The photograph shows the single leaves of (A) a wild-
type plant, (B) a mouse ears mutant, with increased leaf com-
plexity, and (C) a transgenic plant that uses a viral promoter to
overexpress the tomato homologue (LeT6) of the KN1 gene
from maize. (Photographs courtesy of N. Sinha.)
thereby restricting where meristems form (Kumaran et al.

2002). If too much KN1 is present, YABBY is insufficient to
control KN1 expression.
When KN1, or the tomato homologue LeT6, has its pro- FIGURE 20.27 KNOX is known to occur in leaf primordia in
moter replaced with a promoter from cauliflower mosaic species making complex leaves. Here we show that species with
virus and is inserted into the genome of tomato, the gene simple leaves can also express KNOX in leaf primordia that start
is expressed at high levels throughout the plant, and the out complex but undergo secondary alteration to become sim-
leaves become “super compound” (Figure 20.26; Hareven ple. (A) Coffee simple leaf. (B) SEM of primordia (arrow) showing
et al. 1996; Janssen et al. 1998). Simple leaves become more early complexity. (C) Expression of KNOX genes in these early
leaves. (D) Anise simple leaf. (E). SEM showing early complexity.
lobed (but not compound) in response to overexpression
(F) KNOX expression in these primordia. (G) Amborella showing a
of KN1, consistent with the hypothesis that compound simple leaf that is simple throughout development (H) and has
leaves may be an extreme case of lobing in simple leaves no KNOX expression (I). LP, leaf primordia; M, meristem. (From
(Jackson 1996). The role of KN1 in shoot meristem and leaf Bharathan et al. 2002; photographs courtesy of N. Sinha.)
(A) (B) FIGURE 20.28 Leaf morphology mutants

in peas. (A) Wild-type pea plant. (B) The tl
mutant, in which tendrils are converted to
leaflets. (C) The af mutant, in which leaflets
are converted to tendrils. (D) An af tl double
mutant, which results in a “parsley leaf” phe-
notype. (Photographs courtesy of S. Singer.)
(C) (D)
decrease in the expression of a gene needed for the produc- The Vegetative-to-Reproductive
tion of the plant hormone gibberellic acid (Hay et al. 2002).
A second gene, LEAFY, is essential for the transition
Transition
from vegetative to reproductive development and also Unlike most animal systems, in which the germ line is set
appears to play a role in compound leaf development. aside during early embryogenesis, the germ line in plants
LEAFY was identified in Arabidopsis and snapdragons (in is established only after the transition from vegetative to
which it is called FLORICAULA) and has homologues in reproductive development (flowering). The vegetative and
other angiosperms. The pea homologue, UNIFOLIATA, has reproductive structures of the shoot are all derived from
a mutant phenotype in which compound leaves are the shoot meristem formed during embryogenesis. Clon-
reduced to simple leaves (Hofer and Ellis 1998). This find- al analysis indicates that no cells are set aside in the shoot
ing is also indicative of a regulatory relationship between meristem of the embryo to be used solely in the creation
shoots and compound leaves. In an intriguing evolution- of reproductive structures (McDaniel and Poethig 1988).
ary twist, UNI appears to have taken on the role of KN1 In maize, irradiating seeds causes changes in the pigmen-
genes in leaf development in peas (Sinha 2002). It appears tation of some cells. These seeds give rise to plants that
to have been co-opted from its role in flowering in this have visually distinguishable sectors descended from the
highly derived legume. mutant cells. Such sectors may extend from the vegetative
In some compound leaves, developmental decisions portion of the plant into the reproductive regions (Figure
about leaf versus tendril formation are also made. Muta- 20.29), indicating that maize embryos do not have distinct
tions of two leaf-shape genes can individually and in sum reproductive compartments.
dramatically alter the morphology of the compound pea Maximal reproductive success in angiosperms depends
leaf. The acacia (tl) mutant converts tendrils to leaflets; afil- on the timing of flowering and on balancing the number
ia (af) converts leaflet to tendrils (Marx 1987). The af tl dou- of seeds produced with the resources allocated to individ-
ble mutant has a complex architecture and resembles a ual seeds. As in animals, different strategies work best for
parsley leaf (Figure 20.28). different organisms in different environments. There is a
At a more microscopic level, the patterning of stomata great diversity of flowering patterns among the over
(openings for gas and water exchange) and trichomes 300,000 angiosperm species, yet there appears to be an
(hairs) across the leaf is also being investigated. In mono- underlying evolutionary conservation of flowering genes
cots, the stomata form in parallel files, while in dicots the and common patterns of flowering regulation.
distribution appears more random. In both cases, the pat- A simplistic explanation of the flowering process is that
terns appear to maximize the evenness of stomata distri- a signal from the leaves moves to the shoot apex and
bution. Genetic analysis is providing insight into the mech- induces flowering. In some species, this flowering signal
anisms regulating this distribution. A common gene group is a response to environmental conditions. The develop-
appears to be working in both shoots and roots, affecting mental pathways leading to flowering are regulated at
the distribution pattern of both trichomes and root hairs numerous control points in different plant organs (roots,
(Benfey 1999). cotyledons, leaves, and shoot apices) in various species,
648 CHAPTER 20
FIGURE 20.29 Clonal analysis can Tassel

