Cargando…

Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?

Reproductive modes of vertebrates are classified into two major embryonic nutritional types: yolk deposits (i.e., lecithotrophy) and maternal investment (i.e., matrotrophy). Vitellogenin (VTG), a major egg yolk protein synthesized in the female liver, is one of the molecules relevant to the lecithot...

Descripción completa

Detalles Bibliográficos
Autores principales: Ohishi, Yuta, Arimura, Shogo, Shimoyama, Koya, Yamada, Kazuyuki, Yamauchi, Shinya, Horie, Taku, Hyodo, Susumu, Kuraku, Shigehiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10015161/
https://www.ncbi.nlm.nih.gov/pubmed/36808237
http://dx.doi.org/10.1093/gbe/evad028
_version_ 1784907156578893824
author Ohishi, Yuta
Arimura, Shogo
Shimoyama, Koya
Yamada, Kazuyuki
Yamauchi, Shinya
Horie, Taku
Hyodo, Susumu
Kuraku, Shigehiro
author_facet Ohishi, Yuta
Arimura, Shogo
Shimoyama, Koya
Yamada, Kazuyuki
Yamauchi, Shinya
Horie, Taku
Hyodo, Susumu
Kuraku, Shigehiro
author_sort Ohishi, Yuta
collection PubMed
description Reproductive modes of vertebrates are classified into two major embryonic nutritional types: yolk deposits (i.e., lecithotrophy) and maternal investment (i.e., matrotrophy). Vitellogenin (VTG), a major egg yolk protein synthesized in the female liver, is one of the molecules relevant to the lecithotrophy-to-matrotrophy shift in bony vertebrates. In mammals, all VTG genes are lost following the lecithotrophy-to-matrotrophy shift, and it remains to be elucidated whether the lecithotrophy-to-matrotrophy shift in nonmammalians is also associated with VTG repertoire modification. In this study, we focused on chondrichthyans (cartilaginous fishes)—a vertebrate clade that underwent multiple lecithotrophy-to-matrotrophy shifts. For an exhaustive search of homologs, we performed tissue-by-tissue transcriptome sequencing for two viviparous chondrichthyans, the frilled shark Chlamydoselachus anguineus and the spotless smooth-hound Mustelus griseus, and inferred the molecular phylogeny of VTG and its receptor very low-density lipoprotein receptor (VLDLR), across diverse vertebrates. As a result, we identified either three or four VTG orthologs in chondrichthyans including viviparous species. We also showed that chondrichthyans had two additional VLDLR orthologs previously unrecognized in their unique lineage (designated as VLDLRc2 and VLDLRc3). Notably, VTG gene expression patterns differed in the species studied depending on their reproductive mode; VTGs are broadly expressed in multiple tissues, including the uterus, in the two viviparous sharks, and in addition to the liver. This finding suggests that the chondrichthyans VTGs do not only function as the yolk nutrient but also as the matrotrophic factor. Altogether, our study indicates that the lecithotrophy-to-matrotrophy shift in chondrichthyans was achieved through a distinct evolutionary process from mammals.
format Online
Article
Text
id pubmed-10015161
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-100151612023-03-16 Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift? Ohishi, Yuta Arimura, Shogo Shimoyama, Koya Yamada, Kazuyuki Yamauchi, Shinya Horie, Taku Hyodo, Susumu Kuraku, Shigehiro Genome Biol Evol Article Reproductive modes of vertebrates are classified into two major embryonic nutritional types: yolk deposits (i.e., lecithotrophy) and maternal investment (i.e., matrotrophy). Vitellogenin (VTG), a major egg yolk protein synthesized in the female liver, is one of the molecules relevant to the lecithotrophy-to-matrotrophy shift in bony vertebrates. In mammals, all VTG genes are lost following the lecithotrophy-to-matrotrophy shift, and it remains to be elucidated whether the lecithotrophy-to-matrotrophy shift in nonmammalians is also associated with VTG repertoire modification. In this study, we focused on chondrichthyans (cartilaginous fishes)—a vertebrate clade that underwent multiple lecithotrophy-to-matrotrophy shifts. For an exhaustive search of homologs, we performed tissue-by-tissue transcriptome sequencing for two viviparous chondrichthyans, the frilled shark Chlamydoselachus anguineus and the spotless smooth-hound Mustelus griseus, and inferred the molecular phylogeny of VTG and its receptor very low-density lipoprotein receptor (VLDLR), across diverse vertebrates. As a result, we identified either three or four VTG orthologs in chondrichthyans including viviparous species. We also showed that chondrichthyans had two additional VLDLR orthologs previously unrecognized in their unique lineage (designated as VLDLRc2 and VLDLRc3). Notably, VTG gene expression patterns differed in the species studied depending on their reproductive mode; VTGs are broadly expressed in multiple tissues, including the uterus, in the two viviparous sharks, and in addition to the liver. This finding suggests that the chondrichthyans VTGs do not only function as the yolk nutrient but also as the matrotrophic factor. Altogether, our study indicates that the lecithotrophy-to-matrotrophy shift in chondrichthyans was achieved through a distinct evolutionary process from mammals. Oxford University Press 2023-02-20 /pmc/articles/PMC10015161/ /pubmed/36808237 http://dx.doi.org/10.1093/gbe/evad028 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Article
Ohishi, Yuta
Arimura, Shogo
Shimoyama, Koya
Yamada, Kazuyuki
Yamauchi, Shinya
Horie, Taku
Hyodo, Susumu
Kuraku, Shigehiro
Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title_full Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title_fullStr Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title_full_unstemmed Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title_short Egg Yolk Protein Homologs Identified in Live-Bearing Sharks: Co-Opted in the Lecithotrophy-to-Matrotrophy Shift?
title_sort egg yolk protein homologs identified in live-bearing sharks: co-opted in the lecithotrophy-to-matrotrophy shift?
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10015161/
https://www.ncbi.nlm.nih.gov/pubmed/36808237
http://dx.doi.org/10.1093/gbe/evad028
work_keys_str_mv AT ohishiyuta eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT arimurashogo eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT shimoyamakoya eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT yamadakazuyuki eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT yamauchishinya eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT horietaku eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT hyodosusumu eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift
AT kurakushigehiro eggyolkproteinhomologsidentifiedinlivebearingsharkscooptedinthelecithotrophytomatrotrophyshift