Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes

The de novo birth of functional genes from non-coding DNA as an important contributor to new gene formation is increasingly supported by evidence from diverse eukaryotic lineages. However, many uncertainties remain, including how the incipient de novo genes would continue to evolve and the molecular...

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Main Authors: Xuan Zhuang, C.-H. Christina Cheng
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/11/1777
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author Xuan Zhuang
C.-H. Christina Cheng
author_facet Xuan Zhuang
C.-H. Christina Cheng
author_sort Xuan Zhuang
collection DOAJ
description The de novo birth of functional genes from non-coding DNA as an important contributor to new gene formation is increasingly supported by evidence from diverse eukaryotic lineages. However, many uncertainties remain, including how the incipient de novo genes would continue to evolve and the molecular mechanisms underlying their evolutionary trajectory. Here we address these questions by investigating evolutionary history of the de novo antifreeze glycoprotein (AFGP) gene and gene family in gadid (codfish) lineages. We examined AFGP phenotype on a phylogenetic framework encompassing a broad sampling of gadids from freezing and non-freezing habitats. In three select species representing different AFGP-bearing clades, we analyzed all AFGP gene family members and the broader scale <i>AFGP</i> genomic regions in detail. Codon usage analyses suggest that motif duplication produced the intragenic AFGP tripeptide coding repeats, and rapid sequence divergence post-duplication stabilized the recombination-prone long repetitive coding region. Genomic loci analyses support <i>AFGP</i> originated once from a single ancestral genomic origin, and shed light on how the de novo gene proliferated into a gene family. Results also show the processes of gene duplication and gene loss are distinctive in separate clades, and both genotype and phenotype are commensurate with differential local selective pressures.
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spelling doaj.art-f2d432ad91d94eabb2707e52d8e7aa802023-11-22T23:28:39ZengMDPI AGGenes2073-44252021-11-011211177710.3390/genes12111777Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in CodfishesXuan Zhuang0C.-H. Christina Cheng1Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USADepartment of Evolution, Ecology, and Behavior, University of Illinois, Urbana-Champaign, IL 61801, USAThe de novo birth of functional genes from non-coding DNA as an important contributor to new gene formation is increasingly supported by evidence from diverse eukaryotic lineages. However, many uncertainties remain, including how the incipient de novo genes would continue to evolve and the molecular mechanisms underlying their evolutionary trajectory. Here we address these questions by investigating evolutionary history of the de novo antifreeze glycoprotein (AFGP) gene and gene family in gadid (codfish) lineages. We examined AFGP phenotype on a phylogenetic framework encompassing a broad sampling of gadids from freezing and non-freezing habitats. In three select species representing different AFGP-bearing clades, we analyzed all AFGP gene family members and the broader scale <i>AFGP</i> genomic regions in detail. Codon usage analyses suggest that motif duplication produced the intragenic AFGP tripeptide coding repeats, and rapid sequence divergence post-duplication stabilized the recombination-prone long repetitive coding region. Genomic loci analyses support <i>AFGP</i> originated once from a single ancestral genomic origin, and shed light on how the de novo gene proliferated into a gene family. Results also show the processes of gene duplication and gene loss are distinctive in separate clades, and both genotype and phenotype are commensurate with differential local selective pressures.https://www.mdpi.com/2073-4425/12/11/1777de novo genenew gene evolutionrepetitive proteingene family expansionevolutionary processmolecular mechanism
spellingShingle Xuan Zhuang
C.-H. Christina Cheng
Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
Genes
de novo gene
new gene evolution
repetitive protein
gene family expansion
evolutionary process
molecular mechanism
title Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
title_full Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
title_fullStr Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
title_full_unstemmed Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
title_short Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes
title_sort propagation of a de novo gene under natural selection antifreeze glycoprotein genes and their evolutionary history in codfishes
topic de novo gene
new gene evolution
repetitive protein
gene family expansion
evolutionary process
molecular mechanism
url https://www.mdpi.com/2073-4425/12/11/1777
work_keys_str_mv AT xuanzhuang propagationofadenovogeneundernaturalselectionantifreezeglycoproteingenesandtheirevolutionaryhistoryincodfishes
AT chchristinacheng propagationofadenovogeneundernaturalselectionantifreezeglycoproteingenesandtheirevolutionaryhistoryincodfishes