Nucleotide diversity of functionally different groups of immune response genes in Old World camels based on newly annotated and reference-guided assemblies

. 2020 Sep 03 ; 21 (1) : 606. [epub] 20200903

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32883205

Grantová podpora
P 29623 Austrian Science Fund FWF - Austria
P29623-B25 Austrian Science Fund
CEECIND/00372/2018 Fundação para a Ciência e a Tecnologia

Odkazy

PubMed 32883205
PubMed Central PMC7468183
DOI 10.1186/s12864-020-06990-4
PII: 10.1186/s12864-020-06990-4
Knihovny.cz E-zdroje

BACKGROUND: Immune-response (IR) genes have an important role in the defense against highly variable pathogens, and therefore, diversity in these genomic regions is essential for species' survival and adaptation. Although current genome assemblies from Old World camelids are very useful for investigating genome-wide diversity, demography and population structure, they have inconsistencies and gaps that limit analyses at local genomic scales. Improved and more accurate genome assemblies and annotations are needed to study complex genomic regions like adaptive and innate IR genes. RESULTS: In this work, we improved the genome assemblies of the three Old World camel species - domestic dromedary and Bactrian camel, and the two-humped wild camel - via different computational methods. The newly annotated dromedary genome assembly CamDro3 served as reference to scaffold the NCBI RefSeq genomes of domestic Bactrian and wild camels. These upgraded assemblies were then used to assess nucleotide diversity of IR genes within and between species, and to compare the diversity found in immune genes and the rest of the genes in the genome. We detected differences in the nucleotide diversity among the three Old World camelid species and between IR gene groups, i.e., innate versus adaptive. Among the three species, domestic Bactrian camels showed the highest mean nucleotide diversity. Among the functionally different IR gene groups, the highest mean nucleotide diversity was observed in the major histocompatibility complex. CONCLUSIONS: The new camel genome assemblies were greatly improved in terms of contiguity and increased size with fewer scaffolds, which is of general value for the scientific community. This allowed us to perform in-depth studies on genetic diversity in immunity-related regions of the genome. Our results suggest that differences of diversity across classes of genes appear compatible with a combined role of population history and differential exposures to pathogens, and consequent different selective pressures.

Zobrazit více v PubMed

Van Houte S, Ekroth AKE, Broniewski JM, Chabas H, Ashby B, Bondy-denomy J, et al. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature. 2016;532:385. PubMed PMC

Ramey HR, Decker JE, McKay SD, et al. Detection of selective sweeps in cattle using genome-wide SNP data. BMC Genomics. 2013;14:382. PubMed PMC

Horrocks NPC, Matson KD, Tieleman BI. Pathogen pressure puts immune defense into perspective. Integr Comp Biol. 2011;51:563–576. PubMed

Plasil M, Mohandesan E, Fitak RR, Musilova P, Kubickova S, Burger PA, et al. The major histocompatibility complex in Old World camelids and low polymorphism of its class II genes. BMC Genomics. 2016;17:167. doi: 10.1186/s12864-016-2500-1. PubMed DOI PMC

Trowsdale J, Knight JC. Major histocompatibility complex genomics and human disease. Annu Rev Genomics Hum Genet. 2013;14:301–323. PubMed PMC

Jepson A, Banya W, Sisay-Joof F, Hassan-King M, Nunes C, Bennett S, et al. Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Infect Immun. 1997;65:872–876. PubMed PMC

Acevedo-Whitehouse K, Cunningham AA. Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol. 2006;21:433–438. PubMed

Fitak RR, Mohandesan E, Corander J, Burger PA. The de novo genome assembly and annotation of a female domestic dromedary of north African origin. Mol Ecol Resour. 2016;16:314–324. PubMed PMC

Jirimutu Wang Z, et al. Genome sequences of wild and domestic bactrian camels Nat Commun. 2012;3:1202. PubMed PMC

Wu H, Guang X, Al-Fageeh MB, et al. Camelid genomes reveal evolution and adaptation to desert environments. Nat Commun. 2014;5:5188. PubMed