be used to construct a fate map of a (male flowers)
shoot apical meristem in maize.
Seeds that are heterozygous for cer-
tain pigment genes (anthocyanins)
are irradiated so that the dominant SECTOR A
allele is lost in a few cells (a chance Length =
occurrence). All cells derived from 4 internodes
the somatic mutant will be visually
distinct from the nonmutant cells. Width = SECTOR B
Plants A and B have mutant sectors 1/8 stem Length =
that reveal the fate of cells in the circumference 2 internodes
shoot meristem of the seed. The
mutant sector in A includes both Width =
vegetative and reproductive (tassel) internodes. 1/24 stem
Thus there is no distinct developmental compart- circumference
ment that forms the tassel. The mutant sector in A
is longer and wider than the mutant sector in B.
This indicates that more cells were set aside to
contribute to the lower than to the upper intern-
odes in the shoot meristem in the seed. The actual
number of cells can be calculated by taking the
reciprocal of the fraction of the stem circumfer-
ence the sector occupies. Sector A contributes to Plant A Plant B
1/8 of the circumference of the stem; thus 8 cells
were fated to contribute to these internodes in the
seed meristem. Sector B is only 1/24 of the stem
circumference; thus 24 cells were fated to con-
tribute to these internodes. In this example, only
cells derived from the L1 are being analyzed. It is
also important to consider the possible contribu-
tions of the L2 and L3 cell layers of the shoot
meristem. (Data from McDaniel and Poethig 1988;
photographs courtesy of C. McDaniel.)
resulting in a diversity of flowering times and reproduc- respond to an internal or external signal (McDaniel et al.
tive architectures. The nature of the flowering signal, how- 1992; Singer et al. 1992; Huala and Sussex 1993). Even in
ever, remains unknown. There is now evidence that RNA herbaceous plants, there is a phase change from juvenile to
with developmental functions can move through the adult vegetative growth. For example, the EARLY PHASE
phloem, and the role of very small pieces of RNA in CHANGE (EPC) gene in maize is required to maintain the
signaling developmental mechanisms has recently been juvenile state (Vega et al. 2002). Mutant epc plants flower
recognized. early because they have fewer juvenile leaves which are dis-
tinguished from adult leaves by the presence of wax and the
absence of hairs. These epc mutants, however, have the same
Juvenility number of adult leaves as wild-type plants. Juvenile traits
Some plants, especially woody perennials, go through a are not expressed in the absence of EPC. The mechanisms
juvenile phase during which the plant cannot produce of phase change genes are just beginning to be understood.
reproductive structures even if all the appropriate environ- The Arabidopsis juvenility gene HASTY (HST), is necessary
mental signals are present (Lawson and Poethig 1995). The for microRNA processing and export from the nucleus. Loss-
transition from the juvenile to the adult stage may require of-function mutants undergo early phase change because
the acquisition of competence by the leaves or meristem to microRNAs are trapped in the nucleus (Park et al. 2005).
Floral meristem
(A) identity genes
TFL1 TFL1
Phase change Floral organ identity
(HST, EPC) Flowers Flowers genes (ABC genes)
FT FT LFY/
+ +
FD FD API
Light FT
transcript
CO FT
FIGURE 20.30 The vegetative-to-reproductive
transition. (A) Signals promoting or inhibiting
flowering can move from the roots, cotyledons,
Possible florigen?
or leaves to the shoot apex, where meristem
competence determines whether or not the
plant will respond to the signals. Leaves may also
(B) need to develop competence to respond to envi-
ronmental signals before they can produce floral
promoters. Leaves and meristems that are com-
Photoperiodic Autonomous Vernalization Giberellin petent to respond to flowering signals have
pathway pathway pathway pathway undergone a juvenile-to-adult phase change. (B)
Internal and external factors regulate whether a
meristem produces vegetative or reproductive
structures. Not all of the regulatory mechanisms
shown are used in all species, and some species
Phase change Floral meristem Floral organ
flower independently of external environmental
genes identity genes identity genes
signals.
Juvenile Adult
Inflorescence Flower
vegetative vegetative
growth formation
growth growth
Floral signals 1999). Leaves, cotyledons, and roots have been identified
Grafting and organ culture experiments, mutant analyses, as sources of floral inhibitors in some species (McDaniel et
and molecular analyses give us a framework for describ- al. 1992; Reid et al. 1996). A critical balance between
ing the reproductive transition in plants. Grafting experi- inhibitor and promoter is needed for the reproductive tran-
ments have identified the sources of signals that promote sition. In addition, vernalization, a period of chilling, can
or inhibit flowering and have provided information on the enhance the competence of shoots and leaves to perceive
developmental acquisition of meristem competence to or produce a flowering signal.
respond to these signals (Lang et al. 1977; Singer et al. 1992; The “black box” between environmental signals and the
Reid et al. 1996). Analyses of mutants and molecular char- production of a flower is vanishing rapidly, especially in
acterization of genes are yielding information on the the model plant Arabidopsis (Searle and Coupland 2004;
