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1.
PLoS Biol ; 17(10): e3000427, 2019 10.
Artículo en Inglés | MEDLINE | ID: mdl-31600203

RESUMEN

Leaves display a remarkable range of forms, from flat sheets with simple outlines to cup-shaped traps. Although much progress has been made in understanding the mechanisms of planar leaf development, it is unclear whether similar or distinctive mechanisms underlie shape transformations during development of more complex curved forms. Here, we use 3D imaging and cellular and clonal analysis, combined with computational modelling, to analyse the development of cup-shaped traps of the carnivorous plant Utricularia gibba. We show that the transformation from a near-spherical form at early developmental stages to an oblate spheroid with a straightened ventral midline in the mature form can be accounted for by spatial variations in rates and orientations of growth. Different hypotheses regarding spatiotemporal control predict distinct patterns of cell shape and size, which were tested experimentally by quantifying cellular and clonal anisotropy. We propose that orientations of growth are specified by a proximodistal polarity field, similar to that hypothesised to account for Arabidopsis leaf development, except that in Utricularia, the field propagates through a highly curved tissue sheet. Independent evidence for the polarity field is provided by the orientation of glandular hairs on the inner surface of the trap. Taken together, our results show that morphogenesis of complex 3D leaf shapes can be accounted for by similar mechanisms to those for planar leaves, suggesting that simple modulations of a common growth framework underlie the shaping of a diverse range of morphologies.


Asunto(s)
Carnivoría/fisiología , Lamiales/citología , Células Vegetales/ultraestructura , Desarrollo de la Planta/fisiología , Hojas de la Planta/citología , Polaridad Celular , Proliferación Celular , Forma de la Célula , Tamaño de la Célula , Lamiales/crecimiento & desarrollo , Hojas de la Planta/crecimiento & desarrollo
2.
PLoS Biol ; 16(11): e2005952, 2018 11.
Artículo en Inglés | MEDLINE | ID: mdl-30383040

RESUMEN

A developing plant organ exhibits complex spatiotemporal patterns of growth, cell division, cell size, cell shape, and organ shape. Explaining these patterns presents a challenge because of their dynamics and cross-correlations, which can make it difficult to disentangle causes from effects. To address these problems, we used live imaging to determine the spatiotemporal patterns of leaf growth and division in different genetic and tissue contexts. In the simplifying background of the speechless (spch) mutant, which lacks stomatal lineages, the epidermal cell layer exhibits defined patterns of division, cell size, cell shape, and growth along the proximodistal and mediolateral axes. The patterns and correlations are distinctive from those observed in the connected subepidermal layer and also different from the epidermal layer of wild type. Through computational modelling we show that the results can be accounted for by a dual control model in which spatiotemporal control operates on both growth and cell division, with cross-connections between them. The interactions between resulting growth and division patterns lead to a dynamic distributions of cell sizes and shapes within a deforming leaf. By modulating parameters of the model, we illustrate how phenotypes with correlated changes in cell size, cell number, and organ size may be generated. The model thus provides an integrated view of growth and division that can act as a framework for further experimental study.


Asunto(s)
División Celular/fisiología , Proliferación Celular/fisiología , Desarrollo de la Planta/fisiología , Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/fisiología , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/fisiología , Diferenciación Celular/genética , Diferenciación Celular/fisiología , Tamaño de la Célula , Regulación de la Expresión Génica de las Plantas/genética , Modelos Biológicos , Hojas de la Planta/crecimiento & desarrollo , Estomas de Plantas/genética , Estomas de Plantas/crecimiento & desarrollo , Análisis Espacio-Temporal
3.
Development ; 144(23): 4203-4213, 2017 12 01.
Artículo en Inglés | MEDLINE | ID: mdl-29183934

RESUMEN

The mechanisms by which organisms acquire their sizes and shapes through growth was a major focus of D'Arcy Thompson's book On Growth and Form. By applying mathematical and physical principles to a range of biological forms, Thompson achieved fresh insights, such as the notion that diverse biological shapes could be related through simple deformations of a coordinate system. However, Thompson considered genetics to lie outside the scope of his work, even though genetics was a growing discipline at the time the book was published. Here, we review how recent advances in cell, developmental, evolutionary and computational biology allow Thompson's ideas to be integrated with genes and the processes they influence to provide a deeper understanding of growth and morphogenesis. We consider how genes interact with subcellular-, cellular- and tissue-level processes in plants to yield patterns of growth that underlie the developmental and evolutionary shape transformations Thompson so eloquently described.


