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Floral morphogenesis: stochastic explorations of a gene network epigenetic landscape.

Alvarez-Buylla ER, Chaos A, Aldana M, Benítez M, Cortes-Poza Y, Espinosa-Soto C, Hartasánchez DA, Lotto RB, Malkin D, Escalera Santos GJ, Padilla-Longoria P - PLoS ONE (2008)

Bottom Line: Thus, time ordering in the emergence of cell-fate patterns is not an artifact of synchronous updating in the Boolean model.Therefore, our model provides a novel explanation for the emergence and robustness of the ubiquitous temporal pattern of floral organ specification.It also constitutes a new approach to understanding morphogenesis, providing predictions on the population dynamics of cells with different genetic configurations during development.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ecología, Universidad Nacional Autónoma de México, Cd. Universitaria, México, D. F., México. elena.alvarezbuylla@gmail.com

ABSTRACT
In contrast to the classical view of development as a preprogrammed and deterministic process, recent studies have demonstrated that stochastic perturbations of highly non-linear systems may underlie the emergence and stability of biological patterns. Herein, we address the question of whether noise contributes to the generation of the stereotypical temporal pattern in gene expression during flower development. We modeled the regulatory network of organ identity genes in the Arabidopsis thaliana flower as a stochastic system. This network has previously been shown to converge to ten fixed-point attractors, each with gene expression arrays that characterize inflorescence cells and primordial cells of sepals, petals, stamens, and carpels. The network used is binary, and the logical rules that govern its dynamics are grounded in experimental evidence. We introduced different levels of uncertainty in the updating rules of the network. Interestingly, for a level of noise of around 0.5-10%, the system exhibited a sequence of transitions among attractors that mimics the sequence of gene activation configurations observed in real flowers. We also implemented the gene regulatory network as a continuous system using the Glass model of differential equations, that can be considered as a first approximation of kinetic-reaction equations, but which are not necessarily equivalent to the Boolean model. Interestingly, the Glass dynamics recover a temporal sequence of attractors, that is qualitatively similar, although not identical, to that obtained using the Boolean model. Thus, time ordering in the emergence of cell-fate patterns is not an artifact of synchronous updating in the Boolean model. Therefore, our model provides a novel explanation for the emergence and robustness of the ubiquitous temporal pattern of floral organ specification. It also constitutes a new approach to understanding morphogenesis, providing predictions on the population dynamics of cells with different genetic configurations during development.

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Flower development and gene network underlying primordial floral organ cell-fate determination in Arabidopsis thaliana.(A) The inflorescence meristem (IM in the Scanning Electron Micrography) is found at the apex of a reproductively mature plant. Within the IM, four regions can be distinguished. Interestingly, the experimentally observed gene activation configurations of each one of these regions are mimicked by the I1, I2, I3, and I4 attractors of the 15-gene GRN. Flower meristems arise in a helicoidal pattern from the flanks of the IM. The order in which floral meristems appear is indicated with numbers (1, oldest; 5, youngest). (B) Young flower meristems can be subdivided into four regions, each one containing the primordial cells that will eventually develop into the flower organs. In each floral meristem, the outermost region, which is first determined, will give rise to the sepal (se) primordium, the next to petals (pe) and finally, the primordial corresponding to stamens (st) and carpels (car) are determined in the center third and fourth whorls of the flower bud, respectively. (C) The mature flower of Arabidopsis thaliana. (D) I1, I2, I3, and I4 regions of the IM correspond to four of the attractors of the 15-gene GRN model. The expressed genes for each attractor are represented as gray circles, while the non-expressed genes correspond to white circles. (E) The other six attractors of the GRN model match gene expression profiles characteristic of sepal, petal (p1 and p2), stamen (st1 and st2), and carpel primordial cells. Black circles represent a gene (UFO) that can be either expressed or not expressed in the petal and stamen attractors, thus yielding two attractors for petal and stamen primordial cell-type. The gene activation profiles of the attractors recovered for the 15-gene GRN are congruent with the combinatorial activities of A, B, and C-type genes predicted by the ABC model of floral organ determination. See the Results section and [3], [12] for details. (F) Gene regulatory network model underlying cell fate determination in the IM and the flower meristem. A-genes (red), B-genes (yellow), and C-genes (blue) from the ABC model are indicated in the network.
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pone-0003626-g001: Flower development and gene network underlying primordial floral organ cell-fate determination in Arabidopsis thaliana.(A) The inflorescence meristem (IM in the Scanning Electron Micrography) is found at the apex of a reproductively mature plant. Within the IM, four regions can be distinguished. Interestingly, the experimentally observed gene activation configurations of each one of these regions are mimicked by the I1, I2, I3, and I4 attractors of the 15-gene GRN. Flower meristems arise in a helicoidal pattern from the flanks of the IM. The order in which floral meristems appear is indicated with numbers (1, oldest; 5, youngest). (B) Young flower meristems can be subdivided into four regions, each one containing the primordial cells that will eventually develop into the flower organs. In each floral meristem, the outermost region, which is first determined, will give rise to the sepal (se) primordium, the next to petals (pe) and finally, the primordial corresponding to stamens (st) and carpels (car) are determined in the center third and fourth whorls of the flower bud, respectively. (C) The mature flower of Arabidopsis thaliana. (D) I1, I2, I3, and I4 regions of the IM correspond to four of the attractors of the 15-gene GRN model. The expressed genes for each attractor are represented as gray circles, while the non-expressed genes correspond to white circles. (E) The other six attractors of the GRN model match gene expression profiles characteristic of sepal, petal (p1 and p2), stamen (st1 and st2), and carpel primordial cells. Black circles represent a gene (UFO) that can be either expressed or not expressed in the petal and stamen attractors, thus yielding two attractors for petal and stamen primordial cell-type. The gene activation profiles of the attractors recovered for the 15-gene GRN are congruent with the combinatorial activities of A, B, and C-type genes predicted by the ABC model of floral organ determination. See the Results section and [3], [12] for details. (F) Gene regulatory network model underlying cell fate determination in the IM and the flower meristem. A-genes (red), B-genes (yellow), and C-genes (blue) from the ABC model are indicated in the network.

