Skip to main content
SpringerLink
Log in

Single nucleotide polymorphisms at heat shock protein 90 gene and their association with thermo-tolerance potential in selected indigenous Nigerian cattle

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Heat shock protein (HSP) 90 gene provides protection and adaptation to thermal assault and certain polymorphisms have been associated to heat tolerance in humans and animals. Single nucleotide polymorphisms (SNPs) of HSP 90 gene were used to evaluate the scientific basis of heat tolerance in four zebu breeds of Nigeria. The DNA was extracted from skin tissue of 90 adult bulls representing White Fulani (WF), Sokoto Gudali (SG), Red Bororo (RB), and Ambala (AM). The SNPs were determined in DNAs using PCR, sequencing, and visualization and bio-editing by chromatogram in SeqMan Ngen tool. Subsequently, respective genotypes were constructed and genotypic and allelic frequencies were computed. Also, body parameters related to heat stress (HS) including body temperature (BT), rectal temperature (RT), and respiratory rates (RR) were taken for each animal before biological sampling and heat tolerance coefficient (HTC) was calculated. We detected four SNPs distinct/specific for each breed as follows: change from thymine (T) to guanine (G) at position 116 (T116G) in RB, G to cytosine (C) at 220 (G220C) in SG, G to adenine (A) at two positions, 346 (G346A) and 390 (G390A) in AM and WF, respectively. Heterozygous SNPs showed significantly lower values (P < 0.0001) for BT, RT, RR, and HTC than homozygous genotypes at all positions. We hypothesize that animals with heterozygous SNPs in exon 3 of HSP 90 may be tolerant to HS. These SNPs can be used as bio-markers for screening large populations of cattle for tolerance to hot tropical conditions in Nigeria and other sub-humid places.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alphonsus C, Akpa GN, Barje PP, Finangwai HI, Adamu BD (2012) Comparative evaluation of linear udder and body conformation traits of Bunaji and Friesian x Bunaji cows. World J Life Sci Med Res 2:134–140.

    Google Scholar 

  • Babayemi OJ, Abu OA, Opakunbi A (2014) Integrated animal husbandry for schools and colleges, First edition. Positive Press, Ibadan, Nigeria. pp 20–122.

    Google Scholar 

  • Basirico L, Morera P, Primi V, Lacetera N, Nardone A, Bernabucci U (2011) Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperon 16:441–448.

    Article  CAS  Google Scholar 

  • Benezra MV (1954) A new index for measuring the adaptability of cattle to tropical conditions. J Anim Sci 43:505.

    Google Scholar 

  • Blackshaw JK, Blackshaw AW (1994) Heat stress in cattle and the effect of shade on production and behaviour. Aust J Exp Agric 34:285–295.

    Article  Google Scholar 

  • Blench RM, De Jode A, Gherzi E, Di Domenico C (1998) Keteku and Ndama crossbred cattle in Nigeria: History, distribution and productivity. In C. Seignobos and E. Thys Paris (Ed.) Des Taurins au Cameroun et Nigeria. ORSTOM/IEMVT, Maisons-Alfort. 293–310.

    Google Scholar 

  • Charoensook R, Gatphayak K, Sharifi AR, Chaisongkram C, Brenig B, Knorr C (2012) Polymorphisms in the bovine HSP90AB1 gene are associated with heat tolerance in Thai indigenous cattle. Trop Anim Health Prod 44:921–928.

    Article  Google Scholar 

  • Chenyambuga SW, Ngowi EE, Gwakisa PS, Mbaga SH (2008) Phenotypic description and productive performance of Tarime Zebu Cattle in Tanzania. Tanzania Vet J 25:60–74.

    Article  Google Scholar 

  • de Clare Bronsvoort BM, Thumbi SM, Poole EJ, Kiara H, Auguet OT, Handel IG, Jennings A, Conradie I, Mbole-Kairuki MN, Toye PG, Hannote O, Coetzer JA, Woolhouse ME (2013) Design and descriptive epidemiology of the Infectious Diseases of East African Livestock (IDEAL) project, a longitudinal calf cohort study in western Kenya. BMC Vet Res 9:171 Doi: https://doi.org/10.1186/1746-6148-9-171.

    Article  PubMed  PubMed Central  Google Scholar 

  • Christine JA, Leila C, Matthew S (2016) Quantifying the role of burn temperature, burn duration and skin thickness in an in vivo animal skin model of heat conduction. Int J Heat Mass Transf 101:542–549.

