pb2107.

qxd 12/06/1999 2:34 PM Page 23

23

Signaling in plant embryogenesis

John J Harada
Embryogenesis is a critical stage of the sporophytic life cycle heart-stage of embryogenesis, localized cell divisions gen-
during which the basic body plan of the plant is established. erate the cotyledons, embryonic storage organs. Fifth, by
Although positional information is implicated to play a major the torpedo-stage, both the shoot and root apical meristems
role in determining embryo cell fate, little is known about the are visible as organized structures (Figure 1g).
nature of positional signals. Recent studies show that the
monopterous and hobbit mutations reveal signaling during Although progress has been made in establishing a frame-
patterning of the embryonic axis. The LEAFY COTYLEDON1 work for understanding the mechanisms involved in
and PICKLE genes have been implicated to play important embryo development, many questions remain. Little is
roles in controlling embryo development. known about the molecular processes that induce embryo
formation. The morphogenetic events that underlie forma-
Addresses tion of the embryo also remain to be defined. Because cell
Section of Plant Biology, Division of Biological Sciences, University of fate is largely determined by positional information in
California, One Shields Avenue, Davis, CA 95616, USA; plants, signaling and intercellular communication play crit-
e-mail: [email protected]
ical roles in development [8,9]. In this article, I review
Current Opinion in Plant Biology 1999, 2:23–27 primarily information published during the past year that
provide examples of signaling during plant embryogenesis.
http://biomednet.com/elecref/1369526600200023
Due to space limitations, this review will not be compre-
© Elsevier Science Ltd ISSN 1369-5266 hensive but will focus on specific examples.

Introduction Induction of embryo development

Embryogenesis in higher plants begins with a double fer- Although zygotic embryogenesis is induced by the
tilization event in which two sperm nuclei fuse with the fusion of the sperm and egg nuclei, plant cells can initi-
egg cell and central cell nuclei, respectively, to initiate ate embryo development without fertilization. For
embryo and endosperm development. The zygote then example, cultured somatic and male gametic cells can be
undergoes a series of cell divisions and differentiation induced to undergo somatic and microspore embryogen-
events to produce the mature embryo [1–4]. As shown in esis, respectively [10]. Non-zygotic embryos can also
Figure 1, a mature dicot embryo consists of at least five arise through apomixis, a suite of asexual reproductive
major organs/structures along its apical–basal axis, the processes that occurs in the ovule [11]. The ability to ini-
shoot apical meristem, the cotyledons, the hypocotyl, the tiate embryogenesis without sex shows that fertilization
root, and the root apical meristem. Along its radial axis, the is not required for embryo development. The recently
embryo comprises three primary tissue systems: the outer identified FIE (FERTILIZATION INDEPENDENT
protoderm (epidermis); the middle ground meristem; and ENDOSPERM) and FIS (FERTILIZATION INDEPEN-
the inner procambium (vascular tissue). DENT SEED) genes have been implicated in the
suppression of endosperm development before central
A great deal is known at a descriptive level about how cell and sperm nuclei fusion [12,13]. By analogy, it is pos-
embryos form. Figure 1 illustrates embryo development in sible that embryo development is similarly suppressed
the representative dicot plant, Brassica napus, and shows until fertilization. The specific signals that initiate
that the embryonic organ and tissue systems are formed embryogenesis have not been identified.
sequentially during embryogenesis [5–7]. First, the zygote
undergoes an asymmetric division, producing cells with dif- Somatic embryos have been studied, in part, to define the
ferent fates (Figures 1a and 1b). The apical cell goes on to signals that initiate embryogenesis. Somatic cells cultured in
produce the embryo proper, and the basal cell generates the the presence of auxin are thought to acquire the competence
hypophysis and the suspensor, a transient organ that plays to undergo embryogenesis such that subsequent culturing in
structural and physiological roles in embryo development. the absence of auxin induces embryo formation [14]. Recent
Second, periclinal cell divisions within the eight-celled studies show that the rate of Arabidopsis somatic embryo for-
octant stage embryo generate the first embryonic tissue, the mation is increased compared with wild-type when primordia
protoderm (Figure 1d). Later divisions within globular timing, clavata1, and clavata3 mutant seedlings are cultured
embryos produce elongated cells in the center of the [15]. Because these mutants have enlarged shoot apical
embryo that define the procambium and the ground meris- meristems, the authors propose that undifferentiated meris-
tem (Figure 1f). Third, at the globular stage, division of the tem cells may be more responsive to auxin signaling to
uppermost cell of the suspensor defines a lens-shaped cell, acquire embryogenic competence. The enhanced rate of
the hypophysis, that gives rise to part of the quiescent cen- somatic embryo formation, therefore, may reflect the larger
ter and the initials of the central root cap (Figure 1e). number of meristem cells in the mutants. The critical ques-
Fourth, during the transition from the globular-stage to the tion of what processes underlie embryogenic competence,
pb2107.qxd 12/06/1999 2:34 PM Page 24

