Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Young, B.A. Cold stress as it affects animal production. J. Anim. Sci. 1981, 52, 154–163. [Google Scholar] [CrossRef]
- Okumura, J.; Mori, N.; Muramatsu, T.; Tasaki, I.; Saito, F. Analysis of factors affecting year-round performance of single comb white leghorn laying hens reared under an open-sided housing system. Poult. Sci. 1988, 67, 1130–1138. [Google Scholar] [CrossRef] [PubMed]
- Piao, M.Y.; Baik, M. Seasonal variation in carcass characteristics of korean cattle steers. Asian-Australas. J. Anim. Sci. 2015, 28, 442–450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghasemi, E.; Azad-Shahraki, M.; Khorvash, M. Effect of different fat supplements on performance of dairy calves during cold season. J. Dairy Sci. 2017, 100, 5319–5328. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.J.; Piao, M.Y.; Park, S.J.; Na, S.W.; Kim, H.J.; Baik, M. Effects of ambient temperature and rumen-protected fat supplementation on growth performance, rumen fermentation and blood parameters during cold season in Korean cattle steers. Asian-Australas. J. Anim. Sci. 2019, 32, 657–664. [Google Scholar] [CrossRef]
- Weldenegodguad, M.; Popov, R.; Pokharel, K.; Ammosov, I.; Ming, Y.; Ivanova, Z.; Kantanen, J. Whole-genome sequencing of three native cattle breeds originating from the northernmost cattle farming regions. Front. Genet. 2018, 9, 728. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Banerjee, D.; Upadhyay, R.C.; Chaudhary, U.B.; Kumar, R.; Singh, S.; Ashutosh; Mohanarao, G.J.; Polley, S.; Mukherjee, A.; Das, T.K.; et al. Seasonal variation in expression pattern of genes under hsp70 : Seasonal variation in expression pattern of genes under HSP70 Family in heat and cold-adapted goats (Capra hircus). Cell Stress Chaperones 2014, 19, 401–408. [Google Scholar] [CrossRef] [Green Version]
- Gan, M.; Shen, L.; Fan, Y.; Guo, Z.; Liu, B.; Chen, L.; Tang, G.; Jiang, Y.; Li, X.; Zhang, S.; et al. High altitude adaptability and meat quality in Tibetan pigs: A reference for local pork processing and genetic improvement. Animals 2019, 9, 1080. [Google Scholar] [CrossRef] [Green Version]
- Librado, P.; Der Sarkissian, C.; Ermini, L.; Schubert, M.; Jónsson, H.; Albrechtsen, A.; Fumagalli, M.; Yang, M.A.; Gamba, C.; Seguin-Orlando, A.; et al. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proc. Natl. Acad. Sci. USA 2015, 112, E6889–E6897. [Google Scholar] [CrossRef] [Green Version]
- Xie, S.; Yang, X.; Gao, Y.; Jiao, W.; Li, X.; Li, Y.; Ning, Z. Performance differences of Rhode Island Red, Bashang Long-Tail chicken, and their reciprocal crossbreds under natural cold stress. Asian-Australas. J. Anim. Sci. 2017, 30, 1507–1514. [Google Scholar] [CrossRef] [Green Version]
- Kudinov, A.A.; Dementieva, N.V.; Mitrofanova, O.V.; Stanishevskaya, O.I.; Fedorova, E.S.; Larkina, T.A.; Mishina, A.I.; Plemyashov, K.V.; Griffin, D.K.; Romanov, M.N. Genome-wide association studies targeting the yield of extraembryonic fluid and production traits in Russian white chickens. BMC Genom. 2019, 20, 270. [Google Scholar] [CrossRef] [PubMed]
- Phillips, C.J.C. Principles of Cattle Production, 3rd ed.; CABI Wallingford: Oxfordshire, UK, 2018. [Google Scholar]