    Article  Google Scholar 

  • Edea Z, Dadi H, Kim SW, Dessie T, Kim K (2012) Comparison of SNP variation and distribution in indigenous Ethiopian and Korean cattle (Hanwoo) populations. Genomics Inform 10:200–205. doi: https://doi.org/10.5808/GI.2012.10.3.200.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gwakisa PS, Kemp SJ, Teale AJ (1994) Characterization of Zebu cattle breeds in Tanzania using random amplified polymorphic DNA markers. Anim Genet 25:89–94.

    Article  CAS  Google Scholar 

  • Hansen PJ (2004) Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci 82–83:349–360.

    Article  Google Scholar 

  • Kapila N, Kishore A, Sodhi M, Sharma A, Mohanty B, Kumar P, Mukesh M (2013). Temporal changes in mRNA expression of heat shock protein genes in mammary epithelial cells of riverine buffalo in response to heat stress in vitro. Int J Anim Biotechnol 3:5–9.

    Google Scholar 

  • Katie T, Alistair F (1986) The complete book of raising livestock and poultry—A small holder’s guide (University Services Ltd., Yaba Lagos, Nigeria).

    Google Scholar 

  • Kerekoppa RP, Rao A, Basavaraju M, Geetha GR, Krishnamurthy L, Thta VL, Rao N, Das DN, Mukund K (2015) Molecular characterization of the HSPA1A gene by single-strand conformation polymorphism and sequence analysis in Holstein-Friesian crossbred and Deoni cattle raised in India. Turk J Vet Anim Sci 39:128–133.

    Article  CAS  Google Scholar 

  • Kim J, Hanotte O, Mwai OA, Dessie T, Bashir S, Diallo B, Agaba M, Kim K, Kwak W, Sung S, Seo M, Jeong H, Kwon T, Taye M, Song KD, Lim D, Cho S, Lee HJ, Yoon D, Oh SJ, Kemp S, Lee HK, Kim H (2017) The genome landscape of indigenous African cattle. Genome Biol 18(1), 34. doi:https://doi.org/10.1186/s13059-017-1153-y.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kishore A, Sodhi M, Khate K, Kapila N, Kumari P, Mukesh M (2013) Selection of stable reference genes in heat stressed peripheral blood mononuclear cells of tropically adapted Indian cattle and buffaloes. Mol Cell Probe 27(3–4):140–144.

    Article  CAS  Google Scholar 

  • Kubkomawa HI (2017) Indigenous Breeds of Cattle, their Productivity, Economic and Cultural Values in Sub-Saharan Africa. Int J Res Studies in Agric Sci 3:27–43.

    Google Scholar 

  • Kumar R, Gupta ID, Verma A, Verma N, Vineeth MR (2015) Genetic polymorphisms within exon 3 of heat shock protein 90AA1 gene and its association with heat tolerance traits in Sahiwal cows. Vet World 8:932–936. doi: https://doi.org/10.14202/vetworld.2015.932-936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laisser ELK, Kipanyula MJ, Msalya G, Mdegela RH, Karimuribo ED, Mwilawa AJ, Mwega ED, Kusiluka L, Chenyambuga SW. 2014. Tick burden and prevalence of Theileria parva infection in Tarime zebu cattle in the lake zone of Tanzania. Trop Anim Health Prod 46:1391–1396.

    Article  Google Scholar 

  • Lamb M, Okimoto R, Brown M, Brown H Jr, Johnson Z, Rosenkrans C Jr (2007a) Relationship between single nucleotide polymorphisms in the bovine heat shock protein 70 gene and milk characteristics of beef cows. J Anim Sci 85(2):4.

    Google Scholar 

  • Lamb M, Okimoto R, Broun M, Rosenkranes C Jr (2007b) Associations between cattle breed and heat shock protein 70 gene. Res Ser 545:205–206.

    Google Scholar 

  • Latif AA, Pegram RG (1992) Naturally acquired host resistance in tick control in Africa. Insect Sci Appl 13:505–513.

    Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191.

    Article  CAS  Google Scholar 

  • Marcos-Carcavilla A, Mutikainen M, González C, Jorge HC, Kantanen J, Sanz A, Nurbiy SM, Pérez-Guzmán MD, Serrano M (2010) A SNP in the HSP90AA1 gene 5′ flanking region is associated with the adaptation to differential thermal conditions in the ovine species. Cell Stress Chaperones 15:67–81.

