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Signaling in plant embryogenesis
John J Harada
Embryogenesis is a critical stage of the sporophytic life cycle
during which the basic body plan of the plant is established.
Although positional information is implicated to play a major
role in determining embryo cell fate, little is known about the
nature of positional signals. Recent studies show that the
monopterous and hobbit mutations reveal signaling during
patterning of the embryonic axis. The LEAFY COTYLEDON1
and PICKLE genes have been implicated to play important
roles in controlling embryo development.
heart-stage of embryogenesis, localized cell divisions generate the cotyledons, embryonic storage organs. Fifth, by
the torpedo-stage, both the shoot and root apical meristems
are visible as organized structures (Figure 1g).
© Elsevier Science Ltd ISSN 1369-5266
Although progress has been made in establishing a framework for understanding the mechanisms involved in
embryo development, many questions remain. Little is
known about the molecular processes that induce embryo
formation. The morphogenetic events that underlie formation of the embryo also remain to be defined. Because cell
fate is largely determined by positional information in
plants, signaling and intercellular communication play critical roles in development [8,9]. In this article, I review
primarily information published during the past year that
provide examples of signaling during plant embryogenesis.
Due to space limitations, this review will not be comprehensive but will focus on specific examples.
Introduction
Induction of embryo development
Embryogenesis in higher plants begins with a double fertilization event in which two sperm nuclei fuse with the
egg cell and central cell nuclei, respectively, to initiate
embryo and endosperm development. The zygote then
undergoes a series of cell divisions and differentiation
events to produce the mature embryo [1–4]. As shown in
Figure 1, a mature dicot embryo consists of at least five
major organs/structures along its apical–basal axis, the
shoot apical meristem, the cotyledons, the hypocotyl, the
root, and the root apical meristem. Along its radial axis, the
embryo comprises three primary tissue systems: the outer
protoderm (epidermis); the middle ground meristem; and
the inner procambium (vascular tissue).
Although zygotic embryogenesis is induced by the
fusion of the sperm and egg nuclei, plant cells can initiate embryo development without fertilization. For
example, cultured somatic and male gametic cells can be
induced to undergo somatic and microspore embryogenesis, respectively [10]. Non-zygotic embryos can also
arise through apomixis, a suite of asexual reproductive
processes that occurs in the ovule [11]. The ability to initiate embryogenesis without sex shows that fertilization
is not required for embryo development. The recently
identified FIE (FERTILIZATION INDEPENDENT
ENDOSPERM) and FIS (FERTILIZATION INDEPENDENT SEED) genes have been implicated in the
suppression of endosperm development before central
cell and sperm nuclei fusion [12,13]. By analogy, it is possible that embryo development is similarly suppressed
until fertilization. The specific signals that initiate
embryogenesis have not been identified.
Addresses
Section of Plant Biology, Division of Biological Sciences, University of
California, One Shields Avenue, Davis, CA 95616, USA;
e-mail: [email protected]
Current Opinion in Plant Biology 1999, 2:23–27
http://biomednet.com/elecref/1369526600200023
A great deal is known at a descriptive level about how
embryos form. Figure 1 illustrates embryo development in
the representative dicot plant, Brassica napus, and shows
that the embryonic organ and tissue systems are formed
sequentially during embryogenesis [5–7]. First, the zygote
undergoes an asymmetric division, producing cells with different fates (Figures 1a and 1b). The apical cell goes on to
produce the embryo proper, and the basal cell generates the
hypophysis and the suspensor, a transient organ that plays
structural and physiological roles in embryo development.
Second, periclinal cell divisions within the eight-celled
octant stage embryo generate the first embryonic tissue, the
protoderm (Figure 1d). Later divisions within globular
embryos produce elongated cells in the center of the
embryo that define the procambium and the ground meristem (Figure 1f). Third, at the globular stage, division of the
uppermost cell of the suspensor defines a lens-shaped cell,
the hypophysis, that gives rise to part of the quiescent center and the initials of the central root cap (Figure 1e).
