Limits...
Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis: a dynamic spatial model.

Benítez M, Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER - BMC Syst Biol (2008)

Bottom Line: The meta-GRN model shows that interlinked sub-networks contribute redundantly to the formation of robust hair patterns and permits to advance novel and testable predictions regarding the effect of cell shape, signalling pathways and additional gene interactions affecting spatial cell-patterning.Pursuing dynamic analyses of larger (genomic) coupled networks is still not possible.A repertoire of well-characterised regulatory modules, like the one presented here, will, however, help to uncover general principles of the patterning-associated networks, as well as the peculiarities that originate diversity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria 3er Circuito Exterior, Junto Jardín Botánico Exterior, Coyoacán 04510, DF, Mexico. marianabk@gmail.com

ABSTRACT

Background: Dynamical models are instrumental for exploring the way information required to generate robust developmental patterns arises from complex interactions among genetic and non-genetic factors. We address this fundamental issue of developmental biology studying the leaf and root epidermis of Arabidopsis. We propose an experimentally-grounded model of gene regulatory networks (GRNs) that are coupled by protein diffusion and comprise a meta-GRN implemented on cellularised domains.

Results: Steady states of the meta-GRN model correspond to gene expression profiles typical of hair and non-hair epidermal cells. The simulations also render spatial patterns that match the cellular arrangements observed in root and leaf epidermis. As in actual plants, such patterns are robust in the face of diverse perturbations. We validated the model by checking that it also reproduced the patterns of reported mutants. The meta-GRN model shows that interlinked sub-networks contribute redundantly to the formation of robust hair patterns and permits to advance novel and testable predictions regarding the effect of cell shape, signalling pathways and additional gene interactions affecting spatial cell-patterning.

Conclusion: The spatial meta-GRN model integrates available experimental data and contributes to further understanding of the Arabidopsis epidermal system. It also provides a systems biology framework to explore the interplay among sub-networks of a GRN, cell-to-cell communication, cell shape and domain traits, which could help understanding of general aspects of patterning processes. For instance, our model suggests that the information needed for cell fate determination emerges from dynamic processes that depend upon molecular components inside and outside differentiating cells, suggesting that the classical distinction of lineage versus positional cell differentiation may be instrumental but rather artificial. It also suggests that interlinkage of nonlinear and redundant sub-networks in larger networks is important for pattern robustness. Pursuing dynamic analyses of larger (genomic) coupled networks is still not possible. A repertoire of well-characterised regulatory modules, like the one presented here, will, however, help to uncover general principles of the patterning-associated networks, as well as the peculiarities that originate diversity.

Show MeSH
Cellular patterns and meta-gene regulatory network models for leaf and root Arabidopsis epidermis. Spaced-out pattern of trichome distribution in the leaf of Arabidopsis thaliana (A). Root-hairs (green) are arranged in bands that overlie the junction of two cortex cells (yellow) (B). Coupled gene regulatory network (GRN) model for cell type determination in leaf epidermis (C). GRN underlying cell-fate determination in root epidermis (D). (E) and (F) represent the GRN for leaf and root epidermis, respectively. In both networks, nodes correspond to genes, arrows stand for positive regulatory interactions and flat-end edges stand for negative ones. Red nodes represent elements that are able to move among cells and couple the GRN into meta-GRN. Red lines stand for intercellular interactions established by mobile elements. Asterisks in (B) and (D) indicate the H position where the cortex-related signal is acting.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2600786&req=5

Figure 1: Cellular patterns and meta-gene regulatory network models for leaf and root Arabidopsis epidermis. Spaced-out pattern of trichome distribution in the leaf of Arabidopsis thaliana (A). Root-hairs (green) are arranged in bands that overlie the junction of two cortex cells (yellow) (B). Coupled gene regulatory network (GRN) model for cell type determination in leaf epidermis (C). GRN underlying cell-fate determination in root epidermis (D). (E) and (F) represent the GRN for leaf and root epidermis, respectively. In both networks, nodes correspond to genes, arrows stand for positive regulatory interactions and flat-end edges stand for negative ones. Red nodes represent elements that are able to move among cells and couple the GRN into meta-GRN. Red lines stand for intercellular interactions established by mobile elements. Asterisks in (B) and (D) indicate the H position where the cortex-related signal is acting.

Mentions: Arabidopsis leaf epidermis bears hairs (trichomes) that tend to appear away from each other (Figure 1A; [21]), while root epidermis exhibits trichoblast (root hair precursors) and atrichoblasts arranged in bands of a single cell type (Figure 1B; [22,23]). Despite the contrasting spatial patterns, epidermal cell type determination in root and leaf appears to be associated with similar GRNs (Figures 1E and 1F). Furthermore, although root and leaf GRNs exhibit some differences, they seem to be qualitatively equivalent in dynamical terms [18,24].


Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis: a dynamic spatial model.

Benítez M, Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER - BMC Syst Biol (2008)

Cellular patterns and meta-gene regulatory network models for leaf and root Arabidopsis epidermis. Spaced-out pattern of trichome distribution in the leaf of Arabidopsis thaliana (A). Root-hairs (green) are arranged in bands that overlie the junction of two cortex cells (yellow) (B). Coupled gene regulatory network (GRN) model for cell type determination in leaf epidermis (C). GRN underlying cell-fate determination in root epidermis (D). (E) and (F) represent the GRN for leaf and root epidermis, respectively. In both networks, nodes correspond to genes, arrows stand for positive regulatory interactions and flat-end edges stand for negative ones. Red nodes represent elements that are able to move among cells and couple the GRN into meta-GRN. Red lines stand for intercellular interactions established by mobile elements. Asterisks in (B) and (D) indicate the H position where the cortex-related signal is acting.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2600786&req=5

Figure 1: Cellular patterns and meta-gene regulatory network models for leaf and root Arabidopsis epidermis. Spaced-out pattern of trichome distribution in the leaf of Arabidopsis thaliana (A). Root-hairs (green) are arranged in bands that overlie the junction of two cortex cells (yellow) (B). Coupled gene regulatory network (GRN) model for cell type determination in leaf epidermis (C). GRN underlying cell-fate determination in root epidermis (D). (E) and (F) represent the GRN for leaf and root epidermis, respectively. In both networks, nodes correspond to genes, arrows stand for positive regulatory interactions and flat-end edges stand for negative ones. Red nodes represent elements that are able to move among cells and couple the GRN into meta-GRN. Red lines stand for intercellular interactions established by mobile elements. Asterisks in (B) and (D) indicate the H position where the cortex-related signal is acting.
Mentions: Arabidopsis leaf epidermis bears hairs (trichomes) that tend to appear away from each other (Figure 1A; [21]), while root epidermis exhibits trichoblast (root hair precursors) and atrichoblasts arranged in bands of a single cell type (Figure 1B; [22,23]). Despite the contrasting spatial patterns, epidermal cell type determination in root and leaf appears to be associated with similar GRNs (Figures 1E and 1F). Furthermore, although root and leaf GRNs exhibit some differences, they seem to be qualitatively equivalent in dynamical terms [18,24].

Bottom Line: The meta-GRN model shows that interlinked sub-networks contribute redundantly to the formation of robust hair patterns and permits to advance novel and testable predictions regarding the effect of cell shape, signalling pathways and additional gene interactions affecting spatial cell-patterning.Pursuing dynamic analyses of larger (genomic) coupled networks is still not possible.A repertoire of well-characterised regulatory modules, like the one presented here, will, however, help to uncover general principles of the patterning-associated networks, as well as the peculiarities that originate diversity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria 3er Circuito Exterior, Junto Jardín Botánico Exterior, Coyoacán 04510, DF, Mexico. marianabk@gmail.com

ABSTRACT

Background: Dynamical models are instrumental for exploring the way information required to generate robust developmental patterns arises from complex interactions among genetic and non-genetic factors. We address this fundamental issue of developmental biology studying the leaf and root epidermis of Arabidopsis. We propose an experimentally-grounded model of gene regulatory networks (GRNs) that are coupled by protein diffusion and comprise a meta-GRN implemented on cellularised domains.

Results: Steady states of the meta-GRN model correspond to gene expression profiles typical of hair and non-hair epidermal cells. The simulations also render spatial patterns that match the cellular arrangements observed in root and leaf epidermis. As in actual plants, such patterns are robust in the face of diverse perturbations. We validated the model by checking that it also reproduced the patterns of reported mutants. The meta-GRN model shows that interlinked sub-networks contribute redundantly to the formation of robust hair patterns and permits to advance novel and testable predictions regarding the effect of cell shape, signalling pathways and additional gene interactions affecting spatial cell-patterning.

Conclusion: The spatial meta-GRN model integrates available experimental data and contributes to further understanding of the Arabidopsis epidermal system. It also provides a systems biology framework to explore the interplay among sub-networks of a GRN, cell-to-cell communication, cell shape and domain traits, which could help understanding of general aspects of patterning processes. For instance, our model suggests that the information needed for cell fate determination emerges from dynamic processes that depend upon molecular components inside and outside differentiating cells, suggesting that the classical distinction of lineage versus positional cell differentiation may be instrumental but rather artificial. It also suggests that interlinkage of nonlinear and redundant sub-networks in larger networks is important for pattern robustness. Pursuing dynamic analyses of larger (genomic) coupled networks is still not possible. A repertoire of well-characterised regulatory modules, like the one presented here, will, however, help to uncover general principles of the patterning-associated networks, as well as the peculiarities that originate diversity.

Show MeSH