24 Growth and development

Figure 1

(g) cot

(f) sam
(a) (b) (c) (d) (e) p
ac a p

o' c gm
bc b 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 embryonic cotyledon-like organs to emerge at the position
plays a role in initiating zygotic embryogenesis. of leaves, and activates embryo-specific genes.
Remarkably, as shown in Figure 2, embryo structures
Recent work has provided insight into signaling that occurs occasionally form on the surfaces of leaves without cultur-
during the induction of somatic embryogenesis [16••]. ing or pretreatments with auxin. These results suggest
Cultured carrot cells, destined to undergo somatic embryo- that LEC1 plays a critical role in embryo development by
genesis, are marked with a cell wall antigen recognized by directly controlling processes during early and late
the antibody, JIM8. These competent cell divide asymmet- embryogenesis. LEC1 may accomplish these diverse func-
rically, producing one daughter cell with the antigen and the tions by establishing an embryonic environment that
other without, and the epitope-free cells ultimately form permits embryo formation to occur.
somatic embryos. Thus, embryogenic competence is associ-
ated with a cell wall antigen that segregates asymmetrically Mutations of the Arabidopsis PICKLE (PKL) gene reveal
during cell division. A surprising result is that the daughter that gibberellic acid signaling may also be important in con-
cell that does not label with JIM8 requires a soluble signal trolling embryogenesis [18••]. Roots of pkl mutant seedlings
from JIM8-positive cells, thought to be an arabinogalactan accumulate lipids normally found in seeds and express
protein, to continue its development into embryos. Thus, embryo-specific genes. Moreover, culturing of excised pkl
signaling between cells of different fates is required for the roots on hormone-free media generates somatic embryos.
initiation of somatic embryogenesis, although it is not Thus, the pkl mutation either induces or fails to suppress
known if a similar requirement obtains for zygotic embryos. embryonic programs in seedling roots. Because the mutant
phenotype is suppressed by gibberellic acid, PKL is thought
Two recent studies provide insight into the factors that to function in a gibberellic acid signaling pathway. The
control embryo formation. First, the Arabidopsis LEAFY implication is that gibberellic acid signaling may be required
COTYLEDON1 (LEC1) gene that encodes a subunit of the to switch root cells from an embryonic to a vegetative fate.
CCAAT box binding transcription factor is a central regu- Thus, genetic manipulations of LEC1 and PKL gene expres-
lator of both early and late embryogenesis [17••]. The sion establish a cellular environment that permits embryo
LEC1 gene is required for the maintenance of suspensor formation to occur in the absence of hormone treatments.
cell fate, specification of cotyledon identity, initiation and
maintenance of the maturation phase, and suppression of Patterning of the embryonic axis
germination. Analyses of the Lec1– mutant phenotype Analyses of seedling lethal mutants has led to the hypoth-
and of the gene’s expression pattern suggest that LEC1 esis that the early Arabidopsis embryo is divided into three
functions exclusively during embryogenesis. Ectopic domains — apical, central and basal [19,20•]. As shown in
expression of LEC1 during postembryonic growth is suffi- Figure 1, the apical region derives from the upper tier of an
cient to induce embryo development in vegetative octant stage embryo. Although cell fate is generally deter-
tissues. Ectopic LEC1 gene expression inhibits postem- mined by position, the apical region usually contributes
bryonic development of transgenic plants, causes the shoot apical meristem and most of the cotyledons. Part
pb2107.qxd 12/06/1999 2:34 PM Page 25