Fourth, during the transition from the globular-stage to the
Somatic embryos have been studied, in part, to define the
signals that initiate embryogenesis. Somatic cells cultured in
the presence of auxin are thought to acquire the competence
to undergo embryogenesis such that subsequent culturing in
the absence of auxin induces embryo formation [14]. Recent
studies show that the rate of Arabidopsis somatic embryo formation is increased compared with wild-type when primordia
timing, clavata1, and clavata3 mutant seedlings are cultured
[15]. Because these mutants have enlarged shoot apical
meristems, the authors propose that undifferentiated meristem cells may be more responsive to auxin signaling to
acquire embryogenic competence. The enhanced rate of
somatic embryo formation, therefore, may reflect the larger
number of meristem cells in the mutants. The critical question of what processes underlie embryogenic competence,
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Growth and development
Figure 1
(g)
(f)
(a)
(b)
(d)
(c)
ac
bc
o'
a
c
p
sam
p
(e)
b
cot
gm
h
h
pc
r
ram
Current Opinion in Plant Biology
Embryo development in a representative dicot plant. (a) Single-celled zygote of Brassica napus. (b) Two-celled embryo comprising the apical cell
(ac) that gives rise to most of the embryo proper and the basal cell (bc) that becomes part of the root apical meristem and the suspensor. (c) The
O’ line in this octant-stage embryo represents the first transverse division of the embryo proper and separates the apical (a) and central (c)
embryonic domains. The basal domain (b) is from the uppermost cell of the suspensor. (d) Periclinal divisions in the octant-stage embryo give rise
to the protoderm (p). (e) The hypophysis (h) derives from the uppermost cell of the suspensor in a globular-stage embryo. (f) In this transition-stage
embryo, the three major embryonic tissue systems are visible: protoderm (p), ground meristem (gm), and procambium (pc). (g) Five major
organs/structures along the apical–basal axis of this early torpedo-stage embryo are cotyledons (cot), shoot apical meristem (sam), hypocotyl (h),
root (r), and the root apical meristem (ram). Adapted from West and Harada [1].
however, remains unanswered. It is also not known if auxin
plays a role in initiating zygotic embryogenesis.
Recent work has provided insight into signaling that occurs
during the induction of somatic embryogenesis [16••].
Cultured carrot cells, destined to undergo somatic embryogenesis, are marked with a cell wall antigen recognized by
the antibody, JIM8. These competent cell divide asymmetrically, producing one daughter cell with the antigen and the
other without, and the epitope-free cells ultimately form
somatic embryos. Thus, embryogenic competence is associated with a cell wall antigen that segregates asymmetrically
during cell division. A surprising result is that the daughter
cell that does not label with JIM8 requires a soluble signal
from JIM8-positive cells, thought to be an arabinogalactan
protein, to continue its development into embryos. Thus,
signaling between cells of different fates is required for the
initiation of somatic embryogenesis, although it is not
known if a similar requirement obtains for zygotic embryos.
Two recent studies provide insight into the factors that
control embryo formation. First, the Arabidopsis LEAFY
COTYLEDON1 (LEC1) gene that encodes a subunit of the
CCAAT box binding transcription factor is a central regulator of both early and late embryogenesis [17••]. The
LEC1 gene is required for the maintenance of suspensor
cell fate, specification of cotyledon identity, initiation and
maintenance of the maturation phase, and suppression of
germination. Analyses of the Lec1– mutant phenotype
and of the gene’s expression pattern suggest that LEC1
functions exclusively during embryogenesis. Ectopic
expression of LEC1 during postembryonic growth is sufficient to induce embryo development in vegetative
tissues. Ectopic LEC1 gene expression inhibits postembryonic development of transgenic plants, causes
embryonic cotyledon-like organs to emerge at the position
of leaves, and activates embryo-specific genes.
Remarkably, as shown in Figure 2, embryo structures
occasionally form on the surfaces of leaves without culturing or pretreatments with auxin. These results suggest
that LEC1 plays a critical role in embryo development by
directly controlling processes during early and late
embryogenesis. LEC1 may accomplish these diverse functions by establishing an embryonic environment that
permits embryo formation to occur.
Mutations of the Arabidopsis PICKLE (PKL) gene reveal
that gibberellic acid signaling may also be important in controlling embryogenesis [18••]. Roots of pkl mutant seedlings
accumulate lipids normally found in seeds and express
embryo-specific genes. Moreover, culturing of excised pkl
roots on hormone-free media generates somatic embryos.