    Article  CAS  Google Scholar 

  • Maule JP (1990) The cattle of the tropics. In: Maule JP (ed.) The cattle of the tropics. Red Wood Press, Melksham. pp 11–22.

    Google Scholar 

  • Mattioli RC, Pandey VS, Murray M, Fitzpatrick JL (2000) Immunogenetic influences on tick resistance in African cattle with reference to trypanotolerant N’Dama (Bos taurus) and trypanosusceptible Gobra zebu (Bos indicus) cattle. Acta Trop 75:263–277.

    Article  CAS  Google Scholar 

  • Meghen C, MacHugh DE, Sauveroche B, Kana G, Bradley DG (1999) Characterization of the Kuri Cattle of Lake Chad using Molecular Genetic Techniques. In Blench RM, MacDonald KC (Ed.) The origin and development of African livestock. University College Press, London, pp. 28–86.

    Google Scholar 

  • Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259 (5100): 1409–10. doi:https://doi.org/10.1126/science.8451637. PMID 8451637

  • Msalya G, Kim ES, Laisser ELK, Kipanyula MJ, Karimuribo ED, Kusiluka LJM, Chenyambuga SW, Rothschild MF. 2017. Determination of Genetic Structure and Signatures of Selection in Three Strains of Tanzania Shorthorn Zebu, Boran and Friesian Cattle by Genome-Wide SNP Analyses. PLoS ONE 12(1): e0171088 DOI https://doi.org/10.1371/journal.pone.0171088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muralidhar M, Sriramana K, Narasimharao G, Javaregowda N (2004) Genetic characterization of the Indian cattle breeds, Ongole and Deoni (Bos indicus), using microsatellite markers—a preliminary study. Genetics 5:16.

    Google Scholar 

  • NNLRS (1999) Nigerian National Livestock Resource Survey. pp. 627-649.

  • Onasanya GO, Ikeobi CO, Ayotunde AS, Oke FO, Olorunisola RA, Decampos JS (2017) Thermo-Regulatory Functions of Heat Shock Protein Genes in Some Selected Tropically Stressed Livestock Animals. Int J Appl Res Technol 6:37–43.

    Google Scholar 

  • Öner Y, Keskin A, Üstüner H, Soysal D, Karakaş V (2017) Genetic diversity of the 3′ and 5′ untranslated regions of the HSP70.1 gene between native Turkish and Holstein Friesian cattle breeds. S Afr J Anim Sci 47:425–439.

    Article  Google Scholar 

  • Pagot J (1992) Animal Production in the tropics and subtropics (Translated by Wilding J). The MacMillan Press Ltd, London and Basingstoke. pp. 351–358

  • Porter V (1991) In: Cattle—A Handbook to the Breeds of the World. Christopher Helm, London. pp. 186–221.

    Google Scholar 

  • Rosenkrans C Jr, Banks A, Reiter S, Looper M (2010) Calving traits of crossbred Brahman cows are associated with Heat Shock Protein 70 genetic polymorphisms. Anim Rep Sci 119:178–182.

    Article  CAS  Google Scholar 

  • Sajjanar B, Deb R, Singh U, Kumar S, Brahmane M, Nirmale A, Kumar S, Minhas P (2015) Identification of SNP in HSP90AB1 and its association with the relative thermo tolerance and milk production traits in Indian dairy cattle. Anim Biotechnol 26:921–928.

    Article  Google Scholar 

  • Sodhi M, Mukesh M, Kishore A, Mishra BP, Joshi BK (2013). Novel polymorphisms in UTR and coding region of inducible heat shock protein 70.1 gene in tropically adapted Indian zebu cattle (Bos indicus) and riverine buffalo (Bubalus bubalis). Gene 527:606–615.

    Article  CAS  Google Scholar 

  • West JW (2003) Effects of heat stress in dairy cattle. J Dairy Sci 86:2131–2144.

    Article  CAS  Google Scholar 

  • Western D, Finch V (1986) Cattle and pastoralism: Survival and production in arid lands. Hum Ecol 14:77–94.

    Article  Google Scholar 

  • Williamson G, Payne WJA (1990) An introduction to animal husbandry in the tropics. Longman Group, London. pp. 125.