Signaling in plant embryogenesis Harada 25

of the cotyledons, the hypocotyl, the root, and the root api- Figure 2
cal 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 upper-
most cell of the suspensor. Additional support for the
existence of these domains comes from studies showing
that they correspond to transcriptional territories in globu-
lar 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 for-

mation suggest that signaling between embryonic domains
may be essential for root formation. Seedlings with muta-
tions in the MONOPTEROUS (MP) gene do not possess
the hypocotyl, root, root apical meristem, and root cap, sug-
gesting that the gene is required for specification of the
central and basal domains [24]. MP encodes a novel protein LEC1 induces embryo structures from vegetative tissues. Ectopic
with structural similarities to DNA binding proteins, open- embryo structures formed on the surface of a leaf-like organ of a plant
ing the possibility that MP is a transcription factor [25•]. transformed with the 35S/LEC1 gene. a, axis; c, cotyledons.
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 pat- naling between the central and basal domains in root for-
tern of MP gene expression and the phenotype of adult mp mation [20•]. In addition to the hypothesis that
mutant plants, however, indicate that MP plays a role in communication from the central region is required for
establishing vascular tissue organization both in embryos basal region specification, signaling from the hypophysis,
and postembryonic plants [26]. Specifically, the inability of or its derivatives, to the central region may also be
mp mutant embryos to form elongated cells parallel to the required for the formation of root apical meristem initials.
axis in their central regions suggests that MP functions pri-
marily in cell axialization required for the formation of What are the signals required for apical–basal patterning?
vascular cell files. An implication of these results is that Many studies of plant development, such as those cited
communication occurs between the central and basal above, indicate that positional information plays the major
domains of early Arabidopsis embryos. That is, defects in role in determining cell fate [8,9]. In nearly all cases, how-
establishing the cellular organization of the central region ever, an understanding of what constitutes positional
of mp mutant embryos may disrupt the signaling required information is lacking. Studies of embryogenesis in the
to specify the basal region. These results also suggest that brown alga, Fucus, implicate at least two types of positional
MP may not function specifically in the establishment of signals. Similar to many higher plants, Fucus zygotes divide
embryonic domains. Rather, defects in specification of the initially into cells of different fates, the apical thallus cell
central and basal regions may occur as a result of the muta- and the basal rhizoid. Laser ablation studies of two-celled
tion’s primary defect in organizing provascular cells. embryos show that intimate contact of thallus and rhizoid
cells with their walls is required to maintain cell identity
Both the central and basal domains of the early [28]. Thus, in Fucus, the cell wall is one positional determi-
Arabidopsis embryo contribute to root apical meristem nant of cell fate. Other ablation studies also suggest that
formation, and signaling between the two regions may be direct cell-to-cell contact and symplastic communication do
critical. The HOBBIT (HBT) gene is required for correct not play major roles in cell fate determination at later stages
formation of the hypophyseal cell of the early Arabidopsis of Fucus embryogenesis [29•]. Rather, apoplastic diffusible
embryo and, therefore, for root apical meristem formation gradients are implicated as a primary determinant.
[27••]. Unlike wild-type plants, hbt mutants do not make Although in neither case was the signaling molecule identi-
lateral roots, suggesting that the gene also functions fied, these results provide clues about the positional signals
postembryonically. Because the hypophyseal cell is the that may operate in higher plants.
progenitor of the basal region, HBT may be required for
either specification of the basal domain or for specific Auxin has been implicated as at least one signal involved
divisions of the hypophysis. Root apical meristem initials in apical–basal patterning in higher plants. For example,
do not form in hbt mutants, though these initials are large- inhibitors of auxin polar transport have been shown to
ly derived from the central region of the early embryo. block embryos at the transition from globular-stage to
These results provide an elegant second example of sig- heart-stage [30] and to prevent cotyledon separation in
pb2107.qxd 12/06/1999 2:34 PM Page 26

