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Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution

Irrespective of the heuristic value of interpretations of developmental processes in terms of gene regulatory networks (GRNs), larger-angle views often suffer from: (i) an inadequate understanding of the relationship between genotype and phenotype; (ii) a predominantly zoocentric vision; and (iii) o...

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Autores principales: Minelli, Alessandro, Valero-Gracia, Alberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9179533/
https://www.ncbi.nlm.nih.gov/pubmed/35681485
http://dx.doi.org/10.3390/cells11111790
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author Minelli, Alessandro
Valero-Gracia, Alberto
author_facet Minelli, Alessandro
Valero-Gracia, Alberto
author_sort Minelli, Alessandro
collection PubMed
description Irrespective of the heuristic value of interpretations of developmental processes in terms of gene regulatory networks (GRNs), larger-angle views often suffer from: (i) an inadequate understanding of the relationship between genotype and phenotype; (ii) a predominantly zoocentric vision; and (iii) overconfidence in a putatively hierarchical organization of animal body plans. Here, we constructively criticize these assumptions. First, developmental biology is pervaded by adultocentrism, but development is not necessarily egg to adult. Second, during development, many unicells undergo transcriptomic profile transitions that are comparable to those recorded in pluricellular organisms; thus, their study should not be neglected from the GRN perspective. Third, the putatively hierarchical nature of the animal body is mirrored in the GRN logic, but in relating genotype to phenotype, independent assessments of the dynamics of the regulatory machinery and the animal’s architecture are required, better served by a combinatorial than by a hierarchical approach. The trade-offs between spatial and temporal aspects of regulation, as well as their evolutionary consequences, are also discussed. Multicellularity may derive from a unicell’s sequential phenotypes turned into different but coexisting, spatially arranged cell types. In turn, polyphenism may have been a crucial mechanism involved in the origin of complex life cycles.
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spelling pubmed-91795332022-06-10 Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution Minelli, Alessandro Valero-Gracia, Alberto Cells Perspective Irrespective of the heuristic value of interpretations of developmental processes in terms of gene regulatory networks (GRNs), larger-angle views often suffer from: (i) an inadequate understanding of the relationship between genotype and phenotype; (ii) a predominantly zoocentric vision; and (iii) overconfidence in a putatively hierarchical organization of animal body plans. Here, we constructively criticize these assumptions. First, developmental biology is pervaded by adultocentrism, but development is not necessarily egg to adult. Second, during development, many unicells undergo transcriptomic profile transitions that are comparable to those recorded in pluricellular organisms; thus, their study should not be neglected from the GRN perspective. Third, the putatively hierarchical nature of the animal body is mirrored in the GRN logic, but in relating genotype to phenotype, independent assessments of the dynamics of the regulatory machinery and the animal’s architecture are required, better served by a combinatorial than by a hierarchical approach. The trade-offs between spatial and temporal aspects of regulation, as well as their evolutionary consequences, are also discussed. Multicellularity may derive from a unicell’s sequential phenotypes turned into different but coexisting, spatially arranged cell types. In turn, polyphenism may have been a crucial mechanism involved in the origin of complex life cycles. MDPI 2022-05-30 /pmc/articles/PMC9179533/ /pubmed/35681485 http://dx.doi.org/10.3390/cells11111790 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Perspective
Minelli, Alessandro
Valero-Gracia, Alberto
Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title_full Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title_fullStr Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title_full_unstemmed Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title_short Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution
title_sort spatially and temporally distributed complexity—a refreshed framework for the study of grn evolution
topic Perspective
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9179533/
https://www.ncbi.nlm.nih.gov/pubmed/35681485
http://dx.doi.org/10.3390/cells11111790
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