Regulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development

The shoot apical meristem of Arabidopsis thaliana consists of three cell layers that proliferate to give rise to the aerial organs of the plant. By labeling cells in each layer using an Ac-based transposable element system, we mapped their contributions to the floral organs, as well as determined the degree of plasticity in this developmental process. We found that each cell layer proliferates to give rise to predictable derivatives: the L1 contributes to the epidermis, the stigma, part of the transmitting tract and the integument of the ovules, while the L2 and L3 contribute, to different degrees, to the mesophyll and other internal tissues. In order to test the roles of the floral homeotic genes in regulating these patterns of cell proliferation, we carried out similar clonal analyses in apetala3-3 and agamous-1 mutant plants. Our results suggest that cell division patterns are regulated differently at different stages of floral development. In early floral stages, the pattern of cell divisions is dependent on position in the floral meristem, and not on future organ identity. Later, during organogenesis, the layer contributions to the organs are controlled by the homeotic genes. We also show that AGAMOUS is required to maintain the layered structure of the meristem prior to organ initiation, as well as having a non-autonomous role in the regulation of the layer contributions to the petals.

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Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems

Development ◽

10.1242/dev.121.1.27 ◽

1995 ◽

Vol 121 (1) ◽

pp. 27-35 ◽

Cited By ~ 13

Author(s):

S.S. Hantke ◽

R. Carpenter ◽

E.S. Coen

Keyword(s):

Cell Layer ◽

Homeotic Genes ◽

Expression Domain ◽

Phenotypic Properties ◽

Organ Identity ◽

Cell Layers ◽

Periclinal Chimeras ◽

Meristem Identity ◽

Cell Autonomy ◽

Floral Meristems

We show that the flowering sectors on plants mutant for floricaula (flo), a meristem identity gene in Antirrhinum majus, are periclinal chimeras expressing flo in either the L1, L2 or L3 cell layer. Flower morphology is almost normal in L1 chimeras, but altered in L2 and L3 chimeras. Expression of flo in any one cell layer results in the expression of organ identity genes, deficiens (def) and plena (ple) in all three cell layers of the chimeras, showing that flo acts inductively to promote gene transcription. The activation of both def and ple is delayed, and the expression domain of def is reduced, accounting for some of the phenotypic properties of the chimeras. Furthermore, we show that flo exhibits some cell-autonomy with respect to autoregulation.

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Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking

Development ◽

10.1242/dev.122.11.3433 ◽

1996 ◽

Vol 122 (11) ◽

pp. 3433-3441 ◽

Cited By ~ 8

Author(s):

M.C. Perbal ◽

G. Haughn ◽

H. Saedler ◽

Z. Schwarz-Sommer

Keyword(s):

Cell Layer ◽

Epidermal Cells ◽

Molecular Techniques ◽

Cell Trafficking ◽

Mads Box ◽

Organ Identity ◽

Cell Layers ◽

Periclinal Chimeras ◽

The Difference ◽

Cell Autonomy

In Antirrhinum majus, petal and stamen organ identity is controlled by two MADS-box transcription factors, DEFICIENS and GLOBOSA. Mutations in either of these genes result in the replacement of petals by sepaloid organs and stamens by carpelloid organs. Somatically stable def and glo periclinal chimeras, generated by transposon excision events, were used to study the non-cell-autonomous functions of these two MADS-box proteins. Two morphologically distinct types of chimeras were analysed using genetic, morphological and molecular techniques. Restoration of DEF expression in the L1 cell layer results in the reestablishment of DEF and GLO functions in L1-derived cells only; inner layer cells retain their mutant sepaloid features. Nevertheless, this activity is sufficient to allow the expansion of petal lobes, highlighting the role of DEF in the stimulation of cell proliferation and/or cell shape and elongation when expressed in the L1 layer. Establishment of DEF or GLO expression in L2 and L3 cell layers is accompanied by the recovery of petaloid identity of the epidermal cells but it is insufficient to allow petal lobe expansion. We show by in situ immunolocalisation that the non-cell-autonomy is due to direct trafficking of DEF and GLO proteins from the inner layer to the epidermal cells. At least for DEF, this movement appears to be polar since DEF acts cell-autonomously when expressed in the L1 cell layer. Furthermore, the petaloid revertant sectors observed on second whorl mutant organs and the mutant margins of petals of L2L3 chimeras suggest that DEF and GLO intradermal movement is limited. This restriction may reflect the difference in the regulation of primary plasmodesmata connecting cells from the same layer and secondary plasmodesmata connecting cells from different layers. We propose that control of intradermal trafficking of DEF and GLO could play a role in maintaining of the boundaries of their expression domains.

