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HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye

Year 2024, Volume: 37 Issue: 1, 51 - 55, 17.04.2024
https://doi.org/10.29136/mediterranean.1408404

Abstract

Global warming is becoming a greater threat for the agricultural sector, while molecular genetics studies still hold new opportunities, to not only detect heat-tolerant animals, but also to allow for increasing the frequencies of desired genotypes in a certain population. In this study, HSP90AB1 gene associated with heat tolerance was investigated in four cattle breeds known as Zavot (ZAV), Sout Anatolian Yellow (SAY), South Anatolian Red (SAR), and Brown Swiss (BS) reared in Türkiye via Allele-Specific Polymerase Chain Reaction (AS-PCR). 4338T>C mutation of the HSP90AB1 gene yielded a total of three genotypes (CC, CT, and TT) across all cattle breeds in which C allele frequency ranged from 0.34 (SAY) to 0.73 (BS), while T allele frequency varied between 0.27 (BS) and 0.66 (SAY). In BS, CC was the genotype with the highest frequency (0.50), whereas the frequency of CC was lower than CT and TT in the Anatolian breed (ZAV, SAR, and SAY). Similarly, the frequency of TT was higher in native Anatolian breeds than BS (0.05). All the populations studied were in Hardy-Weinberg Equilibrium (HWE) in terms of the HSP90AB1 gene. This study confirmed that the HSP90AB1 gene was polymorphic in four cattle breeds reared in Türkiye. This polymorphism has the potential to allow for improving heat tolerance to maintain animal production in the future via suitable selection studies. Therefore, this polymorphism should be conserved in Anatolian cattle breeds, while other genes related to different environmental stressors may be monitored by further studies.

Ethical Statement

Etik kurul belgesi ek dosya şeklinde yüklenmiştir.