mechanics of these signal-response mechanisms (Levy and Achard et al. 2006). The signaling pathways from light via
Dean 1998; Hempel et al. 2000; Hecht et al. 2005). different phytochromes to key flowering genes are being
Leaves produce a graft-transmissible substance that elucidated (Figure 20.30A). CONSTANS (CO) responds to
induces flowering. In some species, this signal is produced day length, promoting flowering under long-day condi-
only under specific photoperiods (day lengths), while tions. CO activates transcription of a gene called FLOW-
other species are day-neutral and will flower under any ERING LOCUS T (FT). FT is transcribed only in the leaves,
photoperiod (Zeevaart 1984). Not all leaves may be com- but the transcript travels through the phloem (transport
petent to perceive or pass on photoperiodic signals. The tissue) from the leaf to the shoot (see Blázquez 2005). FT is
phytochrome pigments transduce these signals from the likely translated when it arrives at the shoot meristem. The
external environment. The structure of phytochrome is FT protein interacts with the transcription factor FD, which
modified by red and far-red light, and these changes can is expressed only in the shoot tip. Together these two pro-
initiate a cascade of events leading to the production of teins are responsible for the expression of regulatory genes
either floral promoter or floral inhibitor (Deng and Quail that lead to the production of flowers.
650 CHAPTER 20
Is FT the long-sought florigen? Possibly, but we don’t The inflorescence meristem probably arises through the
know if other proteins aid in the movement of FT, or if action of a gene that suppresses terminal flower formation.
other transcripts must also move through the phloem The CENTRORADIALUS (CEN) gene in snapdragons sup-
before flowering can occur. presses terminal flower formation by suppressing expres-
Some of the genes that CONSTANS protein activates in sion of FLORICAULA (FLO), which specifies floral meris-
addition to FT are also activated by transcription factors tem identity (Bradley et al. 1996). Curiously, the expression
in other, non-light-dependent, flowering pathways. Mol- of FLO is necessary for CEN to be turned on. The Arabidop-
ecular explanations are revealing redundant pathways that sis homolog of CEN (TERMINAL FLOWER 1 or TFL1) is
ensure that flowering will occur. In Arabidopsis, four sepa- expressed during the vegetative phase of development as
rable pathways leading to flowering are being elucidated. well, and has the additional function of delaying the com-
Light-dependent, vernalization-dependent, gibberellin, mitment to inflorescence development (Bradley et al. 1997).
and autonomous pathways that regulate the floral transi- Overexpression of TFL1 in transgenic Arabidopsis extends
tion have been genetically dissected (Figure 20.30B). The the time before a terminal flower forms (Ratcliffe et al.
availability of the Arabidopsis genome sequence now makes 1998). TFL1 must delay the reproductive transition.
it possible to search on a broader scale for classes of genes
that regulate critical events such as time of flowering (Rat-
cliffe and Riechmann 2002). Schmid and colleagues (2005) Floral meristem identity
created a developmental gene expression profile of almost The next step in the reproductive process is the specifica-
all the Arabidopsis genes using microarrays. The current tion of floral meristems—those meristems that will actu-
challenge is to integrate the vast amount of expression data ally produce flowers (Weigel 1995). In Arabidopsis, LEAFY
with functional analysis. (LFY), APETALA 1 (AP1), and CAULIFLOWER (CAL) are
One promising approach is the search for quantitative floral meristem identity genes (Figure 20.31). LFY is the
trait loci (QTL) that control responses to environmental homologue of FLO in snapdragons, and its upregulation
and hormonal factors. In Arabidopsis, two lines, including a during development is key to the transition to reproduc-
wild accession with natural variation in light and hormone tive development (Blázquez et al. 1997; Blázquez and
responses, were used to identify new genes (Borevitz et al. Weigel 2000). The LEAFY transcription factor can actually
2002). Once QTL are mapped, the Arabidopsis genome map move between cell layers in the meristem before activat-
makes it more likely that researchers will be able to asso- ing other flowering genes (Sessions et al. 2000). Analysis
ciate function with a specific gene. of the promoter of LFY reveals that there are separate sites
for activation by the photoperiod pathway and the
autonomous pathway. The autonomous pathway works
Inflorescence development through the binding of giberellin to the LFY promoter.
The ancestral angiosperm is believed to
have formed a terminal flower directly
from the terminal shoot apex (Stebbins (A) (B)
1974). In modern angiosperms, a vari-
ety of flowering patterns exist in which
the terminal shoot apex is indetermi-
nate, but axillary buds produce flowers.
This observation introduces an interme-
diate step into the reproductive process:
the transition of a vegetative meristem
to an inflorescence meristem, which
initiates axillary meristems that can pro-
duce floral organs, but does not directly
produce floral parts itself. The inflores-
cence is the reproductive backbone (C) (D)
(stem) that displays the flowers (see Fig-
ure 20.19).
FIGURE 20.31 Floral meristem identity