Thus, the pkl mutation either induces or fails to suppress
embryonic programs in seedling roots. Because the mutant
phenotype is suppressed by gibberellic acid, PKL is thought
to function in a gibberellic acid signaling pathway. The
implication is that gibberellic acid signaling may be required
to switch root cells from an embryonic to a vegetative fate.
Thus, genetic manipulations of LEC1 and PKL gene expression establish a cellular environment that permits embryo
formation to occur in the absence of hormone treatments.
Patterning of the embryonic axis
Analyses of seedling lethal mutants has led to the hypothesis that the early Arabidopsis embryo is divided into three
domains — apical, central and basal [19,20•]. As shown in
Figure 1, the apical region derives from the upper tier of an
octant stage embryo. Although cell fate is generally determined by position, the apical region usually contributes
the shoot apical meristem and most of the cotyledons. Part
Signaling in plant embryogenesis Harada
of the cotyledons, the hypocotyl, the root, and the root apical meristem initials arise from the central domain, a region
that comes from the lower tier of an octant stage embryo.
The basal region gives rise to the quiescent center of the
root apical meristem and the central root cap cells. Basal
region cells are descendants of the hypophysis, the uppermost cell of the suspensor. Additional support for the
existence of these domains comes from studies showing
that they correspond to transcriptional territories in globular stage embryos [21–23]. That is, specific genes, or their
promoters, are active in subdomains of either the apical,
central, or basal regions.
Recent analyses of genes required for embryonic axis formation suggest that signaling between embryonic domains
may be essential for root formation. Seedlings with mutations in the MONOPTEROUS (MP) gene do not possess
the hypocotyl, root, root apical meristem, and root cap, suggesting that the gene is required for specification of the
central and basal domains [24]. MP encodes a novel protein
with structural similarities to DNA binding proteins, opening the possibility that MP is a transcription factor [25•].
Although mp mutants lack embryonic roots, as seedlings
they can form adventitious roots. This result suggests a
specific role for MP in embryonic root formation. The pattern of MP gene expression and the phenotype of adult mp
mutant plants, however, indicate that MP plays a role in
establishing vascular tissue organization both in embryos
and postembryonic plants [26]. Specifically, the inability of
mp mutant embryos to form elongated cells parallel to the
axis in their central regions suggests that MP functions primarily in cell axialization required for the formation of
vascular cell files. An implication of these results is that
communication occurs between the central and basal
domains of early Arabidopsis embryos. That is, defects in
establishing the cellular organization of the central region
of mp mutant embryos may disrupt the signaling required
to specify the basal region. These results also suggest that
MP may not function specifically in the establishment of
embryonic domains. Rather, defects in specification of the
central and basal regions may occur as a result of the mutation’s primary defect in organizing provascular cells.
Both the central and basal domains of the early
Arabidopsis embryo contribute to root apical meristem
formation, and signaling between the two regions may be
critical. The HOBBIT (HBT) gene is required for correct
formation of the hypophyseal cell of the early Arabidopsis
embryo and, therefore, for root apical meristem formation
[27••]. Unlike wild-type plants, hbt mutants do not make
lateral roots, suggesting that the gene also functions
postembryonically. Because the hypophyseal cell is the
progenitor of the basal region, HBT may be required for
either specification of the basal domain or for specific
divisions of the hypophysis. Root apical meristem initials
do not form in hbt mutants, though these initials are largely derived from the central region of the early embryo.
These results provide an elegant second example of sig-
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Figure 2
LEC1 induces embryo structures from vegetative tissues. Ectopic
embryo structures formed on the surface of a leaf-like organ of a plant
transformed with the 35S/LEC1 gene. a, axis; c, cotyledons.
naling between the central and basal domains in root formation [20•]. In addition to the hypothesis that
communication from the central region is required for
basal region specification, signaling from the hypophysis,
or its derivatives, to the central region may also be
required for the formation of root apical meristem initials.
What are the signals required for apical–basal patterning?
Many studies of plant development, such as those cited
above, indicate that positional information plays the major
role in determining cell fate [8,9]. In nearly all cases, however, an understanding of what constitutes positional
information is lacking. Studies of embryogenesis in the
brown alga, Fucus, implicate at least two types of positional
signals. Similar to many higher plants, Fucus zygotes divide
initially into cells of different fates, the apical thallus cell
and the basal rhizoid. Laser ablation studies of two-celled
embryos show that intimate contact of thallus and rhizoid
cells with their walls is required to maintain cell identity
[28]. Thus, in Fucus, the cell wall is one positional determinant of cell fate. Other ablation studies also suggest that
direct cell-to-cell contact and symplastic communication do
not play major roles in cell fate determination at later stages
of Fucus embryogenesis [29•]. Rather, apoplastic diffusible
gradients are implicated as a primary determinant.