Mentions: In plants, morphogenesis takes place during the entire life cycle from groups of undifferentiated cells called meristems. Within meristems, cell fate is mostly determined by position rather than by cell lineage [10]. Flower meristems are formed from the flanks of the inflorescence meristem, which is found at the apex of an Arabidopsis thaliana plant once it has reached a reproductive stage (Figures 1A and B). Early in flower development, a floral meristem is sequentially partitioned into four regions, from which the floral organ primordia are formed and eventually give rise to sepals in the outermost whorl, then to petals in the second whorl, stamens in the third, and carpels in the fourth whorl in the central part of the flower (Figures 1B and C). This spatio-temporal sequence is widely conserved among the quarter of a million flowering plant species [11]; however, the dynamic mechanisms underlying this robust pattern are not yet understood.


Floral morphogenesis: stochastic explorations of a gene network epigenetic landscape.

Alvarez-Buylla ER, Chaos A, Aldana M, Benítez M, Cortes-Poza Y, Espinosa-Soto C, Hartasánchez DA, Lotto RB, Malkin D, Escalera Santos GJ, Padilla-Longoria P - PLoS ONE (2008)

Flower development and gene network underlying primordial floral organ cell-fate determination in Arabidopsis thaliana.(A) The inflorescence meristem (IM in the Scanning Electron Micrography) is found at the apex of a reproductively mature plant. Within the IM, four regions can be distinguished. Interestingly, the experimentally observed gene activation configurations of each one of these regions are mimicked by the I1, I2, I3, and I4 attractors of the 15-gene GRN. Flower meristems arise in a helicoidal pattern from the flanks of the IM. The order in which floral meristems appear is indicated with numbers (1, oldest; 5, youngest). (B) Young flower meristems can be subdivided into four regions, each one containing the primordial cells that will eventually develop into the flower organs. In each floral meristem, the outermost region, which is first determined, will give rise to the sepal (se) primordium, the next to petals (pe) and finally, the primordial corresponding to stamens (st) and carpels (car) are determined in the center third and fourth whorls of the flower bud, respectively. (C) The mature flower of Arabidopsis thaliana. (D) I1, I2, I3, and I4 regions of the IM correspond to four of the attractors of the 15-gene GRN model. The expressed genes for each attractor are represented as gray circles, while the non-expressed genes correspond to white circles. (E) The other six attractors of the GRN model match gene expression profiles characteristic of sepal, petal (p1 and p2), stamen (st1 and st2), and carpel primordial cells. Black circles represent a gene (UFO) that can be either expressed or not expressed in the petal and stamen attractors, thus yielding two attractors for petal and stamen primordial cell-type. The gene activation profiles of the attractors recovered for the 15-gene GRN are congruent with the combinatorial activities of A, B, and C-type genes predicted by the ABC model of floral organ determination. See the Results section and [3], [12] for details. (F) Gene regulatory network model underlying cell fate determination in the IM and the flower meristem. A-genes (red), B-genes (yellow), and C-genes (blue) from the ABC model are indicated in the network.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2572848&req=5