Asunto(s)
Morfogénesis/genética , Animales , Evolución Biológica , Tipificación del Cuerpo/genética , Biología Celular , Biología Computacional , Biología Evolutiva , Modelos Biológicos
4.
Development ; 143(18): 3394-406, 2016 09 15.
Artículo en Inglés | MEDLINE | ID: mdl-27624834

RESUMEN

Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue-level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity.


Asunto(s)
Brassicaceae/anatomía & histología , Brassicaceae/metabolismo , Frutas/anatomía & histología , Frutas/metabolismo , Anisotropía , Arabidopsis/anatomía & histología , Arabidopsis/metabolismo , Capsella/anatomía & histología , Capsella/metabolismo , Regulación de la Expresión Génica de las Plantas
5.
Science ; 380(6651): 1275-1281, 2023 06 23.
Artículo en Inglés | MEDLINE | ID: mdl-37347863

RESUMEN

Growth coordination between cell layers is essential for development of most multicellular organisms. Coordination may be mediated by molecular signaling and/or mechanical connectivity between cells, but how genes modify mechanical interactions between layers is unknown. Here we show that genes driving brassinosteroid synthesis promote growth of internal tissue, at least in part, by reducing mechanical epidermal constraint. We identified a brassinosteroid-deficient dwarf mutant in the aquatic plant Utricularia gibba with twisted internal tissue, likely caused by mechanical constraint from a slow-growing epidermis. We tested this hypothesis by showing that a brassinosteroid mutant in Arabidopsis enhances epidermal crack formation, indicative of increased tissue stress. We propose that by remodeling cell walls, brassinosteroids reduce epidermal constraint, showing how genes can control growth coordination between layers by means of mechanics.


Asunto(s)
Brasinoesteroides , Lamiales , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Brasinoesteroides/biosíntesis , Comunicación Celular , Pared Celular/metabolismo , Lamiales/citología , Lamiales/genética , Lamiales/metabolismo , Epidermis de la Planta/metabolismo
6.
Plant Cell ; 21(10): 2999-3007, 2009 Oct.
Artículo en Inglés | MEDLINE | ID: mdl-19880796

RESUMEN

Correlated variation in shape and size (allometry) is a major component of natural diversity. We examined the evolutionary and genetic basis for allometry using leaves and flower petals of snapdragon species (Antirrhinum). A computational method was developed to capture shape and size variation in both types of organ within the Antirrhinum species group. The results show that the major component of variation between species involves positively correlated changes in leaf and petal size. The correlation was maintained in an F2 population derived from crossing two species with organs of different sizes, suggesting that developmental constraints were involved. Identification of the underlying genes as quantitative trait loci revealed that the larger species carried alleles that increased organ size at all loci. Although this was initially taken as evidence that directional selection has driven diversity in both leaf and petal size, simulations revealed that evolution without consistent directional selection, an undirected walk, could also account for the parental distribution of organ size alleles.


Asunto(s)
Antirrhinum/genética , Evolución Biológica , Antirrhinum/anatomía & histología , Antirrhinum/clasificación , Flores/anatomía & histología , Flores/genética , Hojas de la Planta/anatomía & histología , Hojas de la Planta/genética
7.
PLoS Comput Biol ; 7(6): e1002071, 2011 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-21698124

RESUMEN

A major problem in biology is to understand how complex tissue shapes may arise through growth. In many cases this process involves preferential growth along particular orientations raising the question of how these orientations are specified. One view is that orientations are specified through stresses in the tissue (axiality-based system). Another possibility is that orientations can be specified independently of stresses through molecular signalling (polarity-based system). The axiality-based system has recently been explored through computational modelling. Here we develop and apply a polarity-based system which we call the Growing Polarised Tissue (GPT) framework. Tissue is treated as a continuous material within which regionally expressed factors under genetic control may interact and propagate. Polarity is established by signals that propagate through the tissue and is anchored in regions termed tissue polarity organisers that are also under genetic control. Rates of growth parallel or perpendicular to the local polarity may then be specified through a regulatory network. The resulting growth depends on how specified growth patterns interact within the constraints of mechanically connected tissue. This constraint leads to the emergence of features such as curvature that were not directly specified by the regulatory networks. Resultant growth feeds back to influence spatial arrangements and local orientations of tissue, allowing complex shapes to emerge from simple rules. Moreover, asymmetries may emerge through interactions between polarity fields. We illustrate the value of the GPT-framework for understanding morphogenesis by applying it to a growing Snapdragon flower and indicate how the underlying hypotheses may be tested by computational simulation. We propose that combinatorial intractions between orientations and rates of growth, which are a key feature of polarity-based systems, have been exploited during evolution to generate a range of observed biological shapes.