mutants. (A) Wild-type Arabidopsis. (B) The
leafy mutant. (C) The apetala1 mutant. (D)
The leafy apetala1 double mutant. (Pho-
tographs courtesy of J. Bowman.)
AP1 gene family and most likely arose as a result of gene

duplication and divergence. The FUL gene is partially
redundant to AP1 and CAL (Ferrandiz et al. 2000). CAL,
however, arose only within the brassicas through an AP1
gene duplication event, and appears to have accompanied
the domestication of cauliflower and broccoli (Purugganan
et al. 2000).
Floral meristem identity genes initiate a cascade of gene
expression that turns on region-specifying (cadastral)
genes, which further specify pattern by initiating transcrip-
tion of floral organ identity genes (Weigel 1995). SUPER-
MAN (SUP) is an example of a cadastral gene in Arabidop-
sis that plays a role in specifying boundaries for the
expression of organ identity genes. Three classes (A, B,
and C) of organ identity genes are necessary to specify the
FIGURE 20.32 Arabidopsis double mutant of ap1 and cal. four whorls of floral organs (Figure 20.33; Coen and
Since cal alone gives a wild-type phenotype, the double mutant
demonstrates the redundancy of these two genes in the flower-
Meyerowitz 1991). They are homeotic genes (but not Hox
ing pathway. (Photograph courtesy of J. Bowman.) genes; rather, most are members of the MADS box gene
family that had its origins before the divergence of animals
and plants) and include AP2, AGAMOUS (AG), AP3, and
PISTILLATA (PI) in Arabidopsis. Class A genes (AP2) alone
Expression of floral meristem identity genes is necessary specify sepal development. Class A genes and class B genes
for the transition from an inflorescence meristem to a floral (AP3 and PI) together specify petals. Class B and class C
meristem. Strong lfy mutants tend to form leafy shoots in (AG) genes are necessary for stamen formation; class C
the axils where flowers form in wild-type plants; they are
unable to make the transition to floral development. If LFY
is overexpressed, flowering occurs early. For example,
Se
when aspen was transformed with an
Se
LFY gene that was expressed through-
out the plant, the time to flowering Ca
was dramatically shortened from years Ca Ca Se
to months (Weigel and Nilsson 1995). St Pe
AP1 and CAL are closely related St Pe
and redundant genes. The cal mutant Ca Se*
looks like the wild-type plant, but ap1
cal double mutants produce inflores-
cences that look like cauliflower heads b
(Figure 20.32). More recently another a
gene, FRUITFUL (FUL), with close A c Lf
sequence similarity to AP1 and CAL, A+B Lf
has been characterized. The FRUITFUL B+C Lf
C
gene family is closely related to the Wild-type Ca St Pe Se Lf
abc
FIGURE 20.33 The ABC model for floral ac