Elbers JP, Rogers MF, Perelman PL, Proskuryakova AA, Serdyukova NA, Johnson WE, et al. Improving Illumina assemblies with hi-C and long reads: an example with the north African dromedary. Mol Ecol Resour. 2019;19:1015–1026. PubMed PMC

Ming L, Wang Z, Yi L, Batmunkh M, Liu T, Siren D, et al. Chromosome-level assembly of wild Bactrian camel genome reveals organization of immune gene loci. Mol Ecol Resour. 2020;00:1–11. PubMed

Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60. PubMed

Holt, C., Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 2011;12(491). PubMed PMC

Yandell M, Ence D. A beginner’s guide to eukaryotic genome annotation. Nat Rev Genet. 2012;13:329–342. doi: 10.1038/nrg3174. PubMed DOI

Kolmogorov M, Raney B, Paten B, Pham S. Ragout - a reference-assisted assembly tool for bacterial genomes. Bioinformatics. 2014;30:i302–i309. PubMed PMC

Paten B, Diekhans M, Earl D, John JS, Ma J, Suh B, et al. Cactus graphs for genome comparisons. J Comput Biol. 2011;18:469–481. PubMed PMC

Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol. 2012;13:R56. PubMed PMC

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–3212. PubMed

Zdobnov EM, Tegenfeldt F, Kuznetsov D, Waterhouse RM, Simao FA, Ioannidis P, et al. OrthoDB v9.1: cataloging evolutionary and functional annotations for animal, fungal, plant, archaeal, bacterial and viral orthologs. Nucleic Acids Res. 2017;45:D744–D749. PubMed PMC

Fitak RR, Mohandesan E, Corander J, Yadamsuren A, Chuluunbat B, Abdelhadi O, et al. Genomic signatures of domestication in Old World. Commun Biol. 2020;3:1–10. doi: 10.1038/s42003-020-1039-5. PubMed DOI PMC

Avila F, Baily MP, Perelman P, Das PJ, Pontius J, Chowdhary R, et al. A comprehensive whole-genome integrated cytogenetic map for the alpaca (Lama pacos) Cytogenet Genome Res. 2014;144:196–207. PubMed

Muyldermans S, Baral TN, Retamozzo VC, De Baetselier P, De Genst E, Kinne J, et al. Camelid immunoglobulins and nanobody technology. Vet Immunol Immunopathol. 2009;128:178–183. doi: 10.1016/j.vetimm.2008.10.299. PubMed DOI

Antonacci R, Linguiti G, Burger PA, Castelli V, Pala A, Fitak R, et al. Comprehensive genomic analysis of the dromedary T cell receptor gamma (TRG) locus and identification of a functional TRGC5 cassette. Dev Comp Immunol. 2020;106:103614. PubMed

Futas J, Oppelt J, Jelinek A, Elbers JP, Wijacki J, Knoll A, et al. Natural killer cell receptor genes in camels: Another mammalian model. Front Genet. 2019;10 JUL:1–15. PubMed PMC

Vaccarelli G, Antonacci R, Tasco G, Yang F, Giordano L, El Ashmaoui HM, et al. Generation of diversity by somatic mutation in the Camelus dromedarius T-cell receptor gamma variable domains. Eur J Immunol. 2012;42:3416–3428. PubMed

Abbas B, Omer OH. Review of infectious diseases of the camel. Vet Bull. 2005;75:1–16.

Wernery U, Kinne J. Foot and mouth disease and similar virus infections in camelids: a review. Rev Sci Tech - Off Int des épizooties. 2012;31:907–918. PubMed

Hemida MG, Chu DKW, Poon LLM, Perera RAPM, Alhammadi MA, Ng HY, et al. MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis. 2014;20:1231–1234. PubMed PMC

Kurtz J, Kalbe M, Aeschlimann PB, Häberli MA, Wegner KM, Reusch TBH, et al. Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc B Biol Sci. 2004;271:197–204. PubMed PMC

Uematsu S, Akira S. Toll-like receptors (TLRs) and their ligands. In: Bauer S, Hartmann G, editors. Toll-like receptors (TLRs) and innate immunity. Springer: Berlin Heidelberg; 2008. pp. 1–20.

