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Higher
plant embryogenesis is divided conceptually into two distinct phases:
early morphogenetic processes that give rise to embryonic cell types,
tissues, and organ systems, and late maturation events that allow the
fully developed embryo to enter a desiccated and metabolically quiescent
state ([52] and [13]).
Upon reception of the appropriate signals, the dormant embryo
germinates, and seedling development begins. Thus, seed maturation and
metabolic quiescence interrupt the morphogenetic processes that occur
during embryogenesis and seedling development. This unique form of
development underlies, in part, a plant's ability to make seeds, a trait
that has conferred significant selective advantages to higher plants (Steeves 1983).
Because lower plants do not make seeds and do not undergo embryo
maturation, this bipartite mode of embryogenesis is thought to have
resulted from the insertion of maturation events into the higher plant
life cycle (reviewed by
[51],
[47] and [16]).
Little is known at the mechanistic level about how distinct processes
that occur during the morphogenesis and seed maturation phases are
coordinated.Genetic strategies employed to identify regulators of Arabidopsis thaliana embryo development have distinguished several gene classes that affect embryogenesis. One class of mutations, including raspberry, tinman, and abnormal suspensor ([41],
[56],
[7] and [49];
T. L. et al, unpublished data), causes the arrest of embryo
morphogenesis. Many of the corresponding proteins are involved in basic
cellular functions and probably do not perform direct regulatory roles. A
second class of genes predicted to play a role in embryonic pattern
formation has been identified (Mayer et al. 1991). The expression patterns of two such genes, EMB30 (GNOM) and KNOLLE, suggest that they do not function specifically during embryogenesis ([42] and [23]). Another class, including SHOOTMERISTEMLESS and SCARECROW, is active in the developing shoot or root apical meristems ([9] and [22]).
Although these genes play key roles in meristem function, they are
required for meristem formation during both embryogenesis and
postembryonic development. ABSCISIC ACID INSENSITIVE3 (ABI3), a fourth gene class, encodes an embryo-specific transcription factor that regulates genes expressed during seed maturation ([20] and [38]).
However, its function is limited to the late stages of embryogenesis.
Although each of these gene classes is essential for embryo development,
none appears to act specifically during embryogenesis to control both
the morphogenesis and maturation phases.The LEAFY COTYLEDON1 (LEC1) gene, by contrast, controls many distinct aspects of embryogenesis (Meinke 1992Meinke, 1992, 1994;
[53] and [39]). As summarized in Figure 1, the lec1 mutation is pleiotropic, indicating several roles in late embryo development. LEC1 is required for specific aspects of seed maturation. lec1
mutant embryos are intolerant of desiccation and show defects in the
expression of some, but not all, maturation-specific genes ([28],
[53] and [39]). LEC1 is also involved in inhibiting premature germination. lec1
mutant embryos exhibit morphological and molecular characteristics of
both embryogenesis and postgerminative seedling development, showing
that aspects of both programs can occur simultaneously (Meinke 1992Meinke, 1992, 1994; West et al. 1994). LEC1 plays a role in the specification of embryonic organ identity as well. Embryonic leaves or cotyledons of lec1 mutants possess trichomes, epidermal hairs, which normally form only on leaves and stems in Arabidopsis ([28] and [53]). The anatomy of lec1 mutant cotyledons is intermediate between those of a wild-type cotyledon and a leaf (West et al. 1994). Finally, LEC1 appears to act only during embryo development. Desiccation-intolerant lec1
embryos can be rescued from plants before desiccation and germinated to
produce homozygous mutant plants that are fertile and that do not
display any obvious vegetative or floral mutant phenotypes ([28] and [53]). Two other LEC class genes, LEC2 and FUSCA3 (FUS3), are thought to share similar or overlapping functions with LEC1, including the specification or cotyledon identity and the maintenance of maturation ([2],
[18] and [29]). Although nothing has been reported about how LEC
class genes act at the molecular level, their involvement in many
diverse aspects of embryogenesis suggests that these genes serve as
regulators of higher plant embryonic processes.Figure 1. Pleiotropic Effects of the lec1 Mutation on Embryo DevelopmentMajor differences between wild-type and lec1
mutant embryos are as follows. Embryo shape: the axes of mutant embryos
are short, and their cotyledons are round and do not curl. Anthocyanin
generally accumulates at the tips of mutant cotyledons. Precocious
germination: the shoot apical meristems of lec1 embryos are
activated in that they are domed and possess leaf primordia, unlike
their wild-type counterparts that are flat and do not contain leaf
primordia. Defects in seed maturation: lec1 mutant embryos are intolerant of desiccation and normally die if dried on the plant. However, lec1
embryos isolated before desiccation can be germinated to produce
fertile homozygous mutant plants. The promoter of a 7S storage protein
gene that is normally active during wild-type embryogenesis is not
active in the lec1 mutant. Incomplete specification of cotyledon identity: lec1 seedlings possess trichomes on cotyledons. Trichomes are present on Arabidopsis leaves and stems but not on wild-type cotyledons. a, axis; c, cotyledon; SAM, shoot apical meristem.View thumbnail imagesView high quality image (116K)In this paper, we report the isolation of the LEC1 gene and show that it encodes a homolog of a conserved eukaryotic transcription factor. Expression studies showed that the LEC1 gene is active only within seeds during both early and late seed development. Ectopic expression of the LEC1
gene induces embryonic programs and embryo development in vegetative
cells. We suggest that LEC1 is an important transcriptional regulator
required for both early and late embryogenesis that controls and
coordinates higher plant embryo development.
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