ab
organ specification. Three classes of Ca Pe/St
genes—A, B, and C—regulate organ iden- bc
tity in flowers. The central diagram repre- Ca Pe/St
sents the wild-type flower; surrounding Ca Pe/St
diagrams represent mutants that are miss- Ca Se Pe/St
ing one or more of these gene functions Se
(indicated by the lowercase a, b, or c). Se,
sepal; Pe, petal; St, stamen; Ca, carpel; Se
Pe/St, a hybrid petal/stamen; Lf, leaf; Se*, a Se
modified sepal indicating that other genes
(possibly ovule genes) also regulate floral
organ specification. (Model of Coen and
Meyerowitz 1991.)
652 CHAPTER 20
(A) Wild-type FIGURE 20.34 Wild-type and mutant pheno-

types of the Arabidopsis class A (ap2), class B
B B (ap3, pi), and class C (ag) floral organ identity
Genes
A A C C genes. (Photographs courtesy of J. Bowman.)
Flower
structure Sepal Petal Stamen Carpel
(B) ap2 (A–)

B B
Genes
C C C C
Flower
structure Carpel Stamen
Petal Stamen Carpel
(C) ap3 and pi (B–)
Genes
A A C C
Flower Sepal Sepal Carpel Carpel

structure
(D) ag (C–)
B B dinated with that of the carpel, one would
Genes expect more ancient, independent pathways
A A A A
to exist.
Transcription of floral organ identity
Flower genes is actually the beginning rather than
Sepal Petal Petal Sepal
structure the end of flower development. One of the
amazing attributes of angiosperms is the
tremendous diversity of flower phenotypes,
many of which attract specific pollinators.
Adaxial/abaxial asymmetry in flowers is
genes alone specify carpel formation. When all of these one contributing factor to diverse floral morphologies that
homeotic genes are not expressed in a developing flower, attract pollinators. Phylogenetic evidence indicates that
floral parts become leaflike (Figure 20.34). The ABC genes this trait arose independently many times, as well as being
code for transcription factors that initiate a cascade of lost many times. The cloning of the CYCLOIDEA (CYC)
events leading to the actual production of floral parts. gene in snapdragons has led to extensive discussion of the
While the ABC model is compelling, it is not sufficient molecular mechanisms involved in the evolution of asym-
to support the hypothesis that flowers evolved from leaves. metry (Donoghue et al. 1998; Cubas et al. 2001). In snap-
Overexpressing the ABC genes in leaves does not produce dragons, CYC expression is observed on the adaxial side
petals or other flower parts. About a decade after the ABC of the floral primordium early in development. In cyc
model was proposed, a fourth class of floral organ identi- mutants, flowers have a more radial symmetry. Did CYC
ty genes, SEPALLATA (SEP), was identified (see Jack 2001). evolve independently numerous times, or are there many
These MADS box genes can convert a leaf into a petal when ways to make an asymmetrical flower? Putative CYC
ectopically expressed in the leaf. In the absence of SEP func- orthologues have been identified in other species, and one
tion, flowers become whorls of sepals (Figure 20.35). SEP plausible explanation for the multiple origins of asymme-
transcription factors form dimers with ABC or other SEP try is that the CYC gene was recruited for the same func-
transcription factors to initiate floral development. tion multiple times. The combination of developmental
In addition to the ABC and SEP genes, class D genes are and phylogenetic approaches to the study of patterning in
now being investigated that specifically regulate ovule plants promises to provide insight into the origins of the
development. The ovule evolved long before the other myriad morphological novelties that are found among the
angiosperm floral parts, and while its development is coor- angiosperms.
(A) Wild-type AN OVERVIEW OF PLANT DEVELOPMENT 653

