Constraint and contingency in multifunctional gene regulatory circuits.
Gene regulatory circuits drive the development, physiology, and behavior of organisms from bacteria to humans. The phenotypes or functions of such circuits are embodied in the gene expression patterns they form. Regulatory circuits are typically multifunctional, forming distinct gene expression patt...
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2013
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oai:doaj.org-article:f614bff6e45843878790e3f9024085042021-11-18T05:52:06ZConstraint and contingency in multifunctional gene regulatory circuits.1553-734X1553-735810.1371/journal.pcbi.1003071https://doaj.org/article/f614bff6e45843878790e3f9024085042013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23762020/?tool=EBIhttps://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Gene regulatory circuits drive the development, physiology, and behavior of organisms from bacteria to humans. The phenotypes or functions of such circuits are embodied in the gene expression patterns they form. Regulatory circuits are typically multifunctional, forming distinct gene expression patterns in different embryonic stages, tissues, or physiological states. Any one circuit with a single function can be realized by many different regulatory genotypes. Multifunctionality presumably constrains this number, but we do not know to what extent. We here exhaustively characterize a genotype space harboring millions of model regulatory circuits and all their possible functions. As a circuit's number of functions increases, the number of genotypes with a given number of functions decreases exponentially but can remain very large for a modest number of functions. However, the sets of circuits that can form any one set of functions becomes increasingly fragmented. As a result, historical contingency becomes widespread in circuits with many functions. Whether a circuit can acquire an additional function in the course of its evolution becomes increasingly dependent on the function it already has. Circuits with many functions also become increasingly brittle and sensitive to mutation. These observations are generic properties of a broad class of circuits and independent of any one circuit genotype or phenotype.Joshua L PayneAndreas WagnerPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 9, Iss 6, p e1003071 (2013) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Joshua L Payne Andreas Wagner Constraint and contingency in multifunctional gene regulatory circuits. |
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Gene regulatory circuits drive the development, physiology, and behavior of organisms from bacteria to humans. The phenotypes or functions of such circuits are embodied in the gene expression patterns they form. Regulatory circuits are typically multifunctional, forming distinct gene expression patterns in different embryonic stages, tissues, or physiological states. Any one circuit with a single function can be realized by many different regulatory genotypes. Multifunctionality presumably constrains this number, but we do not know to what extent. We here exhaustively characterize a genotype space harboring millions of model regulatory circuits and all their possible functions. As a circuit's number of functions increases, the number of genotypes with a given number of functions decreases exponentially but can remain very large for a modest number of functions. However, the sets of circuits that can form any one set of functions becomes increasingly fragmented. As a result, historical contingency becomes widespread in circuits with many functions. Whether a circuit can acquire an additional function in the course of its evolution becomes increasingly dependent on the function it already has. Circuits with many functions also become increasingly brittle and sensitive to mutation. These observations are generic properties of a broad class of circuits and independent of any one circuit genotype or phenotype. |
format |
article |
author |
Joshua L Payne Andreas Wagner |
author_facet |
Joshua L Payne Andreas Wagner |
author_sort |
Joshua L Payne |
title |
Constraint and contingency in multifunctional gene regulatory circuits. |
title_short |
Constraint and contingency in multifunctional gene regulatory circuits. |
title_full |
Constraint and contingency in multifunctional gene regulatory circuits. |
title_fullStr |
Constraint and contingency in multifunctional gene regulatory circuits. |
title_full_unstemmed |
Constraint and contingency in multifunctional gene regulatory circuits. |
title_sort |
constraint and contingency in multifunctional gene regulatory circuits. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2013 |
url |
https://doaj.org/article/f614bff6e45843878790e3f902408504 |
work_keys_str_mv |
AT joshualpayne constraintandcontingencyinmultifunctionalgeneregulatorycircuits AT andreaswagner constraintandcontingencyinmultifunctionalgeneregulatorycircuits |
_version_ |
1718424765447798784 |