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An Analysis of Cell Proliferation in the Apical Meristem of Lateral Roots of Vicia faba L.

Annals of Botany ◽

10.1093/oxfordjournals.aob.a085202 ◽

1976 ◽

Vol 40 (4) ◽

pp. 865-875 ◽

Cited By ~ 5

Author(s):

R. D. MACLEOD

Keyword(s):

Cell Proliferation ◽

Vicia Faba ◽

Apical Meristem ◽

Lateral Roots ◽

Vicia Faba L

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Molecular mechanism of cytokinin-activated cell division in Arabidopsis

Science ◽

10.1126/science.abe2305 ◽

2021 ◽

Vol 371 (6536) ◽

pp. 1350-1355

Author(s):

Weibing Yang ◽

Sandra Cortijo ◽

Niklas Korsbo ◽

Pawel Roszak ◽

Katharina Schiessl ◽

...

Keyword(s):

Cell Proliferation ◽

Cell Division ◽

Histidine Kinase ◽

Feedback Loop ◽

Apical Meristem ◽

Nuclear Accumulation ◽

Cytokinin Signaling ◽

Positive Feedback Loop ◽

Nuclear Shuttling ◽

Stimulate Cell Proliferation

Mitogens trigger cell division in animals. In plants, cytokinins, a group of phytohormones derived from adenine, stimulate cell proliferation. Cytokinin signaling is initiated by membrane-associated histidine kinase receptors and transduced through a phosphorelay system. We show that in the Arabidopsis shoot apical meristem (SAM), cytokinin regulates cell division by promoting nuclear shuttling of Myb-domain protein 3R4 (MYB3R4), a transcription factor that activates mitotic gene expression. Newly synthesized MYB3R4 protein resides predominantly in the cytoplasm. At the G2-to-M transition, rapid nuclear accumulation of MYB3R4—consistent with an associated transient peak in cytokinin concentration—feeds a positive feedback loop involving importins and initiates a transcriptional cascade that drives mitosis and cytokinesis. An engineered nuclear-restricted MYB3R4 mimics the cytokinin effects of enhanced cell proliferation and meristem growth.

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Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana

Development ◽

10.1242/dev.116.2.397 ◽

1992 ◽

Vol 116 (2) ◽

pp. 397-403 ◽

Cited By ~ 19

Author(s):

H. M. Ottoline Leyser ◽

I. J. Furner

Keyword(s):

Arabidopsis Thaliana ◽

Root Growth ◽

Shoot Apical Meristem ◽

Apical Meristem ◽

Floral Development ◽

Wild Type ◽

Recessive Mutations ◽

Phenotypic Characterisation ◽

Dicotyledonous Plants ◽

And Function

The shoot apical meristem of dicotyledonous plants is highly regulated both structurally and functionally, but little is known about the mechanisms involved in this regulation. Here we describe the genetic and phenotypic characterisation of recessive mutations at three loci of Arabidopsis thaliana in which meristem structure and function are disrupted. The loci are Clavata1 (Clv1), Fasciata1 (Fas1) and Fasciata2 (Fas2). Plants mutant at these loci are fasciated having broad, flat stems and disrupted phyllotaxy. In all cases, the fasciations are associated with shoot apical meristem enlargement and altered floral development. While all the mutants share some phenotypic features they can be divided into two classes. The pleiotropic fas1 and fas2 mutants are unable to initiate wild- type organs, show major alterations in meristem structure and have reduced root growth. In contrast, clv1 mutant plants show near wild-type organ phenotypes, more subtle changes in shoot apical meristem structure and wild-type root growth.

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CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS

Development ◽

10.1242/dev.126.11.2377 ◽

1999 ◽

Vol 126 (11) ◽

pp. 2377-2386 ◽

Cited By ~ 15

Author(s):

J. Alvarez ◽

D.R. Smyth

Keyword(s):