B B
Genes
A A C C
SEP1 SEP2
Senescence
SEP3
Senescence, a developmental program leading to death,
is closely linked to flowering in many angiosperms. In
Flower
Sepal Petal Stamen Carpel some species, individual flower petals senesce following
structure
pollination; orchids, which can stay fresh for long periods
(B) Wild-type of time unless they are pollinated, are a good example.
B B Fruit ripening (and ultimately overripening) is an exam-
Genes ple of organ senescence. Whole-plant senescence leads to
A A C C the death of the entire sporophyte generation. Monocarpic
SEP1 SEP1 plants flower once and then senesce. Polycarpic plants,
such as the bristlecone pine, can live thousands of years
SEP1
(4,900 years is the current record) and flower repeatedly.
In polycarpic plants, death is accidental; in monocarpic
Flower
Sepal Sepal Sepal Sepal plants, it appears to be genetically programmed.
structure
Flowers and fruits play a key role in senescence, and
their removal can sometimes delay the process. In some
(C)
legumes, senescence can be delayed by removing the
developing seed—in other words, the embryo may trigger
Normal Arabidopsis Ectopic expression of
leaf SEP in Arabidopsis leaf
senescence in the parent plant. During flowering and fruit
development, nutrients are reallocated from other parts of
FIGURE 20.35 SEPALLATA (SEP) genes are a fourth class of the plant to support the development of the next genera-
organ identity genes. Arabidopsis plants with the triple mutation tion. The reproductive structures become a nutrient sink,
sep1–sep 2–sep 3– produce whorls of sepals and lack the other and this can lead to whole-plant senescence.
three floral organs. Ectopic expression of all three SEP genes in
leaves causes them to convert to petals.
Snapshot
Summary Plant Development
1. Plants are characterized by alternation of genera- 5. Early embryogenesis is characterized by the estab-
tions; that is, their life cycle includes both diploid lishment of the shoot-root axis and by radial pattern-
and haploid multicellular generations. ing yielding three tissue systems. Pattern emerges by
2. Land plants have evolved mechanisms to protect regulation of planes of cell division and the direc-
embryos. Angiosperm embryos develop deeply tions of cell expansion, since plant cells do not move
embedded in parent tissue. The parent tissue pro- during development.
vides nutrients and some patterning information. 6. As the angiosperm embryo matures, a food reserve
This evolutionary theme of an increasingly protected is established. Only the rudiments of the basic body
embryo is shared by both plants and animals. plan are established by the time embryogenesis ceas-
3. A multicellular diploid sporophyte produces hap- es and the seed enters dormancy.
loid spores via meiosis. These spores divide mitoti- 7. Pattern is elaborated during postembryonic devel-
cally to produce a haploid gametophyte. Mitotic opment, when meristems construct the reiterative
divisions within the gametophyte produce the structures of the plant.
gametes. The diploid sporophyte results from the 8. Unlike most animals, the germ line is not set aside
fusion of two gametes. early in plant development. Coordination of signal-
4. In angiosperms, the male gamete, pollen, arrives at ing among leaves, roots, and shoot meristems regu-
the style of the female gametophyte and effects fer- lates the transition to the reproductive state.
tilization through the pollen tube. Two sperm cells 9. Floral meristem identity genes and organ identity
move through the pollen tube: one joins with the genes enable the angiosperm flower to display a
ovum to form the zygote, and the other is involved tremendous amount of morphological diversity.
in the formation of the endosperm.
10. Reproduction may be followed by genetically pro-
grammed senescence of the parent plant.
654 CHAPTER 20
For Further Reading