- Howard, J.T.; Kachman, S.D.; Snelling, W.M.; Pollak, E.J.; Ciobanu, D.C.; Kuehn, L.A.; Spangler, M.L. Beef cattle body temperature during climatic stress: A genome-wide association study. Int. J. Biometeorol. 2014, 58, 1665–1672. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yurchenko, A.A.; Daetwyler, H.D.; Yudin, N.; Schnabel, R.D.; Vander Jagt, C.J.; Soloshenko, V.; Lhasaranov, B.; Popov, R.; Taylor, J.F.; Larkin, D.M. Scans for signatures of selection in Russian cattle breed genomes reveal new candidate genes for environmental adaptation and acclimation. Sci. Rep. 2018, 8, 12984. [Google Scholar] [CrossRef] [Green Version]
- Buggiotti, L.; Yurchenko, A.A.; Yudin, N.S.; Vander Jagt, C.J.; Vorobieva, N.V.; Kusliy, M.A.; Vasiliev, S.K.; Rodionov, A.N.; Boronetskaya, O.I.; Zinovieva, N.A.; et al. Demographic history, adaptation, and NRAP convergent evolution at amino acid residue 100 in the world northernmost cattle from Siberia. Mol. Biol. Evol. 2021. [Google Scholar] [CrossRef]
- Xu, Q.; Wang, Y.C.; Liu, R.; Brito, L.F.; Kang, L.; Yu, Y.; Wang, D.S.; Wu, H.J.; Liu, A. Differential gene expression in the peripheral blood of Chinese Sanhe cattle exposed to severe cold stress. Genet. Mol. Res. 2017, 16, gmr16029593. [Google Scholar] [CrossRef]
- Cao, K.X.; Hao, D.; Wang, J.; Peng, W.W.; Yan, Y.J.; Cao, H.X.; Sun, F.; Chen, H. Cold exposure induces the acquisition of brown adipocyte gene expression profiles in cattle inguinal fat normalized with a new set of reference genes for QRT-PCR. Res. Vet. Sci. 2017, 114, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Pokharel, K.; Weldenegodguad, M.; Popov, R.; Honkatukia, M.; Huuki, H.; Lindeberg, H.; Peippo, J.; Reilas, T.; Zarovnyaev, S.; Kantanen, J. Whole blood transcriptome analysis reveals footprints of cattle adaptation to sub-arctic conditions. Anim. Genet. 2019, 50, 217–227. [Google Scholar] [CrossRef] [Green Version]
- Igoshin, A.V.; Yurchenko, A.A.; Belonogova, N.M.; Petrovsky, D.V.; Aitnazarov, R.B.; Soloshenko, V.A.; Yudin, N.S.; Larkin, D.M. Genome-wide association study and scan for signatures of selection point to candidate genes for body temperature maintenance under the cold stress in Siberian cattle populations. BMC Genet. 2019, 20, 5–14. [Google Scholar] [CrossRef]
- Cheruiyot, E.K.; Haile-Mariam, M.; Cocks, B.G.; MacLeod, I.M.; Xiang, R.; Pryce, J.E. New loci and neuronal pathways for resilience to heat stress in cattle. Sci. Rep. 2021, 11, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Hu, Z.-L.; Park, C.A.; Reecy, J.M. Building a livestock genetic and genomic information knowledgebase through integrative developments of animal QTLdb and CorrDB. Nucleic Acids Res. 2019, 47, D701–D710. [Google Scholar] [CrossRef] [Green Version]
- Xiang, R.; van den Berg, I.; MacLeod, I.M.; Hayes, B.J.; Prowse-Wilkins, C.P.; Wang, M.; Bolormaa, S.; Liu, Z.; Rochfort, S.J.; Reich, C.M.; et al. Quantifying the contribution of sequence variants with regulatory and evolutionary significance to 34 bovine complex traits. Proc. Natl. Acad. Sci. USA 2019, 116, 19398–19408. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- DePristo, M.A.; Banks, E.; Poplin, R.; Garimella, K.V.; Maguire, J.R.; Hartl, C.; Philippakis, A.A.; del Angel, G.; Rivas, M.A.; Hanna, M.; et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 2011, 43, 491–498. [Google Scholar] [CrossRef]
- Weir, B.S.; Cockerham, C.C. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38, 1358–1370. [Google Scholar] [CrossRef] [PubMed]
- Danecek, P.; Auton, A.; Abecasis, G.; Albers, C.A.; Banks, E.; DePristo, M.A.; Handsaker, R.E.; Lunter, G.; Marth, G.T.; Sherry, S.T.; et al. The variant call format and VCFtools. Bioinformatics 2011, 27, 2156–2158. [Google Scholar] [CrossRef]