pone-0003626-g001: Flower development and gene network underlying primordial floral organ cell-fate determination in Arabidopsis thaliana.(A) The inflorescence meristem (IM in the Scanning Electron Micrography) is found at the apex of a reproductively mature plant. Within the IM, four regions can be distinguished. Interestingly, the experimentally observed gene activation configurations of each one of these regions are mimicked by the I1, I2, I3, and I4 attractors of the 15-gene GRN. Flower meristems arise in a helicoidal pattern from the flanks of the IM. The order in which floral meristems appear is indicated with numbers (1, oldest; 5, youngest). (B) Young flower meristems can be subdivided into four regions, each one containing the primordial cells that will eventually develop into the flower organs. In each floral meristem, the outermost region, which is first determined, will give rise to the sepal (se) primordium, the next to petals (pe) and finally, the primordial corresponding to stamens (st) and carpels (car) are determined in the center third and fourth whorls of the flower bud, respectively. (C) The mature flower of Arabidopsis thaliana. (D) I1, I2, I3, and I4 regions of the IM correspond to four of the attractors of the 15-gene GRN model. The expressed genes for each attractor are represented as gray circles, while the non-expressed genes correspond to white circles. (E) The other six attractors of the GRN model match gene expression profiles characteristic of sepal, petal (p1 and p2), stamen (st1 and st2), and carpel primordial cells. Black circles represent a gene (UFO) that can be either expressed or not expressed in the petal and stamen attractors, thus yielding two attractors for petal and stamen primordial cell-type. The gene activation profiles of the attractors recovered for the 15-gene GRN are congruent with the combinatorial activities of A, B, and C-type genes predicted by the ABC model of floral organ determination. See the Results section and [3], [12] for details. (F) Gene regulatory network model underlying cell fate determination in the IM and the flower meristem. A-genes (red), B-genes (yellow), and C-genes (blue) from the ABC model are indicated in the network.
Mentions: In plants, morphogenesis takes place during the entire life cycle from groups of undifferentiated cells called meristems. Within meristems, cell fate is mostly determined by position rather than by cell lineage [10]. Flower meristems are formed from the flanks of the inflorescence meristem, which is found at the apex of an Arabidopsis thaliana plant once it has reached a reproductive stage (Figures 1A and B). Early in flower development, a floral meristem is sequentially partitioned into four regions, from which the floral organ primordia are formed and eventually give rise to sepals in the outermost whorl, then to petals in the second whorl, stamens in the third, and carpels in the fourth whorl in the central part of the flower (Figures 1B and C). This spatio-temporal sequence is widely conserved among the quarter of a million flowering plant species [11]; however, the dynamic mechanisms underlying this robust pattern are not yet understood.

Bottom Line: Thus, time ordering in the emergence of cell-fate patterns is not an artifact of synchronous updating in the Boolean model.Therefore, our model provides a novel explanation for the emergence and robustness of the ubiquitous temporal pattern of floral organ specification.It also constitutes a new approach to understanding morphogenesis, providing predictions on the population dynamics of cells with different genetic configurations during development.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ecología, Universidad Nacional Autónoma de México, Cd. Universitaria, México, D. F., México. elena.alvarezbuylla@gmail.com

ABSTRACT
In contrast to the classical view of development as a preprogrammed and deterministic process, recent studies have demonstrated that stochastic perturbations of highly non-linear systems may underlie the emergence and stability of biological patterns. Herein, we address the question of whether noise contributes to the generation of the stereotypical temporal pattern in gene expression during flower development. We modeled the regulatory network of organ identity genes in the Arabidopsis thaliana flower as a stochastic system. This network has previously been shown to converge to ten fixed-point attractors, each with gene expression arrays that characterize inflorescence cells and primordial cells of sepals, petals, stamens, and carpels. The network used is binary, and the logical rules that govern its dynamics are grounded in experimental evidence. We introduced different levels of uncertainty in the updating rules of the network. Interestingly, for a level of noise of around 0.5-10%, the system exhibited a sequence of transitions among attractors that mimics the sequence of gene activation configurations observed in real flowers. We also implemented the gene regulatory network as a continuous system using the Glass model of differential equations, that can be considered as a first approximation of kinetic-reaction equations, but which are not necessarily equivalent to the Boolean model. Interestingly, the Glass dynamics recover a temporal sequence of attractors, that is qualitatively similar, although not identical, to that obtained using the Boolean model. Thus, time ordering in the emergence of cell-fate patterns is not an artifact of synchronous updating in the Boolean model. Therefore, our model provides a novel explanation for the emergence and robustness of the ubiquitous temporal pattern of floral organ specification. It also constitutes a new approach to understanding morphogenesis, providing predictions on the population dynamics of cells with different genetic configurations during development.

Show MeSH