Gnerre S, Lander ES, Lindblad-toh K, Jaffe DB. Assisted assembly: how to improve a de novo genome assembly by using related species. Genome Biol. 2009;10:R88. PubMed PMC

Almathen F, Charruau P, Mohandesan E, Mwacharo JM, Orozco-terWengel P, Pitt D, et al. Ancient and modern DNA reveal dynamics of domestication and cross-continental dispersal of the dromedary. Proc Natl Acad Sci. 2016;113:6707–6712. doi: 10.1073/pnas.1519508113. PubMed DOI PMC

Yadamsuren A, Dulamtseren E, Reading RP. The conservation status and Management of Wild Camels in Mongolia. In: Knoll E-M, Burger PA, editors. Camels in Asia and North-Africa- interdisciplinary perspectives on their past and present significance. Austrian Academy of Sciences Press: Wien; 2012. pp. 45–54.

Dirie MF, Abdurahman O. Observations on little known diseases of camels (Camelus dromedarius) in the horn of Africa. Rev Sci Tech - Off Int des épizooties. 2003;22:1043–1049. PubMed

Fassi-Fehri MM. Diseases of camels. Rev Sci Tech Off Int des Epizoot. 1987;6:337–354.

Bontrop RE, Otting N, de Groot NG, Gaby G. M D. Major histocompatibility complex class II polymorphisms in primates. Syst Lupus Erythematosus. 1999;167:339–350. PubMed

Bernatchez L, Landry C. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol. 2003;16:363–377. PubMed

Janeway Jr CA, Travers P, Walport M, Shlomchik MJ. The complement system and innate immunity. In: Immunobiology: The Immune System in Health and Disease. 5th editio. New York: Garland Science; 2001.

Ujvari B, Belov K. Major histocompatibility complex (MHC) markers in conservation biology. Int J Mol Sci. 2011;12:5168–5186. PubMed PMC

Elbers JP, Clostio RW, Taylor SS. Neutral genetic processes influence MHC evolution in threatened gopher tortoises (Gopherus polyphemus) J Hered. 2017;108:515–523. PubMed

Ming L, Yi L, Sa R, Wang ZX, Wang Z, Ji R. Genetic diversity and phylogeographic structure of Bactrian camels shown by mitochondrial sequence variations. Anim Genet. 2017;48:217–220. PubMed PMC

Ming L, Yuan L, Yi L, Ding G, Hasi S, Chen G, et al. Whole-genome sequencing of 128 camels across Asia reveals origin and migration of domestic Bactrian camels. Commun Biol. 2020;3:1–9. PubMed PMC

Wells K, Gibson DI, Clark NJ, Ribas A, Morand S, McCallum HI. Global spread of helminth parasites at the human–domestic animal–wildlife interface. Glob Chang Biol. 2018;24:3254–3265. PubMed

Lado S, Elbers JP, Doskocil A, Scaglione D, Trucchi E, Banabazi MH, et al. Genome-wide diversity and global migration patterns in dromedaries follow ancient caravan routes. Commun Biol. 2020;3:1–8. doi: 10.1038/s42003-020-1098-7. PubMed DOI PMC

Richardson MF, Munyard K, Croft LJ, Allnutt TR, Jackling F, Alshanbari F, et al. Chromosome-level alpaca reference genome VicPac3.1 improves genomic insight into the biology of new world camelids. Front Genet. 2019;10:1–15. PubMed PMC

Plasil M, Wijkmark S, Elbers JP, Oppelt J, Burger PA, Horin P. The major histocompatibility complex of Old World camelids: class I and class I-related genes. Hla. 2019;93:203–215. PubMed

Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res. 2009;19:1117–1123. PubMed PMC

Putnam NH, Connell BO, Stites JC, Rice BJ, Blanchette M, Calef R, et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 2016;26:342–350. PubMed PMC

English AC, Richards S, Han Y, Wang M, Vee V, Qu J, et al. Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology. PLoS ONE. 2012;7(11):e47768. PubMed PMC

Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9:e112963. PubMed PMC

Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, et al. ABySS 2.0: resource-efficient assembly of large genomes using a bloom filter effect of bloom filter false positive rate. Genome Res. 2017;27:768–777. PubMed PMC

Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements Daehwan HHS public access. Nat Methods. 2015;12:357–360. PubMed PMC

Alim FZD, Romanova EV, Tay Y-L, Rahman AYBA, Chan KG, Hong KW, et al. Seasonal adaptations of the hypothalamo-neurohypophyseal system of the dromedary camel. PLoS One. 2019;14:1–33. PubMed PMC

Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. Sambamba: fast processing of NGS alignment formats. Bioinformatics. 2015;31:2032–2034. PubMed PMC

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36. PubMed PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188–196. PubMed PMC

Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005;33:6494–6506. PubMed PMC

Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33:290–295. PubMed PMC

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006;34(Web Server Issue):W435–W439. PubMed PMC

Boutet E, Lieberherr D, Tognolli M, Schneider M, Bansal P, Bridge AJ, et al. UniProtKB/Swiss-Prot, the manually annotated section of the UniProt KnowledgeBase: how to use the entry view. Methods Mol Biol. 2016;1374:23–54. doi: 10.1007/978-1-4939-3167-5. PubMed DOI

Campbell MS, Law MY, Holt C, Stein JC, Moghe GD, Hufnagel DE, et al. MAKER-P: a tool kit for the rapid creation, management, and quality control of plant genome annotations. Plant Physiol. 2014;164:513–524. PubMed PMC

Watson M, Warr A. Errors in long-read assemblies can critically affect protein prediction. Nat Biotechnol. 2019;37:124–126. PubMed

Paten B, Earl D, Nguyen N, Diekhans M, Zerbino D, Haussler D. Cactus: algorithms for genome multiple sequence alignment. Genome Res. 2011;21:1512–1528. PubMed PMC

Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462–467. PubMed

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25. PubMed PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. PubMed PMC

Cabanettes F, Klopp C. D-GENIES: Dot plot large genomes in an interactive, efficient and simple way. PeerJ. 2018;2018(6):e4958. PubMed PMC

Kofler R, Orozco-terWengel P, de Maio N, Pandey RV, Nolte V, Futschik A, et al. Popoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One. 2011;6:e15925. PubMed PMC

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio.GN]; 2013.

Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009;25:1754–1760. PubMed PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. PubMed PMC

Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly (Austin) 2012;6:80–92. PubMed PMC

Pedersen BS, Quinlan AR. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics. 2018;34:867–868. PubMed PMC

Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289–300.

Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50:346–363. PubMed

Gremme G, Steinbiss S, Kurtz S. Genome tools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans Comput Biol Bioinforma. 2013;10:645–656. PubMed

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. PubMed PMC

Venables WN, Ripley BD. Modern applied statistics with S. New York: Springer; 2002.

Pinheiro J, Bates D, DebRoy S, Sarkar D. nlme: linear and nonlinear mixed effects models. R package version 3.1–111. 2013.

Elbers JP, Taylor SS. GO2TR: a gene ontology-based workflow to generate target regions for target enrichment experiments. Conserv Genet Resour. 2015;7:851–857.

Bradley RK, Roberts A, Smoot M, et al. Fast statistical alignment. PLoS Comput Biol. 2009;5(5):e1000392. PubMed PMC

Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. MUMmer4: A fast and versatile genome alignment system. PLoS Comput Biol. 2018;14:1–14. PubMed PMC

Paradis E. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26:419–420. PubMed

Canty A, Ripley B. boot: Bootstrap R (S-Plus) Functions. R package version 1.3–24. 2019.

Ciccarese S, Burger PA, Ciani E, Castelli V, Linguiti G, Plasil M, et al. The camel adaptive immune receptors repertoire as a singular example of structural and functional genomics. Front Genet. 2019;10(OCT):1–14. PubMed PMC

Hamer-Casterman C, Atarchouch T, Muyldermans S, Robinson G, Hamers C, Bajyana E, et al. Naturally occurring antibodies devoid of light chains. Nature. 1993;363:446–448. PubMed

Shumate A, Salzberg SL. Liftoff: an accurate gene annotation mapping tool. bioRxiv. 2020;2020.06.24.169680. 10.1101/2020.06.24.169680.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...