    Google Scholar 

  • Wilkerson DC, Sarge KD (2009) RNA polymerase II interacts with the Hspa1b promoter in mouse epididymal spermatozoa. Reproduction 137:923–929.

    Article  CAS  Google Scholar 

  • Yakubu A, Yahaya A, Omeje JN (2015) Heat tolerance traits and tick infestation in some indigenous breeds of cattle in Nigeria. Slovak J Anim Sci 48:79–85.

    Google Scholar 

Download references

Acknowledgments

We thank the management of slaughter houses in Nigeria for giving us permission to sample from the animals in their custodian.

Funding

The Government of India funded the main analyses of this study in a form of visiting scholarships through the Research Fellowship for Developing Countries Scientists (RFD-CS) to GOO and CV Raman International Fellowship for African Researchers for GMM. Both programs are administered by the Department of Science and Technology (DST) and Ministry of External Affairs (MEA) of the Government of India, New Delhi.

Author information

Authors and Affiliations

  1. Department of Animal Science, Federal University Dutse, Dutse, Nigeria

    Gbolabo O. Onasanya

  2. Deparment of Animal Breeding and Genetics, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria

    Gbolabo O. Onasanya, Timothy M. Sanni, Olajide Olowofeso & Christian O. Ikeobi

  3. Mecheri Sheep Research Station, Pottaneri, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India

    Gbolabo O. Onasanya, George M. Msalya & Aranganoor K. Thiruvenkadan

  4. Biotechnology Center, Postgraduate Research Institute in Animal Sciences, Kattupakkum, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India

    Gbolabo O. Onasanya & Chirukandoth Sreekumar

  5. Department of Animal, Aquaculture and Range Sciences (DAARS), Sokoine University of Agriculture (SUA), PO Box 3004, Morogoro, Tanzania

    George M. Msalya

  6. Department of Animal Biotechnology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India

    Gopalan K. Tirumurugaan

  7. Department of Animal Production, University of Ilorin, Ilorin, Kwara State, Nigeria

    John S. Decampos

  8. Department of Animal production, Federal College of Animal Health and Production Technology, Moor Plantation, Ibadan, Nigeria

    Samuel A. Amusan

  9. Department of Animal Nutrition, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria

    Adeboye O. Fafiolu

  10. Department of Genetics, School of Life Sciences, University of KwaZulu-Natal, Westvile Campus, Durban, South Africa

    Moses Okpeku

  11. Department of Animal Science, Faculty of Agriculture, Nasarawa State University, Keffi, Shabu-Lafia Campus, Lafia, Nigeria

    Abdulmojeed Yakubu

Authors
  1. Gbolabo O. Onasanya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. George M. Msalya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aranganoor K. Thiruvenkadan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chirukandoth Sreekumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gopalan K. Tirumurugaan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Timothy M. Sanni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John S. Decampos
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Samuel A. Amusan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Olajide Olowofeso
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Adeboye O. Fafiolu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Moses Okpeku
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Abdulmojeed Yakubu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Christian O. Ikeobi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualized and designed the experiments: GOO, COI, AOF, OO, AKT, CS; contributed reagents: AKT, CS, GKT; performed the experiments: GOO, GMM, CS; carried out the analysis: GOO, GMM, CS; did the statistical analyses: GOO; drafted the manuscript: GOO, GMM; structured scientific content: GOO, GMM, CS, TMS, OO, AY; all authors provided editorial suggestions and revisions, and read and approved the final draft: GOO, GMM, AKT, CS, GKT, TMS, JSD, ASA, OO, AOF, MO, AY, COI.

Corresponding author

Correspondence to George M. Msalya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Declaration

We declare to the Editor of the Biochemical Genetics that this is our original work and has not been submitted for publication elsewhere. Animal welfare was not compromised anytime during this study and all of our research protocols were cleared by the responsible institutions both in Nigeria and India prior to embarking on the various activities reported here.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onasanya, G.O., Msalya, G.M., Thiruvenkadan, A.K. et al. Single nucleotide polymorphisms at heat shock protein 90 gene and their association with thermo-tolerance potential in selected indigenous Nigerian cattle. Trop Anim Health Prod 52, 1961–1970 (2020). https://doi.org/10.1007/s11250-020-02222-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-020-02222-9

Keywords

Search

Navigation