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Website Topic 20.1: Plant Life Cycles
(Originally included in the Developmental Biology, Eighth Edition Companion Website)
Plants have both multicellular haploid and multicellular diploid stages in their life cycles.
Embryonic development is seen only in the diploid generation. The embryo, however, is
produced by the fusion of gametes, which are formed only by the haploid generation.
Understanding the relationship between the two generations is important in the study of plant
development.
In plants, gametes develop in the multicellular haploid gametophyte (Greek phyton, “plant”).
Fertilization gives rise to a multicellular diploid sporophyte, which produces haploid spores via
meiosis. This type of life cycle is called a haplodiplontic life cycle (Figure 1). It differs from the
diplontic life cycle of most animals, in which only the gametes are in the haploid state. In
haplodiplontic life cycles, gametes are not the direct result of a meiotic division. Diploid
sporophyte cells undergo meiosis to produce haploid spores. Each spore then goes through
mitotic divisions to yield a multicellular, haploid gametophyte. Mitotic divisions within the
gametophyte are required to produce the gametes. The diploid sporophyte results from the fusion
of two gametes. Among the Plantae, the gametophytes and sporophytes of a species have distinct
morphologies (in some algae they look alike). How a single genome can be used to create two
unique morphologies is an intriguing puzzle.
Figure 1 Plants have haplodiplontic life cycles that involve mitotic divisions
(resulting in multicellularity) in both the haploid and diploid generations (paths A
and D). Most animals are diplontic and undergo mitosis only in the diploid
generation (paths B and D). Multicellular organisms with haplontic life cycles
follow paths A and C.
All plants alternate generations. There is an evolutionary trend from sporophytes that are
nutritionally dependent on autotrophic (self-feeding) gametophytes to the opposite—
gametophytes that are dependent on autotrophic sporophytes. This trend is exemplified by
comparing the life cycles of a moss, a fern, and an angiosperm (see Figures 2-4). (Gymnosperm
life cycles bear many similarities to those of angiosperms; the distinctions will be explored in the
context of angiosperm development.)
The “leafy” moss you walk on in the woods is the gametophyte generation of that plant (Figure
2). Mosses are heterosporous, which means they make two distinct types of spores; these develop
into male and female gametophytes. Male gametophytes develop reproductive structures called
antheridia (singular, antheridium) that produce sperm by mitosis. Female gametophytes develop
archegonia (singular, archegonium) that produce eggs by mitosis. Sperm travel to a neighboring
plant via a water droplet, are chemically attracted to the entrance of the archegonium, and
fertilization results.1 The embryonic sporophyte develops within the archegonium, and the mature
sporophyte stays attached to the gametophyte. The sporophyte is not photosynthetic. Thus both
the embryo and the mature sporophyte are nourished by the gametophyte. Meiosis within the
capsule of the sporophyte yields haploid spores that are released and eventually germinate to form
a male or female gametophyte.
Figure 2 Life cycle of a moss (genus Polytrichum). The sporophyte generation is dependent on
the photosynthetic gametophyte for nutrition. Cells within the sporangium of the sporophyte
undergo meiosis to produce male and female spores, respectively. These spores divide mitotically
to produce multicellular male and female gametophytes. Differentiation of the growing tip of the
gametophyte produces antheridia in males and archegonia in females. The sperm and eggs are
produced mitotically in the antheridia and archegonia, respectively. Sperm are carried to the
archegonia in water droplets. After fertilization, the sporophyte generation develops in the
archegonium and remains attached to the female gametophyte.
Ferns follow a pattern of development similar to that of mosses, although most (but not all) ferns
are homosporous. That is, the sporophyte produces only one type of spore within a structure
called the sporangium (Figure 3). A single gametophyte can produce both male and female sex
organs. The greatest contrast between the mosses and the ferns is that both the gametophyte and
the sporophyte of the fern photosynthesize and are thus autotrophic; the shift to a dominant
sporophyte generation is taking place.2
Figure 3 Life cycle of a fern (genus Polypodium). The sporophyte generation is photosynthetic
and is independent of the gametophyte. The sporangia are protected by a layer of cells called the
indusium. This entire structure is called a sorus. Meiosis within the sporangia yields a haploid
spore. Each spore divides mitotically to produce a heart-shaped gametophyte, which differentiates
both archegonia and antheridia on one individual. The gametophyte is photosynthetic and
independent, although it is smaller than the sporophyte. Fertilization takes place when water is
available for sperm to swim to the archegonia and fertilize the eggs. The sporophyte has vascular
tissue and roots; the gametophyte does not.
At first glance, angiosperms may appear to have a diplontic life cycle because the gametophyte
generation has been reduced to just a few cells (Figure 4). However, mitotic division still follows
meiosis in the sporophyte, resulting in a multicellular gametophyte, which produces eggs or
sperm. All of this takes place in the organ that characterizes the angiosperms: the flower. Male
and female gametophytes have distinct morphologies (i.e., angiosperms are heterosporous), but
the gametes they produce no longer rely on water for fertilization. Rather, wind or members of
the animal kingdom deliver the male gametophyte “pollen” to the female gametophyte. Another
evolutionary innovation found in the gymnosperms and angiosperms is the production of a seed
coat, which adds an extra layer of protection around the embryo. A further protective layer, the
fruit, is unique to the angiosperms and aids in the dispersal of the enclosed embryos by wind or
animals.
Figure 4 Life cycle of an angiosperm, represented here by a pea plant (genus Pisum). The
sporophyte is the dominant generation, but multicellular male and female gametophytes are
produced within the flowers of the sporophyte. Cells of the microsporangium within the anther
undergo meiosis to produce microspores. Subsequent mitotic divisions are limited, but the end
result is a multicellular pollen grain. The megasporangium is protected by two layers of
integuments and the ovary wall. Within the megasporangium, meiosis yields four megaspores—
three small and one large. Only the large megaspore survives to produce the embryo sac.
Fertilization occurs when the pollen germinates and the pollen tube grows toward the embryo sac.
The sporophyte generation may be maintained in a dormant state, protected by the seed coat.
1
Have you ever wondered why there are no moss trees? Aside from the fact that the gametophytes
of mosses (and other plants) do not have the necessary structural support and transport systems to
attain tree height, it would be very difficult for a sperm to swim up a tree!
2
It is possible to have tree ferns, for two reasons. First, the gametophyte develops on the ground,
where water can facilitate fertilization. Second, unlike mosses, the fern sporophyte has vascular
tissue, which provides the support and transport system necessary to achieve substantial height.