26 Growth and development

developing embryos [31]. Similar phenotypes have been axis. These studies provide elegant examples of signaling in
observed with Arabidopsis and tobacco mutants defective plant embryogenesis, although more work is needed to
in auxin polar transport [32–34]. Two recent studies in define, at a mechanistic level, the nature of the signals that
wheat and Brassica juncea suggest that auxin may be constitute positional information.
involved in shoot and root apical meristem formation
[35,36]. The mechanisms by which auxin acts during
Acknowledgements
embryogenesis, however, remain to be determined. 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.
Specification of organ identity
Signaling within the shoot apex appears to be important in References and recommended reading
the specification of organ identity. Mutations of Arabidopsis Papers of particular interest, published within the annual period of review,
have been highlighted as:
EXTRA COTYLEDON1 (XTC1), XTC2, and ALTERED
MERISTEM PROGRAMMING1 (AMP1) genes cause the • of special interest
•• of outstanding interest
transformation of the first seedling leaves into ‘extra cotyle-
1. West MA, Harada JJ: Embryogenesis in higher plants: an overview.
dons’ [37•]. These ‘extra cotyledons’ have characteristics of Plant Cell 1993, 5:1361-1369.
embryonic cotyledons, such as reduced trichome numbers 2. Yadegari R, Goldberg RB: Embryogenesis in dicotyledonous plants.
and the presence of lipid and protein bodies. The effects of In Cellular and Molecular Biology of Plant Seed Development. Edited by
these mutations are similar to those observed when imma- Larkins BA, Vasil IK. Dordrecht: Kluwer Academic Publishers; 1997:3-52.
ture Brassica napus embryos are germinated prematurely 3. Laux T, Jürgens G: Embryogenesis: a new start in life. Plant Cell
1997, 9:989-1000.
[38]. In precociously germinated Brassica napus embryos,
leaf primordia that would normally develop into leaves are 4. Berleth T: Experimental approaches to Arabidopsis embryogenesis.
Plant Physiol Biochem 1998, 36:69-82.
converted into cotyledon-like organs that lack trichomes and
5. Tykarska T: Rape embryogenesis. I. The proembryo development.
express embryo-specific genes [39]. The extra cotyledon Acta Soc Bot Poloniae 1976, 45:3-16.
phenotypes of the Arabidopsis xtc and amp mutants and the
6. Tykarska T: Rape embryogenesis. II. Development of embryo
cultured Brassica napus embryos are attributed to their pre- proper. Acta Soc Bot Poloniae 1979, 48:391-421.
cocious activation of their shoot apical meristems during 7. Mansfield SG, Briarty LG: Early embryogenesis in Arabidopsis
embryogenesis. Premature development of leaf primordia in thaliana. II. The developing embryo. Can J Bot 1991, 69:461-476.
an embryonic environment is thought to be sufficient to 8. Dawe RK, Freeling M: Cell lineage and its consequences in higher
alter the identity of these organs, suggesting that these pri- plants. Plant J 1991, 1:3-8.
mordia respond to embryonic signals. The converse 9. Szymkoviak EJ, Sussex IM: What chimeras can tell us about plant
situation is observed with lec1 mutants whose cotyledons development. Annu Rev Plant Physiol Plant Molec Biol 1996,
47:351-376.
have trichomes, normally a leaf trait. In lec1 mutant embryos,
10. Zimmerman JL: Somatic embryogenesis: a model for early
premature activation of the postgermination program is development in higher plants. Plant Cell 1993, 5:1411-1423.
thought to interfere with the specification of cotyledon
11. Koltunow AM: Apomixis: embryo sacs and embryos formed without
identity [40]. These results emphasize that an embryonic meiosis or fertilization in ovules. Plant Cell 1993, 5:1425-1437.
environment has profound effects on plant development. 12. Ohad N, Margossian L, Hsu Y-C, Williams C, Repetti P, Fischer RL:
A mutation that allows endosperm development without
Conclusions fertilization. Proc Natl Acad Sci USA 1996, 93:5319-5324.
In recent years, progress has been made in unraveling some 13. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ:
Fertilization-independent seed development in Arabidopsis
of the complexities of embryogenesis in higher plants. I thaliana. Proc Natl Acad Sci USA 1997, 94:4223-4228.
have discussed primarily two areas that provide examples of
14. Dodeman VL, Ducreux G, Kreis M: Zygotic embryogenesis versus
signaling during embryogenesis. One conclusion to be somatic embryogenesis. J Exp Bot 1997, 48:1493-1509.
drawn from recent work is that specific genes appear able to 15. Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, van Went J,
create a cellular environment that enhances embryo forma- Koornneef M, de Vries SC: Somatic embryogenesis in Arabidopsis
tion. The effects of the pkl mutation and the ectopic thaliana is facilitated by mutations in genes repressing
meristematic cell divisions. Genetics 1998, 149:549-563.
expression of LEC1 are similar in that both induce embry-
16. McCabe PF, Valentine TA, Forsberg LS, Pennell RI: Soluble signals
onic characteristics in the organs of postembryonic plants. •• from cells identified at the cell wall establish a developmental
Although the specific mechanisms by which these genetic pathway in carrot. Plant Cell 1997, 9:2225-2241.
This paper provides information about signaling during the induction of
alterations enhance embryo formation is not known, it is somatic embryogenesis. The authors show that cells competent to become
possible that the creation of an embryonic environment may embryogenic require soluble signals from other cells to form somatic
embryos. They also show that a cell wall antigen on cells destined to form
be critical. How the induction of embryo formation by LEC1 embryos segregates asymmetrically during a formative division.
and PKL relates to somatic and zygotic embryogenesis
17. Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K,
remains to be determined. It is interesting to note, however, •• Fischer RL, Goldberg RB, Harada JJ: Arabidopsis LEAFY
that somatic embryo formation is much more efficient when COTYLEDON1 is sufficient to induce embryo development in
vegetative cells. Cell 1998, 93:1195-1205.
immature zygotic embryos are used as a starting material The cloning of LEAFY COTYLEDON1, a major regulator of Arabidopsis
rather than seedlings [15]. A second conclusion is that sig- embryogenesis, and the consequences of ectopically expressing the gene
postembryonically is described. LEC1 is a homolog of a subunit of the CCAAT
naling between different embryonic domains may be box binding transcription factor. Results show that ectopically expressed LEC1
required for precise patterning of the embryo’s apical–basal induces embryonic programs and embryo formation in vegetative tissues.
pb2107.qxd 12/06/1999 2:34 PM Page 27

