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The architecture of an empirical genotype-phenotype map


Aguilar-Rodríguez, José; Peel, Leto; Stella, Massimo; Wagner, Andreas; Payne, Joshua L (2018). The architecture of an empirical genotype-phenotype map. Evolution, 72(6):1242-1260.

Abstract

Recent advances in high‐throughput technologies are bringing the study of empirical genotype‐phenotype (GP) maps to the fore. Here, we use data from protein‐binding microarrays to study an empirical GP map of transcription factor (TF) ‐binding preferences. In this map, each genotype is a DNA sequence. The phenotype of this DNA sequence is its ability to bind one or more TFs. We study this GP map using genotype networks, in which nodes represent genotypes with the same phenotype, and edges connect nodes if their genotypes differ by a single small mutation. We describe the structure and arrangement of genotype networks within the space of all possible binding sites for 525 TFs from three eukaryotic species encompassing three kingdoms of life (animal, plant, and fungi). We thus provide a high‐resolution depiction of the architecture of an empirical GP map. Among a number of findings, we show that these genotype networks are “small‐world” and assortative, and that they ubiquitously overlap and interface with one another. We also use polymorphism data from Arabidopsis thaliana to show how genotype network structure influences the evolution of TF‐binding sites in vivo. We discuss our findings in the context of regulatory evolution.

Abstract

Recent advances in high‐throughput technologies are bringing the study of empirical genotype‐phenotype (GP) maps to the fore. Here, we use data from protein‐binding microarrays to study an empirical GP map of transcription factor (TF) ‐binding preferences. In this map, each genotype is a DNA sequence. The phenotype of this DNA sequence is its ability to bind one or more TFs. We study this GP map using genotype networks, in which nodes represent genotypes with the same phenotype, and edges connect nodes if their genotypes differ by a single small mutation. We describe the structure and arrangement of genotype networks within the space of all possible binding sites for 525 TFs from three eukaryotic species encompassing three kingdoms of life (animal, plant, and fungi). We thus provide a high‐resolution depiction of the architecture of an empirical GP map. Among a number of findings, we show that these genotype networks are “small‐world” and assortative, and that they ubiquitously overlap and interface with one another. We also use polymorphism data from Arabidopsis thaliana to show how genotype network structure influences the evolution of TF‐binding sites in vivo. We discuss our findings in the context of regulatory evolution.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Uncontrolled Keywords:Genetics, Ecology, Evolution, Behavior and Systematics, General Agricultural and Biological Sciences
Language:English
Date:1 June 2018
Deposited On:07 Mar 2019 10:39
Last Modified:07 Mar 2019 10:39
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:0014-3820
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1111/evo.13487
Project Information:
  • : FunderSNSF
  • : Grant ID31003A_146137
  • : Project TitlePhenotypic innovation, robustness, and recombination in genome-scale metabolic networks
  • : FunderSNSF
  • : Grant IDPZ00P3_154773
  • : Project TitleThe evolution and robustness of transcription factor binding sites

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Embargo till: 2019-04-20