- Grant, J.R.; Arantes, A.S.; Liao, X.; Stothard, P. In-depth annotation of SNPs arising from resequencing projects using NGS-SNP. Bioinformatics 2011, 27, 2300–2301. [Google Scholar] [CrossRef] [Green Version]
- Hinrichs, A.S.; Raney, B.J.; Speir, M.L.; Rhead, B.; Casper, J.; Karolchik, D.; Kuhn, R.M.; Rosenbloom, K.R.; Zweig, A.S.; Haussler, D.; et al. UCSC data integrator and variant annotation integrator. Bioinformatics 2016, 32, 1430–1432. [Google Scholar] [CrossRef] [Green Version]
- Verma, P.; Sharma, A.; Sodhi, M.; Thakur, K.; Kataria, R.S.; Niranjan, S.K.; Bharti, V.K.; Kumar, P.; Giri, A.; Kalia, S.; et al. Transcriptome analysis of circulating PBMCs to understand mechanism of high altitude adaptation in native cattle of Ladakh region. Sci. Rep. 2018, 8, 7681. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Long, Y.; Li, X.; Li, F.; Ge, G.; Liu, R.; Song, G.; Li, Q.; Qiao, Z.; Cui, Z. Transcriptional programs underlying cold acclimation of common carp (Cyprinus carpio L.). Front. Genet. 2020, 11, 556418. [Google Scholar] [CrossRef]
- Pitt, D.; Bruford, M.W.; Barbato, M.; Orozco-terWengel, P.; Martínez, R.; Sevane, N. Demography and rapid local adaptation shape Creole cattle genome diversity in the tropics. Evol. Appl. 2019, 12, 105–122. [Google Scholar] [CrossRef]
- Coppe, A.; Agostini, C.; Marino, I.A.M.; Zane, L.; Bargelloni, L.; Bortoluzzi, S.; Patarnello, T. Genome evolution in the cold: Antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function. Genome Biol. Evol. 2013, 5, 45–60. [Google Scholar] [CrossRef] [Green Version]
- Bhardwaj, S.; Singh, S.; Ganguly, I.; Bhatia, A.K.; Bharti, V.K.; Dixit, S.P. Genome-wide diversity analysis for signatures of selection of Bos indicus adaptability under extreme agro-climatic conditions of temperate and tropical ecosystems. Anim. Gene 2021, 20, 200115. [Google Scholar] [CrossRef]
- Lin, J.; Cao, C.; Tao, C.; Ye, R.; Dong, M.; Zheng, Q.; Wang, C.; Jiang, X.; Qin, G.; Yan, C.; et al. Cold adaptation in pigs depends on UCP3 in beige adipocytes. J. Mol. Cell Biol. 2017, 9, 364–375. [Google Scholar] [CrossRef]
- Tavares, E.; Miñano, F.J. RANTES: A new prostaglandin dependent endogenous pyrogen in the rat. Neuropharmacology 2000, 39, 2505–2513. [Google Scholar] [CrossRef]
- Liu, P.; Guo, L.; Mao, H.; Gu, Z. Serum proteomics analysis reveals the thermal fitness of crossbred dairy buffalo to chronic heat stress. J. Therm. Biol. 2020, 89, 102547. [Google Scholar] [CrossRef]
- Freitas, P.H.F.; Wang, Y.; Yan, P.; Oliveira, H.R.; Schenkel, F.S.; Zhang, Y.; Xu, Q.; Brito, L.F. Genetic diversity and signatures of selection for thermal stress in cattle and other two Bos species adapted to divergent climatic conditions. Front. Genet. 2021, 12, 604823. [Google Scholar] [CrossRef]
- Shore, A.M.; Karamitri, A.; Kemp, P.; Speakman, J.R.; Graham, N.S.; Lomax, M.A. Cold-induced changes in gene expression in brown adipose tissue, white adipose tissue and liver. PLoS ONE 2013, 8, e68933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Srikanth, K.; Kwon, A.; Lee, E.; Chung, H. Characterization of genes and pathways that respond to heat stress in Holstein calves through transcriptome analysis. Cell Stress Chaperones 2017, 22, 29–42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rim, J.S.; Kozak, L.P. Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene. J. Biol. Chem. 2002, 277, 34589–34600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eslamizad, M.; Albrecht, D.; Kuhla, B. The effect of chronic, mild heat stress on metabolic changes of nutrition and adaptations in rumen papillae of lactating dairy cows. J. Dairy Sci. 2020, 103, 8601–8614. [Google Scholar] [CrossRef] [PubMed]