Signaling in plant embryogenesis Harada 27

18. Ogas J, Cheng J-C, Sung ZR, Somerville C: Cellular differentiation 29. Bouget F-Y, Berger F, Brownlee C: Position dependent control of
•• regulated by gibberellin in the Arabidopsis thaliana pickle mutant. • cell fate in the Fucus embryo: role of intercellular communication.
Science 1997, 277:91-94. Development 1998, 125:1999-2008.
A novel mutation, pickle, that induces embryonic characteristics in the roots of Ablation studies in the brown alga Fucus suggest that cell walls and gradi-
Arabidopsis seedlings is described. Somatic embryo formation is induced when ents of diffusible apoplastic signals are involved in pattern formation during
mutant pkl roots are cultured. The ability of gibberellic acid to suppress the embryo development.
mutation suggests that PKL functions in a gibberellic acid signaling pathway
that controls the transition of root cells from an embryonic to a vegetative fate. 30. Schiavone FM, Cooke TJ: Unusual patterns of somatic
embryogenesis in the domesticated carrot: develpmental effects
19. Mayer U, Torres Ruiz RAT, Berleth T, Misera S, Jürgens G: Mutations
affecting body organization in the Arabidopsis embryo. Nature of exogenous auxins and auxin transport inhibitors. Cell Diff 1987,
1991, 353:402-407. 21:53-62.