Radial Growth ◽

Genetic Evidence ◽

Longitudinal Growth ◽

Transmitting Tract ◽

The Third ◽

Organ Identity ◽

Carpel Development ◽

Carpel Wall

To help understand the process of carpel morphogenesis, the roles of three carpel development genes have been partitioned genetically. Mutants of CRABS CLAW cause the gynoecium to develop into a wider but shorter structure, and the two carpels are unfused at the apex. Mutants of a second gene, SPATULA, show reduced growth of the style, stigma, and septum, and the transmitting tract is absent. Double mutants of crabs claw and spatula with homeotic mutants that develop ectopic carpels demonstrate that CRABS CLAW and SPATULA are necessary for, and inseparable from, carpel development, and that their action is negatively regulated by A and B organ identity genes. The third carpel gene studied, AGAMOUS, encodes C function that has been proposed to fully specify carpel identity. When AGAMOUS function is removed together with the A class gene APETALA2, however, the organs retain many carpelloid properties, suggesting that other genes are also involved. We show here that further mutant disruption of both CRABS CLAW and SPATULA function removes remaining carpelloid properties, revealing that the three genes together are necessary to generate the mature gynoecium. In particular, AGAMOUS is required to specify the identity of the carpel wall and to promote the stylar outgrowth at the apex, CRABS CLAW suppresses radial growth of the developing gynoecium but promotes its longitudinal growth, and SPATULA supports development of the carpel margins and tissues derived from them. The three genes mostly act independently, although there is genetic evidence that CRABS CLAW enhances AGAMOUS and SPATULA function.

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Phi Thickenings in Fossil Seed Plants from Antarctica

IAWA Journal ◽

10.1163/22941932-90001046 ◽

1987 ◽

Vol 8 (3) ◽

pp. 191-201 ◽

Cited By ~ 16

Author(s):

Michael A. Millay ◽

Thomas N. Taylor ◽

Edith L. Taylor

Keyword(s):

Middle Triassic ◽

Cell Layer ◽

Vascular Cambium ◽

Secondary Development ◽

Water Regulation ◽

Secondary Phloem ◽

Primary Xylem ◽

Sieve Cells ◽

Ray Parenchyma ◽

Cell Layers

Primary anatomy and secondary development is described for two root types from the Fremouw Peak locality (Transantarctic Mts, Antarctica) of early to middle Triassic age. Roots of Antarcticycas have a bilayered cortex with thick surface cuticle, diarch xylem, and a clearIy defined endodermis surrounded by a single cell layer possessing phi thickenings. Secondary development begins with phellern and phelloderm production from the out er primary phloem position, and is followed bya bifacial vascular cambium next to the primary xylem that pro duces sieve cells and ray parenchyma to the outside. Young roots of Antarcticoxylon are similar to those of Antarcticycas, but may possess 2-3 cell layers with phi thickenings. Secondary development from a bifacial vascular cambium produces alternating bands of sieve cells and phloem parenchyma cells in the secondary phloem and wood with uniseriate rays and scattered axial parenchyma. The presence of phi thickenings and an epidermal cutieie in both roots suggests environmental stress related to water regulation. The occurrence of phi thickenings in the roots of some conifers, angiosperms, a fossil cycad and a probable seed fern suggests this character is of ecological rather than phylogenetic significance.

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Molecular characterization of berry color locus on the portuguese cv. ‘Fernão Pires’ and cv. ‘Verdelho’ and their red-berried somatic variant cultivars

Ciência e Técnica Vitivinícola ◽

10.1051/ctv/20183302184 ◽

2018 ◽

Vol 33 (2) ◽

pp. 184-190

Author(s):

Vanessa Ferreira ◽

Isaura Castro ◽

David Carrasco ◽

Olinda Pinto-Carnide ◽

Rosa Arroyo-García

Keyword(s):

Skin Color ◽

Apical Meristem ◽

Genomic Region ◽

Grape Berry ◽

Color Variation ◽

Berry Skin ◽

Somatic Variant ◽

Functional Allele ◽

Cell Layers

Genotyping studies are increasing the knowledge on grapevine biodiversity, particularly regarding grape berry skin color somatic variants, supporting the research on the color trait. This study aimed to evaluate the effect of the berry color locus, and its surrounding genomic region, on the color variation of the Portuguese white-skinned cultivars ‘Fernão Pires’ and ‘Verdelho’ and its derived red-berried somatic variants cv. ‘Fernão Pires Rosado’ and cv. ‘Verdelho Roxo’, respectively. The analysis of Gret1 insertion within the VvMYBA1 gene revealed no polymorphism responsible for white-to-red shift of the red-skinned cv. ‘Fernão Pires Rosado’ and cv. ‘Verdelho Roxo’. Moreover, VvMYBA2 showed an important role regarding the phenotypic variation of cv. ‘Fernão Pires’, through the recovery of the functional allele G on cv. ‘Fernão Pires Rosado’. Regarding the data obtained for cv. ‘Verdelho’ and cv. ‘Verdelho Roxo’, both cultivars showed Gret1 insertion on VvMYBA1 and non-functional T allele on VvMYBA2 in homozygosity for both cell layers of shoot apical meristem, suggesting the occurrence of other mutational events responsible for the color gain.

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