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Complete Inactivation of Sebum-Producing Genes Parallels the Loss of Sebaceous Glands in Cetacea

Complete Inactivation of Sebum-Producing Genes Parallels the Loss of Sebaceous Glands in Cetacea


Title: Complete Inactivation of Sebum-Producing Genes Parallels the Loss of Sebaceous Glands in Cetacea
Author: Lopes-Marques, Mónica
Machado, André M
Alves, Luís Q
Fonseca, Miguel M
Barbosa, Susana
Sinding, Mikkel-Holger S
Rasmussen, Marianne   orcid.org/0000-0002-6887-8616
Iversen, Maria Refsgaard
Frost Bertelsen, Mads
Campos, Paula F
... 3 more authors Show all authors
Date: 2019-03-20
Language: English
Scope: 1270-1280
University/Institute: Háskóli Íslands
University of Iceland
Department: Rannsóknasetur á Húsavík (HÍ)
Research Centre in Húsavík (HÍ)
Series: Molecular Biology and Evolution;36(6)
ISSN: 0737-4038
1537-1719 (eISSN)
DOI: 10.1093/molbev/msz068
Subject: Comparative genomics; Gene loss; Marine mammals; Skin lipids; Genamengi; DNA-rannsóknir; Sjávarspendýr; Fituefni
URI: https://hdl.handle.net/20.500.11815/1732

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Citation:

Mónica Lopes-Marques, André M Machado, Luís Q Alves, Miguel M Fonseca, Susana Barbosa, Mikkel-Holger S Sinding, Marianne Helene Rasmussen, Maria Refsgaard Iversen, Mads Frost Bertelsen, Paula F Campos, Rute da Fonseca, Raquel Ruivo, L Filipe C Castro, Complete Inactivation of Sebum-Producing Genes Parallels the Loss of Sebaceous Glands in Cetacea, Molecular Biology and Evolution, Volume 36, Issue 6, June 2019, Pages 1270–1280, https://doi.org/10.1093/molbev/msz068

Abstract:

Genomes are dynamic biological units, with processes of gene duplication and loss triggering evolutionary novelty. The mammalian skin provides a remarkable case study on the occurrence of adaptive morphological innovations. Skin sebaceous glands (SGs), for instance, emerged in the ancestor of mammals serving pivotal roles, such as lubrication, waterproofing, immunity, and thermoregulation, through the secretion of sebum, a complex mixture of various neutral lipids such as triacylglycerol, free fatty acids, wax esters, cholesterol, and squalene. Remarkably, SGs are absent in a few mammalian lineages, including the iconic Cetacea. We investigated the evolution of the key molecular components responsible for skin sebum production: Dgat2l6, Awat1, Awat2, Elovl3, Mogat3, and Fabp9. We show that all analyzed genes have been rendered nonfunctional in Cetacea species (toothed and baleen whales). Transcriptomic analysis, including a novel skin transcriptome from blue whale, supports gene inactivation. The conserved mutational pattern found in most analyzed genes, indicates that pseudogenization events took place prior to the diversification of modern Cetacea lineages. Genome and skin transcriptome analysis of the common hippopotamus highlighted the convergent loss of a subset of sebum-producing genes, notably Awat1 and Mogat3. Partial loss profiles were also detected in non-Cetacea aquatic mammals, such as the Florida manatee, and in terrestrial mammals displaying specialized skin phenotypes such as the African elephant, white rhinoceros and pig. Our findings reveal a unique landscape of “gene vestiges” in the Cetacea sebum-producing compartment, with limited gene loss observed in other mammalian lineages: suggestive of specific adaptations or specializations of skin lipids.

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This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited

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