- Mottillo, E.P.; Desjardins, E.M.; Crane, J.D.; Smith, B.K.; Green, A.E.; Ducommun, S.; Henriksen, T.I.; Rebalka, I.A.; Razi, A.; Sakamoto, K.; et al. Lack of adipocyte AMPK exacerbates insulin resistance and hepatic steatosis through brown and beige adipose tissue function. Cell Metab. 2016, 24, 118–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, A.K.; Upadhyay, R.C.; Chandra, G.; Kumar, S.; Malakar, D.; Singh, S.V.; Singh, M.K. Genome-wide expression analysis of the heat stress response in dermal fibroblasts of Tharparkar (Zebu) and Karan-Fries (Zebu × Taurine) cattle. Cell Stress Chaperones 2020, 25, 327–344. [Google Scholar] [CrossRef] [PubMed]
- Khaibullina, A.; Kenyon, N.; Guptill, V.; Quezado, M.M.; Wang, L.; Koziol, D.; Wesley, R.; Moya, P.R.; Zhang, Z.; Saha, A.; et al. In a model of batten disease, palmitoyl protein thioesterase-1 deficiency is associated with brown adipose tissue and thermoregulation abnormalities. PLoS ONE 2012, 7, e48733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walsh, I.M.; Bowman, M.A.; Soto Santarriaga, I.F.; Rodriguez, A.; Clark, P.L. Synonymous codon substitutions perturb cotranslational protein folding in vivo and impair cell fitness. Proc. Natl. Acad. Sci. USA 2020, 117, 3528–3534. [Google Scholar] [CrossRef]
- Tang, X.; Miao, Y.; Luo, Y.; Sriram, K.; Qi, Z.; Lin, F.-M.; Gu, Y.; Lai, C.-H.; Hsu, C.-Y.; Peterson, K.L.; et al. Suppression of endothelial AGO1 promotes adipose tissue browning and improves metabolic dysfunction. Circulation 2020, 142, 365–379. [Google Scholar] [CrossRef]
- Wu, J.; Cohen, P.; Spiegelman, B.M. Adaptive thermogenesis in adipocytes: Is beige the new brown? Genes Dev. 2013, 27, 234–250. [Google Scholar] [CrossRef] [Green Version]
- Swain, L.L.; Mishra, C.; Sahoo, S.S.; Nayak, G.; Pradhan, S.K.; Mishra, S.R.; Dige, M. An in vivo and in silico analysis of novel variation in TMBIM6 gene affecting cardiopulmonary traits of Indian goats. J. Therm. Biol. 2020, 88, 102491. [Google Scholar] [CrossRef]
- Weldenegodguad, M.; Pokharel, K.; Niiranen, L.; Soppela, P.; Ammosov, I.; Honkatukia, M.; Lindeberg, H.; Peippo, J.; Reilas, T.; Mazzullo, N.; et al. Adipose gene expression profiles reveal novel insights into the adaptation of northern Eurasian semi-domestic reindeer (Rangifer tarandus). bioRxiv 2021. [Google Scholar] [CrossRef]
- Worthmann, A.; John, C.; Rühlemann, M.C.; Baguhl, M.; Heinsen, F.-A.; Schaltenberg, N.; Heine, M.; Schlein, C.; Evangelakos, I.; Mineo, C.; et al. Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat. Med. 2017, 23, 839–849. [Google Scholar] [CrossRef]
- Pereira-da-Silva, M.; Torsoni, M.A.; Nourani, H.V.; Augusto, V.D.; Souza, C.T.; Gasparetti, A.L.; Carvalheira, J.B.; Ventrucci, G.; Marcondes, M.C.C.G.; Cruz-Neto, A.P.; et al. Hypothalamic melanin-concentrating hormone is induced by cold exposure and participates in the control of energy expenditure in rats. Endocrinology 2003, 144, 4831–4840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sambeat, A.; Gulyaeva, O.; Dempersmier, J.; Sul, H.S. Epigenetic regulation of the thermogenic adipose program. Trends Endocrinol. Metab. 2017, 28, 19–31. [Google Scholar] [CrossRef] [Green Version]
- Gracey, A.Y.; Fraser, E.J.; Li, W.; Fang, Y.; Taylor, R.R.; Rogers, J.; Brass, A.; Cossins, A.R. Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 2004, 101, 16970–16975. [Google Scholar] [CrossRef] [Green Version]
