Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera

Homeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome...

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Main Authors: Mulhair, PO, Crowley, L, Boyes, DH, Harper, A, Lewis, OT, Holland, PWH
Other Authors: Darwin Tree of Life Consortium
Format: Journal article
Language:English
Published: Cold Spring Harbor Laboratory Press 2022
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author Mulhair, PO
Crowley, L
Boyes, DH
Harper, A
Lewis, OT
Holland, PWH
author2 Darwin Tree of Life Consortium
author_facet Darwin Tree of Life Consortium
Mulhair, PO
Crowley, L
Boyes, DH
Harper, A
Lewis, OT
Holland, PWH
author_sort Mulhair, PO
collection OXFORD
description Homeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome assemblies mean that little is known about the dynamics of homeobox gene evolution across Lepidoptera or about how changes in homeobox gene number and organization relate to diversity in this large order of insects. Here we analyze an extensive data set of high-quality genomes to characterize the number and organization of all homeobox genes in 123 species of Lepidoptera from 23 taxonomic families. We find most Lepidoptera have around 100 homeobox loci, including an unusual Hox gene cluster in which the <i>lab</i> gene is repositioned and the <i>ro</i> gene is next to <i>pb</i>. A topologically associating domain spans much of the gene cluster, suggesting deep regulatory conservation of the Hox cluster arrangement in this insect order. Most Lepidoptera have four Shx genes, divergent <i>zen</i>-derived loci, but these loci underwent dramatic duplication in several lineages, with some moths having over 165 homeobox loci in the Hox gene cluster; this expansion is associated with local LINE element density. In contrast, the NK gene cluster content is more stable, although there are differences in organization compared with other insects, as well as major rearrangements within butterflies. Our analysis represents the first description of homeobox gene content across the order Lepidoptera, exemplifying the potential of newly generated genome assemblies for understanding genome and gene family evolution.
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spelling oxford-uuid:1b9e2682-c2e0-4313-a65d-1b1d8bb215662023-03-30T14:49:43ZDiversity, duplication, and genomic organization of homeobox genes in LepidopteraJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:1b9e2682-c2e0-4313-a65d-1b1d8bb21566EnglishSymplectic ElementsCold Spring Harbor Laboratory Press2022Mulhair, POCrowley, LBoyes, DHHarper, ALewis, OTHolland, PWHDarwin Tree of Life ConsortiumHomeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome assemblies mean that little is known about the dynamics of homeobox gene evolution across Lepidoptera or about how changes in homeobox gene number and organization relate to diversity in this large order of insects. Here we analyze an extensive data set of high-quality genomes to characterize the number and organization of all homeobox genes in 123 species of Lepidoptera from 23 taxonomic families. We find most Lepidoptera have around 100 homeobox loci, including an unusual Hox gene cluster in which the <i>lab</i> gene is repositioned and the <i>ro</i> gene is next to <i>pb</i>. A topologically associating domain spans much of the gene cluster, suggesting deep regulatory conservation of the Hox cluster arrangement in this insect order. Most Lepidoptera have four Shx genes, divergent <i>zen</i>-derived loci, but these loci underwent dramatic duplication in several lineages, with some moths having over 165 homeobox loci in the Hox gene cluster; this expansion is associated with local LINE element density. In contrast, the NK gene cluster content is more stable, although there are differences in organization compared with other insects, as well as major rearrangements within butterflies. Our analysis represents the first description of homeobox gene content across the order Lepidoptera, exemplifying the potential of newly generated genome assemblies for understanding genome and gene family evolution.
spellingShingle Mulhair, PO
Crowley, L
Boyes, DH
Harper, A
Lewis, OT
Holland, PWH
Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title_full Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title_fullStr Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title_full_unstemmed Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title_short Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera
title_sort diversity duplication and genomic organization of homeobox genes in lepidoptera
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