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Chapter 20 pagestest .

qxd 8/5/10 10:35 AM Page 627

[From Developmental Biology, Eighth Edition,

The search for differences or fun-

• Developmental mechanisms evolved independently Diploid generation Haploid generation

AN OVERVIEW OF PLANT DEVELOPMENT 629

Diploid sporophyte generation Haploid gametophyte generation

Petals Flower Microsporangium

Microspores (1n) Gametophyte

Endosperm Embryo sac FERTILIZATION

Intine FIGURE 20.3 (A) Pollen grains

AN OVERVIEW OF PLANT DEVELOPMENT 631

(A)–Gametophytic self-incompatibility (B)–Sporophytic self-incompatibility

Pollen S1 S2 Pollen S1 S2 FIGURE 20.6 Self-incompatibility.

POLLEN GERMINATION If the pollen and the stigma are com-

Genetic approaches have been useful in investigating

how the growing pollen tube is guided toward unfertil-

ized ovules. In Arabidopsis, the pollen tube appears to be

guided by a long-distance signal from the ovule (Hul-

skamp et al. 1995; Wilhelmi and Preuss 1999). Analysis of

pollen tube growth in ovule mutants of Arabidopsis indi-

cates that the haploid embryo sac is particularly important

Tube (A) Self-pollination (B) Cross-pollination

Pollen tube inhibition Pollen tube growth

FIGURE 20.8 Receptor-ligand self-recognition is the key to

AN OVERVIEW OF PLANT DEVELOPMENT 633

FIGURE 20.9 Pollen tube germination. (A) Scanning electron micrograph of an

FIGURE 20.10 Ancestral angiosperms.

Fertilization is not an absolute prerequisite for angi- Central cell

AN OVERVIEW OF PLANT DEVELOPMENT 635

(A) (B) FIGURE 20.11 Axis formation in the

25 hours after fertilization

Root Shoot Cotyledons

AN OVERVIEW OF PLANT DEVELOPMENT 637

(A) (B) (C)

FIGURE 20.14 The SUS gene (a DCL1 allele) suppresses

(A) (B) Wild type (C) PID overexpression

Suspensor Concentration No PIN 1

Auxin transport via PIN family

FIGURE 20.16 An auxin gradient specifies the shoot-root axis. Auxin-induced

AN OVERVIEW OF PLANT DEVELOPMENT 639

Aux/IAA (inhibitor) SCF (enzyme)

FIGURE 20.18 Viviparous maize mutant. Each kernel on this

metabolic activity in the developing embryo is fueled by

Terminal AN OVERVIEW OF PLANT DEVELOPMENT 641

Meristems (B) Shoot meristems

(A) (B) tity in the cells positioned above,

AN OVERVIEW OF PLANT DEVELOPMENT 643

AN OVERVIEW OF PLANT DEVELOPMENT 645

(A) Leaf Adaxial

Ad rfa PHB, PHV

FIGURE 20.24 Patterning of adaxial and abaxial leaf surfaces

development, however, is consistent with the hypothesis

(A) (B) (C)

(D) (E) (F)

(G) (H) (I)

thereby restricting where meristems form (Kumaran et al.

AN OVERVIEW OF PLANT DEVELOPMENT 647

(A) (B) FIGURE 20.28 Leaf morphology mutants

FIGURE 20.29 Clonal analysis can Tassel

AN OVERVIEW OF PLANT DEVELOPMENT 649

FIGURE 20.31 Floral meristem identity

AN OVERVIEW OF PLANT DEVELOPMENT 651