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Genus-Level Evolutionary Relationships of FAR Proteins Reflect the Diversity

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Genus-Level Evolutionary Relationships of FAR Proteins Reflect the Diversity Yuan et al. BMC Biology (2021) 19:178 https://doi.org/10.1186/s12915-021-01111-3 RESEARCH ARTICLE Open Access Genus-level evolutionary relationships of FAR proteins reflect the diversity of lifestyles of free-living and parasitic nematodes Dongjuan Yuan1,2, Song Li1,2, Ziyu Shang1,2, Muchun Wan1,2, Yu Lin1,2, Yanhua Zhang3, Yaoyu Feng1,2, Lian Xu4* and Lihua Xiao1,2* Abstract 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. * Correspondence: [email protected]; [email protected] 4Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Co-innovation Center of Neuroregeneration, Nantong University, Nantong 226019, China 1Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural University, Guangzhou 510642, China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This 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/. The Creative Commons Public Domain Dedication waiver (http://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. Yuan et al. BMC Biology (2021) 19:178 Page 2 of 18 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. Keywords: Fatty acid and retinol-binding protein, Evolution, Expansion, Nematoda, Transcriptome Background [18, 24, 25]. However, the evolution of FAR across the Parasitic nematodes infect animals and plants as well as phylum Nematoda remains elusive. human beings, causing detrimental impacts on economic Growing genomic and transcriptomic data are now crops, farm animals, and human health. Comparative available for many nematodes, including free-living genomics studies indicated that the fewer orthologs were nematodes of C. elegans, Rhabditophanes sp., Pristino- found in the lipid biosynthesis and metabolism of para- chus,andDiploscapter coronatus; pine wood, stem, root- sitic nematodes than in free-living C. elegans [1–3]. knot, and cyst nematodes of plants; whipworm, Ascaris, Lipids are hydrophobic components, including fatty Onchocerca, lymphatic filaria, hookworm; other nema- acids, phospholipids, cholesterol, steroids, and fat- todes of veterinary importance; and insect-parasitic soluble vitamins. Lipids play diverse roles in regulating nematodes Romanomermis culicivorax and Steinernema physiological and pathological functions of organisms. spp. In the present study, we analyzed gene number, Fatty acids are important components in the synthesis structure, origin, evolution of FAR in 58 nematodes, and and construction of epidermis and influence embryo transcription pattern of the far gene across developmen- development [4–6]. Polyunsaturated fatty acids (PUFAs) tal stages of several nematodes. We detected genes and their metabolites are signaling molecules and encoding FAR proteins in genomes of most nematodes participate in regulating signal transduction and post- as well as trematode Schistosome mansoni, cestode translational modifications to promote the development, Echinococcus multilocularis, free-living Schmidtea reproduction, and lifespan of worms and are even mediterranea, and bacteria. We further assessed ligand- involved in pathogenic processes following nematode binding properties and structure of FAR protein from infection of a host [7–12]. Retinol or retinoic acid and Angiostrongylus cantonensis, the rat lung worm. fat-soluble vitamins direct programmed spermatogonial and meiotic differentiation that are essential for the gen- Results eration of functional spermatozoa [13, 14]. Furthermore, Loss, duplication, and genus-level expansion of far genes retinoic acid also affects a wide variety of biological in nematodes membranes and plays an important role in regulating We found 586 FAR proteins from 58 nematode species signaling pathways and tissue differentiation, tissue by searching for the Gp-FAR-1 domain (pfam05823, repairs, and the IgA and Th2 cytokine levels [15]. Due Additional file 2: Table S1). The FAR domain was not to the fewer orthologs in fatty acid biosynthesis and found in 5 species from Clade I, but present in Clades metabolism pathways compared to free-living C. elegans III, IV, and V. The median number of far genes in 53 [1, 2], parasitic nematodes might rely on lipid binding species from Clades III, IV, and V was 5. The number of and transport proteins to absorb, transport, and phago- the far genes varied at the genus level (Fig. 1 and cytose various lipid or metabolic molecules from their Additional file 3: Table S2). The number of the far genes hosts. ranged from 1 to 5 in Clade III, and being 3 in most spe- Fatty acid and retinol-binding protein (FAR), first cies in Clade IIIc. In Clade IV, the number of the far discovered in Onchocerca volvulus [16], is a secretory genes in plant-parasitic nematodes (1-7, in Clade IVc) protein. The mRNA for its expression was localized in was significantly lower than in entomopathogenic nema- the hypodermis below the cuticle in in situ hybridization tode Steinernema (37-43, in Clade IVa) and partheno- studies of plant-parasitic nematodes [17, 18]. FAR is genetic nematode Strongyloides (16, in Clade IVb) (Fig. 1 widely known as a unique protein in nematodes, en- and Additional file 1: Fig. S1). Variations in numbers of gaging in promoting the uptake, transport, and distribu- far genes in Clade V was detected not only among free- tion of lipid and retinol. Comparative genomics studies living nematodes C. elegans (9, in Clade Vb), D. corona- showed the presence of FAR expansions in some Steiner- tus (6, in Clade Vb), and Pristinochus (21-23, in Clade nema spp. and strongylids [19, 20]. Functional studies Va), but also among parasitic nematodes of Angiostron- through gene silencing indicated that far-1 could regu- gylus (3-4, in Clade Vd), Dictyocaulus viviparus (4, in late the development and reproduction of nematodes Clade Vd), and expanded Ancylostoma (18-30, in Clade [17, 21–23]. A few reports showed that FAR could affect Vc), Nippostrongylus brasiliensis (12, in Clade Ve), and the infection and pathogenicity of nematodes in plants Haemonchus (12-19, in Clade Ve) (Fig. 1 and Additional Yuan et al. BMC Biology (2021) 19:178 Page 3 of 18 Fig. 1 Comparison of Gene Numbers of far in 58 nematodes. The range of definitive hosts and intermediate hosts of the nematodes is shown. Taxonomic classification of nematodes was retrieved from the Taxonomy database. The topology of Nematoda phylogeny was inferred as described
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