Table Of ContentChapter 20 pagestest(cid:1).qxd 8/5/10 10:35 AM Page 627
[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 PLANTShave 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-
essential similarities, has been pur-
rant separate discussion in this chapter. What are the fundamental differences
sued by few; the contrasts are apt to
between development in animals and development in the land plants?
loom too large, great though they
• Plant cells do not migrate. Plant cells are trapped within rigid cellulose
may be.”
walls that generally prevent cell and tissue migration. Plants, like most
metazoan animals, develop three basic tissue systems (dermal, ground, and D’ARCYTHOMPSON(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- “Do not quench your inspiration
gy that is adaptive for a stationary organism. and your imagination; 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
VINCENTVANGOGH
divisions following meiosis.
• 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 CHAPTER20
• 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
1n
Genome-level comparisons indicate that there is mini-
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 C Path B Path A
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
the haploid and diploid generations (paths A and D). Most ani-
tinct from the red and brown plants. While comparisons
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. WEBSITE 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
haplodiplonticlife cycle (Figure 20.1). It differs from the division follows meiosis in the sporophyte, resulting in a
diplonticlife 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. Megasporesproduce female gametophytes, while ed by both the tapetum (sporophyte generation that pro-
microsporesproduce 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
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AN OVERVIEW OF PLANT DEVELOPMENT 629
Diploid sporophyte generation Haploid gametophyte generation
Petals Microsporangium
Flower Pollen
(2n)
Sporophyte (2n)
Microspores (1n) Gametophyte
Anther Carpel
MEIOSIS Mitosis
Stamen
Filament
Ovary
Seed Ovule
germination
Embryo sac
Megaspores (1n) Gametophyte
Megasporangium
(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. Amature 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
Tube cell pollen grain consists of a 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.
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630 CHAPTER20
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 cellsform 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
female gametophyte development in maize and Arabidop-
1n
sis*are providing insight into the regulation of the specif-
Placenta
Micropyle ic steps in this process (Pagnussat et al. 2005).
1n
1n
1n Pollination
Pollinationrefers to the landing and subsequent germina-
tion of the pollen on the stigma. Hence it involves an inter-
Sepals
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
and female gametophytes on the same plant. However,
(the female gametophyte).
about 25 percent of these produce two different types of
flowers on the same plant, rather than perfect flowers.
Staminateflowers lack carpels, while carpellateflow-
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-
*Asmall 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 ovulesattached by a placentato 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
Integuments
develop into the seed coat, a waterproof physical barrier
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.
FIGURE 20.5 The embryo sac is the product of three mitotic
Within the ovule, meiosis and unequal cytokinesis yield
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 sacwith 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.
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AN OVERVIEW OF PLANT DEVELOPMENT 631
“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 Salleles of the pollen-producing sporophyte
species are considered to be dioecious (“two houses”). (not the gametophyte) matches one of the Salleles 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 Slocus consists of several physically linked genes
tion, not to the sporophyte (Cruden and Lloyd 1995). that regulate recognition and rejection of pollen. An Sgene
has been cloned that codes for an RNase (called SRNase)
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 incompatibilityrefers 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 incompatibilityis incom- F-box gene†within the Slocus (Sijacic et al. 2004).
patibility that occurs within a species. Self-incompatibil- Adifferent, 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 Sallele of the pollen ton, and cessation of pollen tube growth (Franklin-Tong et
grain matches either of the Salleles 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 Salleles, 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 S3are 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.
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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,
Ovule
sac 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
e angiosperms the tube can grow as rapidly as 1 cm per hour.
Pollen wav Genetic approaches have been useful in investigating
tube 2+ how the growing pollen tube is guided toward unfertil-
a
C
of ized ovules. In Arabidopsis, the pollen tube appears to be
n guided by a long-distance signal from the ovule (Hul-
o
cti skamp et al. 1995; Wilhelmi and Preuss 1999). Analysis of
e
Dir pollen tube growth in ovule mutants of Arabidopsisindi-
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)
å å
FIGURE 20.7 Calcium and pollen tube tip growth. After com-
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
Slocus 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 Slocus, specifically the SKRand 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 SKRand SCRgenes that encode self-recog-
nizing proteins from A. lyrata(a self-incompatible species).
This experiment demonstrates that A. thalianastill 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 SRCgenes 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 Sloci) rather than nonself. (After Nasrallah 2002;
photographs courtesy of J. Nasrallah.)
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AN OVERVIEW OF PLANT DEVELOPMENT 633
(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
Arabidopsispollen 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 Arabidopsisgene “popped” endosperm. The other accessory cells in the
POP2encodes an enzyme that degrades γ-amino butyric embryo sac degenerate after fertilization.
acid (GABA) and establishes a gradient of GABAin 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 GABAgradient. POP2is expressed in been found in the gymnosperm genera Ephedraand 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 pop2genotype. The wild-type enzyme ond zygote “sacrificed” as a food supply in an early gym-
in the pollen tube may degrade GABAand 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. Asingle 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 2nendosperm (Figure 20.10B). The
2nendosperm provides convincing evidence that the four-
The growing pollen tube enters the embryo sac through celled embryo sac in Nuphardoes 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.
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634 CHAPTER20
(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 2nendosperms. 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 2nendosperm. 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 embryogenesiscovers 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 patterningpro-
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 patterningestablishes 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). Afemale 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 Drosophilamaternal effect gene (Gross-
embryo until the embryo becomes autotrophic.
niklaus et al. 1998). Curiously, MEDEAis 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 MEDEAaffects 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.
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or disseminated in any form without the express written permission of the publisher.
Chapter 20 pagestest(cid:1).qxd 8/5/10 10:35 AM Page 635
AN OVERVIEW OF PLANT DEVELOPMENT 635
FIGURE 20.11 Axis formation in the
(A) (B)
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
D
ir shone in the direction of the arrow. The
e
c sperm-induced axis was overridden, and
tio an F-actin patch formed on the dark side,
n
o where the rhizoid will later form. (Pho-
f lig tographs courtesy of W. Hables.)
h
t
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
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Chapter 20 pagestest(cid:1).qxd 8/5/10 10:35 AM Page 636
636 CHAPTER20
Root Shoot Cotyledons
meristem meristem
Embryo
Terminal cell
2-Cell embryo
Suspensor
Suspensor
Zygote Basal cell 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
et al. 1994). In these mutants, abnormalities in the embryo
suspensor and the embryo is the hypophysis. While there are
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). Asignal 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 SUS1gene 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, DCL1has
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. DCL1alleles include sin1alleles. 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 DCL1causes 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 DrosophilaDicer 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 RNAprod-
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 Arabidopsishave provided genetic evidence that ble developmental signals are arising from the work being
the suspensor has the capacity to develop embryo-like done on DCL1alleles 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.
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or disseminated in any form without the express written permission of the publisher.
