LEAFY COTYLEDON1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis

West, Marilyn A. L.; Yee, Kelly Matsudaira; Danao, Jay; Zimmerman, J. Lynn; Fischer, Robert L.; Goldberg, Robert B.; Harada, John J.

doi:10.2307/3869904

Cited by 150 publications

(157 citation statements)

References 31 publications

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“…LEC1, which encodes subunit B9 of a nuclear factor Y protein (NF‐YB9), and the B3 domain protein LEC2 are part of a larger network of “LAFL” proteins (for L EC1/LEC1‐LIKE [L1L], A BSCISIC ACID [ABA] INSENSITIVE 3 [ABI3], F USCA3 [FUS3] and L EC2) that regulate embryo identity and maturation (Jia, McCarty, & Suzuki, 2013). Loss‐of‐function mutations in LAFL genes result in defects in cotyledon development, storage macromolecule accumulation, and desiccation tolerance in zygotic embryos (Keith, Kraml, Dengler, & McCourt, 1994; Meinke, Franzmann, Nickle, & Yeung, 1994; Parcy, Valon, Kohara, Misera, & Giraudat, 1997; Stone et al., 2001; West et al., 1994). In contrast, ectopic expression of LEC1 and LEC2 induces somatic embryo formation on the cotyledons and leaves of arabidopsis seedlings (Lotan et al., 1998; Stone et al., 2001).…”

Section: A Network Of Arabidopsis Transcription Factors Controls Somamentioning

confidence: 99%

A transcriptional view on somatic embryogenesis

2017

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Somatic embryogenesis is a form of induced plant cell totipotency where embryos develop from somatic or vegetative cells in the absence of fertilization. Somatic embryogenesis can be induced in vitro by exposing explants to stress or growth regulator treatments. Molecular genetics studies have also shown that ectopic expression of specific embryo‐ and meristem‐expressed transcription factors or loss of certain chromatin‐modifying proteins induces spontaneous somatic embryogenesis. We begin this review with a general description of the major developmental events that define plant somatic embryogenesis and then focus on the transcriptional regulation of this process in the model plant Arabidopsis thaliana (arabidopsis). We describe the different somatic embryogenesis systems developed for arabidopsis and discuss the roles of transcription factors and chromatin modifications in this process. We describe how these somatic embryogenesis factors are interconnected and how their pathways converge at the level of hormones. Furthermore, the similarities between the developmental pathways in hormone‐ and transcription‐factor‐induced tissue culture systems are reviewed in the light of our recent findings on the somatic embryo‐inducing transcription factor BABY BOOM.

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Section: A Network Of Arabidopsis Transcription Factors Controls Somamentioning

confidence: 99%

A transcriptional view on somatic embryogenesis

2017

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“…1). Similarly, the leafy cotyledon1-2 mutation in Arabidopsis causes plants to express germination-specific genes without completely suppressing the expression of a storage protein gene that is normally expressed during the maturation phase of embryogenesis (5). Conversely, the raspberry mutant of Arabidopsis thaliana is blocked at a globular stage of embryogenesis, but expresses genes that are normally activated much later (6).…”

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Mutations of Arabidopsis thaliana that transform leaves into cotyledons

Poethig

1997

Proc. Natl. Acad. Sci. U.S.A.

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We describe mutations of three genes in Arabidopsis thaliana-extra cotyledon1 (xtc1), extra cotyledon2 (xtc2), and altered meristem programming1 (amp1)-that transform leaves into cotyledons. In all three of these mutations, this transformation is associated with a change in the timing of events in embryogenesis. xtc1 and xtc2 delay the morphogenesis of the embryo proper at the globular-to-heart transition but permit the shoot apex to develop to an unusually advanced stage late in embryogenesis. Both mutations have little or no effect on seed maturation and do not affect the viability of the shoot or the rate of leaf initiation after germination. amp1 perturbs the pattern of cell division at an early globular stage, dramatically increases the size of the shoot apex and, like xtc1 and xtc2, produces enlarged leaf primordia during seed development. These unusual phenotypes suggest that these genes play important regulatory roles in embryogenesis and demonstrate that the development of the shoot apical meristem and the development of the embryo proper are regulated by independent processes that must be temporally coordinated to ensure normal organ identity.Embryogenesis in seed plants consists of several discrete processes (1-4). During the early, morphogenetic phase of embryogenesis, the primary axis of the plant is established, one or more cotyledons are formed, and the primordia of the root and shoot systems are initiated. The embryo subsequently undergoes a process of maturation in which it acquires the capacity for autonomous growth, accumulates nutritional reserves, becomes desiccation tolerant, and then enters a period of dormancy. Upon germination, the seedling uses its stored reserves, and the shoot and root meristems resume growth. Recent work has shown that although these events usually occur in a predictable temporal sequence, they are not part of a linear developmental pathway (4). For example, in several species, precocious germination leads to the simultaneous expression of genes that are normally expressed only during embryo maturation and genes that are normally expressed only during germination (reviewed in ref. 1). Similarly, the leafy cotyledon1-2 mutation in Arabidopsis causes plants to express germination-specific genes without completely suppressing the expression of a storage protein gene that is normally expressed during the maturation phase of embryogenesis (5). Conversely, the raspberry mutant of Arabidopsis thaliana is blocked at a globular stage of embryogenesis, but expresses genes that are normally activated much later (6).To study how morphogenetic events are temporally coordinated during embryogenesis, we screened for mutations of A. thaliana that mimicked the cotyledon-leaf phenotype of precociously germinated Brassica napus embryos (7, 8). We identified three mutations that have this phenotype. Here we describe the effect of these mutations on the morphogenesis of the embryo and provide evidence that the effect of these mutations on leaf identity is the result of a change i...