Asunto(s)
Antirrhinum/fisiología , Biología Computacional/métodos , Modelos Biológicos , Morfogénesis/fisiología , Anisotropía , Antirrhinum/anatomía & histología , Antirrhinum/citología , Antirrhinum/crecimiento & desarrollo , Polaridad Celular/fisiología , Simulación por Computador , Regulación de la Expresión Génica de las Plantas
8.
Science ; 367(6473): 91-96, 2020 01 03.
Artículo en Inglés | MEDLINE | ID: mdl-31753850

RESUMEN

Leaves vary from planar sheets and needle-like structures to elaborate cup-shaped traps. Here, we show that in the carnivorous plant Utricularia gibba, the upper leaf (adaxial) domain is restricted to a small region of the primordium that gives rise to the trap's inner layer. This restriction is necessary for trap formation, because ectopic adaxial activity at early stages gives radialized leaves and no traps. We present a model that accounts for the formation of both planar and nonplanar leaves through adaxial-abaxial domains of gene activity establishing a polarity field that orients growth. In combination with an orthogonal proximodistal polarity field, this system can generate diverse leaf forms and account for the multiple evolutionary origins of cup-shaped leaves through simple shifts in gene expression.


Asunto(s)
Evolución Biológica , Lamiales/anatomía & histología , Lamiales/fisiología , Hojas de la Planta/anatomía & histología , Hojas de la Planta/fisiología , Expresión Génica , Lamiales/genética , Hojas de la Planta/genética
9.
Open Biol ; 9(5): 190057, 2019 05 31.
Artículo en Inglés | MEDLINE | ID: mdl-31138099

RESUMEN

Differential growth is the driver of tissue morphogenesis in plants, and also plays a fundamental role in animal development. Although the contributions of growth to shape change have been captured through modelling tissue sheets or isotropic volumes, a framework for modelling both isotropic and anisotropic volumetric growth in three dimensions over large changes in size and shape has been lacking. Here, we describe an approach based on finite-element modelling of continuous volumetric structures, and apply it to a range of forms and growth patterns, providing mathematical validation for examples that admit analytic solution. We show that a major difference between sheet and bulk tissues is that the growth of bulk tissue is more constrained, reducing the possibility of tissue conflict resolution through deformations such as buckling. Tissue sheets or cylinders may be generated from bulk shapes through anisotropic specified growth, oriented by a polarity field. A second polarity field, orthogonal to the first, allows sheets with varying lengths and widths to be generated, as illustrated by the wide range of leaf shapes observed in nature. The framework we describe thus provides a key tool for developing hypotheses for plant morphogenesis and is also applicable to other tissues that deform through differential growth or contraction.


Asunto(s)
Morfogénesis , Fenómenos Fisiológicos de las Plantas , Animales , Anisotropía , Análisis de Elementos Finitos , Modelos Biológicos
10.
Nat Plants ; 4(9): 618-619, 2018 09.
Artículo en Inglés | MEDLINE | ID: mdl-30185983

Asunto(s)
Hojas de la Planta
11.
Science ; 335(6072): 1092-6, 2012 Mar 02.
Artículo en Inglés | MEDLINE | ID: mdl-22383846

RESUMEN

A major challenge in biology is to understand how buds comprising a few cells can give rise to complex plant and animal appendages like leaves or limbs. We address this problem through a combination of time-lapse imaging, clonal analysis, and computational modeling. We arrive at a model that shows how leaf shape can arise through feedback between early patterns of oriented growth and tissue deformation. Experimental tests through partial leaf ablation support this model and allow reevaluation of previous experimental studies. Our model allows a range of observed leaf shapes to be generated and predicts observed clone patterns in different species. Thus, our experimentally validated model may underlie the development and evolution of diverse organ shapes.


Asunto(s)
Modelos Biológicos , Morfogénesis , Hojas de la Planta/anatomía & histología , Hojas de la Planta/crecimiento & desarrollo , Antirrhinum/anatomía & histología , Antirrhinum/genética , Antirrhinum/crecimiento & desarrollo , Arabidopsis/anatomía & histología , Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Polaridad Celular , Simulación por Computador , Genes de Plantas , Hojas de la Planta/citología , Imagen de Lapso de Tiempo
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