Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome

The generation of large immune gene families is often driven by evolutionary pressure exerted on host genomes by their pathogens, which has been described as the immunological arms race. The SpTransformer (SpTrf) gene family from the California purple sea urchin, Strongylocentrotus purpuratus, is up...

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Autores principales:	Megan A. Barela Hudgell, L. Courtney Smith
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	sea urchin invertebrate immunity Strongylocentrotus purpuratus gene family evolution large gene families Immunologic diseases. Allergy RC581-607
Acceso en línea:	https://doaj.org/article/166c087668174330b40fb5afaa665d63
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spelling	oai:doaj.org-article:166c087668174330b40fb5afaa665d632021-11-15T06:17:23ZSequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome1664-322410.3389/fimmu.2021.744783https://doaj.org/article/166c087668174330b40fb5afaa665d632021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fimmu.2021.744783/fullhttps://doaj.org/toc/1664-3224The generation of large immune gene families is often driven by evolutionary pressure exerted on host genomes by their pathogens, which has been described as the immunological arms race. The SpTransformer (SpTrf) gene family from the California purple sea urchin, Strongylocentrotus purpuratus, is upregulated upon immune challenge and encodes the SpTrf proteins that interact with pathogens during an immune response. Native SpTrf proteins bind both bacteria and yeast, and augment phagocytosis of a marine Vibrio, while a recombinant SpTrf protein (rSpTrf-E1) binds a subset of pathogens and a range of pathogen associated molecular patterns. In the sequenced sea urchin genome, there are four SpTrf gene clusters for a total of 17 genes. Here, we report an in-depth analysis of these genes to understand the sequence complexities of this family, its genomic structure, and to derive a putative evolutionary history for the formation of the gene clusters. We report a detailed characterization of gene structure including the intron type and UTRs with conserved transcriptional start sites, the start codon and multiple stop codons, and locations of polyadenylation signals. Phylogenetic and percent mismatch analyses of the genes and the intergenic regions allowed us to predict the last common ancestral SpTrf gene and a theoretical evolutionary history of the gene family. The appearance of the gene clusters from the theoretical ancestral gene may have been driven by multiple duplication and deletion events of regions containing SpTrf genes. Duplications and ectopic insertion events, indels, and point mutations in the exons likely resulted in the extant genes and family structure. This theoretical evolutionary history is consistent with the involvement of these genes in the arms race in responses to pathogens and suggests that the diversification of these genes and their encoded proteins have been selected for based on the survival benefits of pathogen binding and host protection.Megan A. Barela HudgellL. Courtney SmithFrontiers Media S.A.articlesea urchininvertebrate immunityStrongylocentrotus purpuratusgene family evolutionlarge gene familiesImmunologic diseases. AllergyRC581-607ENFrontiers in Immunology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	sea urchin invertebrate immunity Strongylocentrotus purpuratus gene family evolution large gene families Immunologic diseases. Allergy RC581-607
spellingShingle	sea urchin invertebrate immunity Strongylocentrotus purpuratus gene family evolution large gene families Immunologic diseases. Allergy RC581-607 Megan A. Barela Hudgell L. Courtney Smith Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
description	The generation of large immune gene families is often driven by evolutionary pressure exerted on host genomes by their pathogens, which has been described as the immunological arms race. The SpTransformer (SpTrf) gene family from the California purple sea urchin, Strongylocentrotus purpuratus, is upregulated upon immune challenge and encodes the SpTrf proteins that interact with pathogens during an immune response. Native SpTrf proteins bind both bacteria and yeast, and augment phagocytosis of a marine Vibrio, while a recombinant SpTrf protein (rSpTrf-E1) binds a subset of pathogens and a range of pathogen associated molecular patterns. In the sequenced sea urchin genome, there are four SpTrf gene clusters for a total of 17 genes. Here, we report an in-depth analysis of these genes to understand the sequence complexities of this family, its genomic structure, and to derive a putative evolutionary history for the formation of the gene clusters. We report a detailed characterization of gene structure including the intron type and UTRs with conserved transcriptional start sites, the start codon and multiple stop codons, and locations of polyadenylation signals. Phylogenetic and percent mismatch analyses of the genes and the intergenic regions allowed us to predict the last common ancestral SpTrf gene and a theoretical evolutionary history of the gene family. The appearance of the gene clusters from the theoretical ancestral gene may have been driven by multiple duplication and deletion events of regions containing SpTrf genes. Duplications and ectopic insertion events, indels, and point mutations in the exons likely resulted in the extant genes and family structure. This theoretical evolutionary history is consistent with the involvement of these genes in the arms race in responses to pathogens and suggests that the diversification of these genes and their encoded proteins have been selected for based on the survival benefits of pathogen binding and host protection.
format	article
author	Megan A. Barela Hudgell L. Courtney Smith
author_facet	Megan A. Barela Hudgell L. Courtney Smith
author_sort	Megan A. Barela Hudgell
title	Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
title_short	Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
title_full	Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
title_fullStr	Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
title_full_unstemmed	Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome
title_sort	sequence diversity, locus structure, and evolutionary history of the sptransformer genes in the sea urchin genome
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/166c087668174330b40fb5afaa665d63
work_keys_str_mv	AT meganabarelahudgell sequencediversitylocusstructureandevolutionaryhistoryofthesptransformergenesintheseaurchingenome AT lcourtneysmith sequencediversitylocusstructureandevolutionaryhistoryofthesptransformergenesintheseaurchingenome
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Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome

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