- Yudin, N.S.; Larkin, D.M.; Ignatieva, E.V. A compendium and functional characterization of mammalian genes involved in adaptation to Arctic or Antarctic environments. BMC Genet. 2017, 18, 111. [Google Scholar] [CrossRef] [Green Version]
- Hancock, A.M.; Witonsky, D.B.; Gordon, A.S.; Eshel, G.; Pritchard, J.K.; Coop, G.; Di Rienzo, A. Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet. 2008, 4, e32. [Google Scholar] [CrossRef]
Gene | SNP Position (UMD3.1), (RefSNP) | Reference/Alternate Allele | Sum of Ranks | Reference Allele Frequency | Functional Class | Literature Evidence | |
---|---|---|---|---|---|---|---|
Cold-Sensitive Group | Cold-Tolerant Group | ||||||
DDX23 | Chr5:31,112,894 (rs108955444) | C/T | 0.002 | 0.08 | 0.80 | synonymous variant | Climate adaptation in cattle [29], cold adaptation in common carp [30] |
MAATS1 | Chr1:65,062,344 (rs43234266) | T/C | 0.01 | 1.00 | 0.13 | synonymous variant | Adaptation of cattle to tropical climates [31] |
GRIA4 | Chr15:2,312,905 (rs207668622) | C/A | 0.01 | 1.00 | 0.30 | intron variant | Cold [19] and heat [20] adaptations in cattle |
COX17 | Chr1:65,031,883 (rs208045948) | C/T | 0.02 | 1.00 | 0.50 | missense variant | Adaptation of cattle to tropical climates [31], cold adaptation in Antarctic icefish [32] |
THBS1 | Chr10:35,315,375 (rs43707861) | A/G | 0.02 | 0.33 | 0.92 | missense variant | Cold [18] and heat [33] adaptations in cattle, cold adaptation in pigs [34] |
Chr10:35,320,988 (rs17870352) | A/G | 0.02 | 0.33 | 0.90 | missense variant | ||
CCL5 | Chr19:14,825,116 (rs208398974) | C/T | 0.02 | 0.25 | 1.00 | synonymous variant | Cold adaptation in cattle [18], thermoregulation in rats [35] |
UPK1B | Chr1:64,592,185 (rs43652277) | A/G | 0.02 | 0.10 | 0.63 | missense variant | Adaptation of cattle to tropical climates [31] |
PLA1A | Chr1:64,966,636 (rs43233262) | C/A | 0.03 | 0.00 | 0.83 | intron variant | Adaptation of buffaloes to heat stress [36] |
NR1I2 | Chr1:65,236,459 (rs43235975) | T/C | 0.04 | 0.00 | 0.42 | synonymous variant | Adaptation of cattle to heat stress [31,37], cold stress response in mice [38] |
ATF1 | Chr5:29,271,337 (rs210280224) | A/G | 0.06 | 0.00 | 0.63 | downstream gene variant | Adaptation of cattle to heat stress [39], regulation of brown adipose tissue thermogenesis in mammals [40] |
PRKAG1 | Chr5:30,981,551 (rs29002398) | T/C | 0.06 | 0.08 | 0.83 | 3′-UTR variant | Adaptation of cattle to heat stress [41], regulation of brown adipose tissue thermogenesis in mammals [42] |
IFNGR1 | Chr9:76,093,074 (rs41569368) | T/G | 0.06 | 0.83 | 0.33 | synonymous variant | Cold adaptation in cattle [18] |
PPT1 | Chr3:106,629,521 (rs42791314) | T/C | 0.07 | 0.30 | 0.88 | missense variant | Heat adaptation in cattle [43], thermoregulation in mice [44] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Igoshin, A.; Yudin, N.; Aitnazarov, R.; Yurchenko, A.A.; Larkin, D.M. Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations. Life 2021, 11, 959. https://doi.org/10.3390/life11090959
Igoshin A, Yudin N, Aitnazarov R, Yurchenko AA, Larkin DM. Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations. Life. 2021; 11(9):959. https://doi.org/10.3390/life11090959
Chicago/Turabian StyleIgoshin, Alexander, Nikolay Yudin, Ruslan Aitnazarov, Andrey A. Yurchenko, and Denis M. Larkin. 2021. "Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations" Life 11, no. 9: 959. https://doi.org/10.3390/life11090959