Although in neither case was the signaling molecule identified, these results provide clues about the positional signals
that may operate in higher plants.
Auxin has been implicated as at least one signal involved
in apical–basal patterning in higher plants. For example,
inhibitors of auxin polar transport have been shown to
block embryos at the transition from globular-stage to
heart-stage [30] and to prevent cotyledon separation in
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Growth and development
developing embryos [31]. Similar phenotypes have been
observed with Arabidopsis and tobacco mutants defective
in auxin polar transport [32–34]. Two recent studies in
wheat and Brassica juncea suggest that auxin may be
involved in shoot and root apical meristem formation
[35,36]. The mechanisms by which auxin acts during
embryogenesis, however, remain to be determined.
Specification of organ identity
Signaling within the shoot apex appears to be important in
the specification of organ identity. Mutations of Arabidopsis
EXTRA COTYLEDON1 (XTC1), XTC2, and ALTERED
MERISTEM PROGRAMMING1 (AMP1) genes cause the
transformation of the first seedling leaves into ‘extra cotyledons’ [37•]. These ‘extra cotyledons’ have characteristics of
embryonic cotyledons, such as reduced trichome numbers
and the presence of lipid and protein bodies. The effects of
these mutations are similar to those observed when immature Brassica napus embryos are germinated prematurely
[38]. In precociously germinated Brassica napus embryos,
leaf primordia that would normally develop into leaves are
converted into cotyledon-like organs that lack trichomes and
express embryo-specific genes [39]. The extra cotyledon
phenotypes of the Arabidopsis xtc and amp mutants and the
cultured Brassica napus embryos are attributed to their precocious activation of their shoot apical meristems during
embryogenesis. Premature development of leaf primordia in
an embryonic environment is thought to be sufficient to
alter the identity of these organs, suggesting that these primordia respond to embryonic signals. The converse
situation is observed with lec1 mutants whose cotyledons
have trichomes, normally a leaf trait. In lec1 mutant embryos,
premature activation of the postgermination program is
thought to interfere with the specification of cotyledon
identity [40]. These results emphasize that an embryonic
environment has profound effects on plant development.
Conclusions
In recent years, progress has been made in unraveling some
of the complexities of embryogenesis in higher plants. I
have discussed primarily two areas that provide examples of
signaling during embryogenesis. One conclusion to be
drawn from recent work is that specific genes appear able to
create a cellular environment that enhances embryo formation. The effects of the pkl mutation and the ectopic
expression of LEC1 are similar in that both induce embryonic characteristics in the organs of postembryonic plants.
Although the specific mechanisms by which these genetic
alterations enhance embryo formation is not known, it is
possible that the creation of an embryonic environment may
be critical. How the induction of embryo formation by LEC1
and PKL relates to somatic and zygotic embryogenesis
remains to be determined. It is interesting to note, however,
that somatic embryo formation is much more efficient when
immature zygotic embryos are used as a starting material
rather than seedlings [15]. A second conclusion is that signaling between different embryonic domains may be
required for precise patterning of the embryo’s apical–basal
axis. These studies provide elegant examples of signaling in
plant embryogenesis, although more work is needed to
define, at a mechanistic level, the nature of the signals that
constitute positional information.
Acknowledgements
I thank Marilyn West and Tami Lotan for help in preparing Figures 1 and 2,
and Neelima Sinha and Tami Lotan for their comments about the
manuscript. Work from my lab was supported by a grant from DOE.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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••
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The cloning of LEAFY COTYLEDON1, a major regulator of Arabidopsis
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postembryonically is described. LEC1 is a homolog of a subunit of the CCAAT
box binding transcription factor. Results show that ectopically expressed LEC1
induces embryonic programs and embryo formation in vegetative tissues.
Signaling in plant embryogenesis Harada
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A novel mutation, pickle, that induces embryonic characteristics in the roots of
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•
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•
encodes a transcription factor mediating embryo axis formation
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••
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27
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•
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