20. Mayer U, Jürgens G: Pattern formation in plant embryogenesis: a 31. Liu CM, Xu Z-H, Chua N-H: Auxin polar transport is essentital for
• reassessment. Sem Cell Dev Biol 1998, 9:187-193. the establishment of bilateral symmetry during early plant
A useful review that presents the authors’ current hypotheses about the pat- embryogenesis. Plant Cell 1993, 5:621-630.
terning of the embryonic axis.
32. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y: Requirement of
21. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, the auxin polar transport system in early stages of Arabidopsis
Gerentes D, Perez P, Smyth DR: AINTEGUMENTA, an APETEALA2- floral bud formation. Plant Cell 1991, 3:667-684.
like gene of Arabidopsis with pleiotropic roles in ovule
development and floral organ growth. Plant Cell 1996, 8:155-168. 33. Bennet SRM, Alvarez J, Bossinger G, Smyth DR: Morphogenesis of
the pinoid mutant of Arabidopsis. Plant J 1995, 8:505-520.
22. Goldberg RB, de Paiva G, Yadegari R: Plant embryogenesis: zygote
to seed. Science 1994, 266:605-614. 34. Naderi M, Caplan A, Berger PH: Phenotypic characterization of
tobacco mutant impaired in auxin polar transport. Plant Cell Rep
23. Long JA, Moan EI, Medford JI, Barton MK: A member of the
1997, 17:32-38.
KNOTTED class of homeodomain proteins encoded by the STM
gene of Arabidopsis. Nature 1996, 379:66-69. 35. Hadfi K, Speth V, Neuhaus G: Auxin-induced developmental
24. Berleth T, Jürgens G: The role of the MONOPTEROUS gene in patterns in Brassica juncea embryos. Development 1998,
organising the basal body region of the Arabidopsis embryo. 125:879-887.
Development 1993, 118:575-587.
36. Fischer C, Speth V, Fleig-Eberenz S, Neuhaus G: Induction of
25. Hardtke CS, Berleth T: The Arabidopsis gene MONOPTEROS zygotic polyembryos in wheat: influence of auxin polar transport.
• encodes a transcription factor mediating embryo axis formation Plant Cell 1997, 9:1767-1780.
and vascular development. EMBO J 1998, 17:1405-1411.
This paper describes the cloning of the Arabidopsis MONOPTEROUS 37. Conway LJ, Poethig RS: Mutations of Arabidopsis thaliana that
gene, a gene required for specification of the embryonic central and basal • transform leaves into cotyledons. Proc Natl Acad Sci USA 1997,
domains. The corresponding protein possesses motifs characteristic of DNA 94:10209-10214.
binding proteins. Analyses of MP RNA accumulation provide support for the Three mutations, extra cotyledon1 and 2 and altered meristem programing1,
conclusions that MP functions in the early organization of vascular tissue in are shown to cause the first leaves of Arabidopsis seedlings to be trans-
embryonic and postembryonic plants. formed into cotyledon-like organs. The authors suggest that these changes
in organ identity result from the precocious activation of the shoot apical
26. Przemeck GKH, Mattsson J, Hardtke CS, Sung ZR, Berleth T: Studies
on the role of the Arabidopsis gene MONOPTEROS in vascular meristems of these mutants during embryogenesis.
development and plant cell axialization. Planta 1996, 200:229-237. 38. Finkelstein RR, Crouch ML: Precociously germinating rapeseed
27. Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B: The embryos retain characteristics of embryogeny. Planta 1984,
•• HOBBIT gene is required for formation of the root meristem in the 162:125-131.
Arabidopsis embryo. Development 1998, 125:521-531.
This paper presents a detailed analysis of the effects of the hobbit mutation 39. Fernandez DE: Developmental basis of homeosis in precociously
on root development. HBT is required for root apical meristem formation in germinating Brassica napus embryos: phase change at the shoot
embryos and postembryonic plants. Results suggest that HBT functions in apex. Development 1997, 124:1149-1157.
the formation of the hypophyseal cell in early embryos and, therefore, in the
40. West MAL, Matsudaira Yee KL, Danao J, Zimmerman JL, Fischer RL,
specification of the basal domain.
Goldberg RB, Harada JJ: LEAFY COTYLEDON1 is an essential
28. Berger F, Taylor A, Brownlee C: Cell fate determination by the cell regulator of late embryogenesis and cotyledon identity in
wall in early Fucus development. Science 1994, 263:1421-1423. Arabidopsis. Plant Cell 1994, 6:1731-1745.