Cargando…

Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes

BACKGROUND: Nematodes are a widespread and diverse group comprising free-living and parasitic species, some of which have major detrimental effects on crops, animals, and human health. Genomic comparisons of nematodes may help reveal the genetic bases for the evolution of parasitic lifestyles. Fatty...

Descripción completa

Detalles Bibliográficos
Autores principales: Yuan, Dongjuan, Li, Song, Shang, Ziyu, Wan, Muchun, Lin, Yu, Zhang, Yanhua, Feng, Yaoyu, Xu, Lian, Xiao, Lihua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407040/
https://www.ncbi.nlm.nih.gov/pubmed/34461887
http://dx.doi.org/10.1186/s12915-021-01111-3
_version_ 1783746584324866048
author Yuan, Dongjuan
Li, Song
Shang, Ziyu
Wan, Muchun
Lin, Yu
Zhang, Yanhua
Feng, Yaoyu
Xu, Lian
Xiao, Lihua
author_facet Yuan, Dongjuan
Li, Song
Shang, Ziyu
Wan, Muchun
Lin, Yu
Zhang, Yanhua
Feng, Yaoyu
Xu, Lian
Xiao, Lihua
author_sort Yuan, Dongjuan
collection PubMed
description BACKGROUND: Nematodes are a widespread and diverse group comprising free-living and parasitic species, some of which have major detrimental effects on crops, animals, and human health. Genomic comparisons of nematodes may help reveal the genetic bases for the evolution of parasitic lifestyles. Fatty acid and retinol-binding proteins (FARs) are thought to be unique to nematodes and play essential roles in their development, reproduction, infection, and possibly parasitism through promoting the uptake, transport, and distribution of lipid and retinol. However, the evolution of FAR family proteins across the phylum Nematoda remains elusive. RESULTS: We report here the evolutionary relationship of the FAR gene family across nematodes. No FAR was found in Trichocephalida species and Romanomermis culicivorax from Clade I, and FAR could be found in species from Clades III, IV, and V. FAR proteins are conserved in Clade III species and separated into three clusters. Tandem duplications and high divergence events lead to variable richness and low homology of FARs in Steinernema of Clade IVa, Strongyloides of Clade IVb, and intestinal parasitic nematodes from Clades Vc and Ve. Moreover, different richness and sequence variations of FARs in pine wood, root-knot, stem, and cyst nematodes might be determined by reproduction mode or parasitism. However, murine lungworm Angiostrongylus and bovine lungworm Dictyocaulus viviparus from Clade Vd have only 3–4 orthologs of FAR. RNA-seq data showed that far genes, especially far-1 and far-2, were highly expressed in most nematodes. Angiostrongylus cantonensis FAR-1 and FAR-3 have low sequence homology and distinct ligand-binding properties, leading to differences in the cavity volume of proteins. These data indicate that FAR proteins diverged early and experienced low selective pressure to form genus-level diversity. The far genes are present in endophyte or root-colonized bacteria of Streptomyces, Kitasatospora sp., Bacillus subtilis, and Lysobacter, suggesting that bacterial far genes might be derived from plant-parasitic nematodes by horizontal gene transfer. CONCLUSIONS: Data from these comparative analyses have provided insights into genus-level diversity of FAR proteins in the phylum Nematoda. FAR diversification provides a glimpse into the complicated evolution history across free-living and parasitic nematodes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01111-3.
format Online
Article
Text
id pubmed-8407040
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-84070402021-09-01 Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes Yuan, Dongjuan Li, Song Shang, Ziyu Wan, Muchun Lin, Yu Zhang, Yanhua Feng, Yaoyu Xu, Lian Xiao, Lihua BMC Biol Research Article BACKGROUND: Nematodes are a widespread and diverse group comprising free-living and parasitic species, some of which have major detrimental effects on crops, animals, and human health. Genomic comparisons of nematodes may help reveal the genetic bases for the evolution of parasitic lifestyles. Fatty acid and retinol-binding proteins (FARs) are thought to be unique to nematodes and play essential roles in their development, reproduction, infection, and possibly parasitism through promoting the uptake, transport, and distribution of lipid and retinol. However, the evolution of FAR family proteins across the phylum Nematoda remains elusive. RESULTS: We report here the evolutionary relationship of the FAR gene family across nematodes. No FAR was found in Trichocephalida species and Romanomermis culicivorax from Clade I, and FAR could be found in species from Clades III, IV, and V. FAR proteins are conserved in Clade III species and separated into three clusters. Tandem duplications and high divergence events lead to variable richness and low homology of FARs in Steinernema of Clade IVa, Strongyloides of Clade IVb, and intestinal parasitic nematodes from Clades Vc and Ve. Moreover, different richness and sequence variations of FARs in pine wood, root-knot, stem, and cyst nematodes might be determined by reproduction mode or parasitism. However, murine lungworm Angiostrongylus and bovine lungworm Dictyocaulus viviparus from Clade Vd have only 3–4 orthologs of FAR. RNA-seq data showed that far genes, especially far-1 and far-2, were highly expressed in most nematodes. Angiostrongylus cantonensis FAR-1 and FAR-3 have low sequence homology and distinct ligand-binding properties, leading to differences in the cavity volume of proteins. These data indicate that FAR proteins diverged early and experienced low selective pressure to form genus-level diversity. The far genes are present in endophyte or root-colonized bacteria of Streptomyces, Kitasatospora sp., Bacillus subtilis, and Lysobacter, suggesting that bacterial far genes might be derived from plant-parasitic nematodes by horizontal gene transfer. CONCLUSIONS: Data from these comparative analyses have provided insights into genus-level diversity of FAR proteins in the phylum Nematoda. FAR diversification provides a glimpse into the complicated evolution history across free-living and parasitic nematodes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01111-3. BioMed Central 2021-08-30 /pmc/articles/PMC8407040/ /pubmed/34461887 http://dx.doi.org/10.1186/s12915-021-01111-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yuan, Dongjuan
Li, Song
Shang, Ziyu
Wan, Muchun
Lin, Yu
Zhang, Yanhua
Feng, Yaoyu
Xu, Lian
Xiao, Lihua
Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title_full Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title_fullStr Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title_full_unstemmed Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title_short Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
title_sort genus-level evolutionary relationships of far proteins reflect the diversity of lifestyles of free-living and parasitic nematodes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407040/
https://www.ncbi.nlm.nih.gov/pubmed/34461887
http://dx.doi.org/10.1186/s12915-021-01111-3
work_keys_str_mv AT yuandongjuan genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT lisong genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT shangziyu genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT wanmuchun genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT linyu genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT zhangyanhua genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT fengyaoyu genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT xulian genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes
AT xiaolihua genuslevelevolutionaryrelationshipsoffarproteinsreflectthediversityoflifestylesoffreelivingandparasiticnematodes