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“…The Arabidopsis LEAFY COTYLEDON1 (LEC1) gene is expressed during embryogenesis, and its expression pattern is similar in both zygotic and somatic embryos (16)(17)(18). Loss-of-function mutation of LEC1 results in embryos that do not undergo developmental arrest and are nonviable because they are desiccation-intolerant (19)(20)(21)(22)(23). Ectopic expression of LEC1 in transgenic plants induces somatic embryos in vegetative cells (16).…”

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“…FUS3 is a LEC class gene that encodes a B3 domain protein (30,31). The Arabidopsis fus3 mutants resemble lec1 mutants morphologically (19,21,32), suggesting that both proteins regulate a common set of downstream genes (33). The KdFUS3 protein shares 64% identity with Arabidopsis FUS3.…”

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“…Three different versions of the KdLEC1 gene were inserted between the LEC1 promoter and terminator (36) (SI Table 2) and used to transform Arabidopsis Ws-O WT and lec1-1 mutant plants (37). Two versions of the KdLEC1 gene encoding defective B domains, either the endogenous (construct 1) or a modified version (construct 2) (SI Table 2), could not rescue the desiccation-intolerance of lec1-1 mutant embryos (16,19,21). However, when the deleted nucleotides of the KdLEC1 B domain were replaced by the corresponding nucleotides from the Arabidopsis LEC1-LIKE (L1L) gene (construct 3) to reconstitute a complete B domain, 0.65% of lec1-1 mutant seeds produced viable seedlings (SI Table 2).…”

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Evolution of asexual reproduction in leaves of the genus Kalanchoë

Garcês

Champagne

Townsley

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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108

100

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Plant somatic cells have the remarkable ability to regenerate an entire organism. Many species in the genus Kalanchoë , known as ''mother of thousands,'' develop plantlets on the leaf margins. Using key regulators of organogenesis (STM) and embryogenesis (LEC1 and FUS3) processes, we analyzed asexual reproduction in Kalanchoë leaves. Suppression of STM abolished the ability to make plantlets. Here, we report that constitutive plantlet-forming species, like Kalanchoë daigremontiana, form plantlets by coopting both organogenesis and embryogenesis programs into leaves. These species have a defective LEC1 gene and produce nonviable seed, whereas species that produce plantlets only upon stress induction have an intact LEC1 gene and produce viable seed. The latter species are basal in the genus, suggesting that inducedplantlet formation and seed viability are ancestral traits. We provide evidence that asexual reproduction likely initiated as a process of organogenesis and then recruited an embryogenesis program into the leaves in response to loss of sexual reproduction within this genus.nlike animal cells, somatic cells of plants are capable of regenerating the entire adult organism, and this potential for regeneration is called totipotency. In some plants, this ability is used as a mechanism of vegetative reproduction (1) and may represent the only means of reproduction. Species in the genus Kalanchoë (Crassulaceae) reproduce asexually by forming plantlets along their leaf margins. Although some of these species produce plantlets only when placed under stress (induced plantlet-forming species), others spontaneously make plantlets on leaves (constitutive plantlet-forming species). To date, leaf plantlet development in Kalanchoë has been studied extensively at the morphological and anatomical levels (2-10). Although these studies have provided detailed descriptive information, the morphogenic process involved in the origin of these plantlets and the different reproductive strategies undertaken by species of this genus are still not well understood.Genetic analyses of model species have identified key molecular regulators of organogenesis and embryogenesis. Loss-offunction mutations in Arabidopsis SHOOT MERISTEMLESS (STM), a class 1 KNOTTED1-LIKE HOMEOBOX (KNOX1) gene, result in plants that are unable to form a shoot apical meristem (SAM) and arrest at the seedling stage (11, 12). Transgenic plants constitutively overexpressing KNOX1 genes form ectopic shoots on leaves (13-15). The Arabidopsis LEAFY COTYLEDON1 (LEC1) gene is expressed during embryogenesis, and its expression pattern is similar in both zygotic and somatic embryos (16)(17)(18). Loss-of-function mutation of LEC1 results in embryos that do not undergo developmental arrest and are nonviable because they are desiccation-intolerant (19)(20)(21)(22)(23). Ectopic expression of LEC1 in transgenic plants induces somatic embryos in vegetative cells (16). Because leaf-plantlet formation resembles aspects of both STM and LEC1 overexpression phenotypes, we investigate...

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LEAFY COTYLEDON1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis

Cited by 150 publications

References 31 publications

A transcriptional view on somatic embryogenesis

A transcriptional view on somatic embryogenesis

Mutations of Arabidopsis thaliana that transform leaves into cotyledons

Evolution of asexual reproduction in leaves of the genus Kalanchoë

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