References

  • Atalay S, Kök S (2023) The Comparison of Polymorphisms in the Heat Shock Transcription Factor 1 Gene of Turkish Grey Cattle and Holstein Cattle. Kafkas Universitesi Veteriner Fakültesi Dergisi 29(5): 429-435.
  • Bayram A, Marvuglia A, Gutierrez TN, Weis J P, Conter G, Zimmer S (2023) Sustainable farming strategies for mixed crop-livestock farms in Luxembourg simulated with a hybrid agent-based and life-cycle assessment model. Journal of Cleaner Production 386: 135759.
  • Bilgen N, Cinar Kul B, Offord V, Werling D, Ertugrul O. (2016) Determination of genetic variations of Toll-like receptor (TLR) 2, 4, and 6 with next-generation sequencing in native cattle breeds of Anatolia and Holstein Friesian. Diversity 8(4): 23.
  • Çıldır ÖŞ, Özmen Ö (2019) Sıcak stresi ve termotolerans: Heat stress and thermotolerance: Molecular studies in cattle. Livestock Studies 59 (Ek Sayı): 117-129.
  • Çobanoğlu Ö, Ardicli S (2022) Genetic variation at the OLR1, ANXA9, MYF5, LTF, IGF1, LGB, CSN3, PIT1, MBL1, CACNA2D1, and ABCG2 loci in Turkish Grey Steppe, Anatolian Black, and EastAnatolian Red cattle. Turkish Journal of Veterinary and Animal Sciences 46(3): 494-504.
  • Demir E, Bilginer U, Balcioglu MS, Karsli T (2021a) Direct and indirect contributions of molecular genetics to farm animal welfare: a review. Animal Health Research Reviews 22(2): 177-186.
  • Demir E, Karsli T, Balcıoğlu MS (2021b) A comprehensive review on genetic diversity and phylogenetic relationships amongnative Turkish cattle breeds based on microsatellite markers. Turkish Journal of Veterinary and Animal Sciences 45(1): 1-10.
  • Demir E, Ceccobelli S, Bilginer U, Pasquini M, Attard G, Karsli T (2022a) Conservation and selection of genes related to environmental adaptation in native small ruminant breeds: a review. Ruminants 2(2): 255-270.
  • Demir E, Moravčíková N, Karsli T, Kasarda R (2022b) Future perspective of NGS data for evaluation of population genetic structure in Turkish cattle. Acta fytotechnica et zootechnica ISSN 1336-9245-25(2).
  • Duangjinda M, Jindatajak, Y, Tipvong, W, Sriwarothai, J, Pattarajinda, V, Katawati S., Boonkum W (2013) Association of BoLA-DRB3 alleles with tick-borne disease tolerance in dairy cattle in a tropical environment. Veterinary Parasitology 196(3-4): 314-320.
  • El-Zarei MF, Alseaf AM, Alhaidary AA, Mousa EF, Okab AB, Samara E M, Abdoun KA (2019) Short-term heat shock proteins 70 and 90 mRNA expression profile and its relation to thermo-physiological parameters in goats exposed to heat stress. International journal of biometeorology 63: 459-465.
  • Gaughan JB, Mader TL, Holt SM, Sullivan ML, Hahn GL. (2010) Assessing the heat tolerance of 17 beef cattle genotypes. International Journal of Biometerology 54: 617-627.
  • GDARP (2009) Introduction catalogue of Turkish domestic animal genetic resources (in Turkish). https://www.tarimorman.gov.tr/TAGEM/Belgeler/yayin/Katalog%20T%C3%BCrk%C3%A7e.pdf. Accessed 28 November, 2023.
  • Guzmán LF, Martínez-Velázquez G, Villaseñor-González F, Vega-Murillo VE, Palacios-Fránquez JA, Ríos-Utrera Á, Montaño-Bermúdez M (2023) Expression of heat shock protein genes in Simmental cattle exposed to heat stress. doi: 10.5713/ab.22.0266.
  • Hariyono DNH, Prihandini P W. (2022) Association of selected gene polymorphisms with thermotolerance traits in cattle–A review. Animal Bioscience 35(11): 1635.
  • Irivboje YI, Sanni MT, Fafiolu AO, Olowofeso O, Ikeobi CON (2020) Genetic polymorphisms in part of intron 7 and exon 8 of HSP90AA1 gene and its association with heat tolerance traits in two exotic layer chicken strains. Tropical animal health and production 52: 969-977.
  • Jia P, Cai C, Qu K, Chen N, Jia Y. Hanif Q, Liu J, Zhang J, Chen H, Huang B, Lei, C (2019). Four novel SNPs of MYO1A gene associated with heat-tolerance in Chinese cattle. Animals 9(11): 964.
  • Karayel F, Karslı T (2022) Genotypic structure of four cattle breeds raised in Turkey by loci related to several diseases. Mediterranean Agricultural Sciences 35(1): 39-45.
  • Kumar R, Gupta ID, Verma A, Singh S, Kumari R, Verma N (2022) Genetic polymorphism in HSPB6 gene and their association with heat tolerance traits in Indian Karan Fries (Bos taurus x Bos indicus) cattle. Animal Biotechnology 33(7): 1416-1427.
  • Lu H, Guan Y, He L, Adhikari H, Pellikka P, Heiskanen J, Maeda E (2020) Patch aggregation trends of the global climate landscape under future global warming scenario. International Journal of Climatology 40(5): 2674-2685.
  • Malhi GS, Kaur M, Kaushik P (2021) Impact of climate change on agriculture and its mitigation strategies: A review. Sustainability 13(3): 1318.
  • Miller S, Dykes D, Plesky HA (1988) Simple Salting out Procedure for Extracting DNA from Human Cells Nucleic Acids Research 16: 1215.
  • Mohanarao GJ, Mukherjee A, Banerjee D, Gohain M, Dass, G, Brahma B, De S (2014) HSP70 family genes and HSP27 expression in response to heat and cold stress in vitro in peripheral blood mononuclear cells of goat (Capra hircus). Small Ruminant Research 116(2-3): 94-99.
  • Öner Y, Keskin A, Üstüner H, Soysal D, Karakaş V (2017) Genetic diversity of the 3ꞌ and 5ꞌ untranslated regions of the HSP70. 1 gene between native Turkish and Holstein Friesian cattle breeds. South African Journal of Animal Science 47(4): 424-439.
  • Prastowo S, Adzdzakiy MM, Vanessa R, Pambuko G, Susilowati A (2021) Polymorphism scanning of HSP90AB1 gene in local Friesian Holstein as molecular marker for heat stress resistance. In E3S Web of Conferences EDP Sciences 306, 05016.
  • Rawash RAA, Sharaby MA, Hassan GEDA, Elkomy AE, Hafez EE, Hafsa SHA, Salem MM (2022) Expression profiling of HSP 70 and interleukins 2, 6 and 12 genes of Barki sheep during summer and winter seasons in two different locations. International Journal of Biometeorology 66(10): 2047-2053.
  • Sajjanar B, Deb R, Singh U, Kumar S, Brahmane M, Nirmale A, Bal SK, Minhas P (2015) Identification of SNP in HSP90AB1 and its association with the relative thermotolerance and milk production traits in Indian dairy cattle. Animal Biotechnology 26(1): 45-50.
  • Şenel A, Duman E, Türel ÖO (2019) Genetic adaptation mechanisms against changing climate conditions on farm animals. Gaziosmanpaşa Üniversitesi Tıp Fakültesi Dergisi 11(1): 1-23.
  • Sheraiba N, Hemeda S, Mahboub H (2019) HSP70 and HSP90β genes polymorphism and its association with thermotolerance in Fayoumi and Leghorn chicken breeds. Journal of Current Veterinary Research 1(2): 56-62.
  • Sheraz M, ud Din F, Un Nabi MS, Rao S, Shafiq B, Murtaza G, Farooq M, Iqbal F (2023). Association of single nucleotide polymorphisms in heat stress protein 70 (HSP70) and 90 (HSP90) with the susceptibility of Pakistani sheep breeds to hemoparasitic infections. Animal Biotechnology 1-8.
  • TUIK (2022) Statistical Tables, Number of Bovine Animals, https://data.tuik.gov.tr/Kategori/GetKategori?p=tarim-111&dil=1. Accessed: 28 November, 2023.
  • UNEP (2022) United Nations Environment Programme, Emissions gap report, The closing window-Climate crisis calls for rapid transformation of societies, Nairobi.
  • Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, The user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada.
  • Yer EN (2017) Genome-Wıde survey of heat shock proteıns (hsp) and expressıon analysıs of hsp genes under abıotıc stress condıtıons ın some Populus taxons. PhD Thesis, Kastamonu Üniversitesi, Fen Bilimleri Enstitüsü, Kastamonu.
  • Yurdagül KG, Sude A, Bilginer Ü, Karslı T, Demir E (2023) Genetic variations in HSP90AA1 gene region in Pırlak sheep breed. Hayvansal Üretim 64(1): 12-16.
  • Zhang M, Wu D, Ahmed Z, Liu X, Chen J, Ma, J, Wang M, Liu J, Zhang J, Huang B, Lei C (2023) The genetic secrets of adaptation: decoding the significance of the 30-bp insertion in the KRT77 gene for Chinese cattle. Animal Biotechnology 1-8.

HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye

Year 2024, Volume: 37 Issue: 1, 51 - 55, 17.04.2024
https://doi.org/10.29136/mediterranean.1408404

Abstract

Global warming is becoming a greater threat for the agricultural sector, while molecular genetics studies still hold new opportunities, to not only detect heat-tolerant animals, but also to allow for increasing the frequencies of desired genotypes in a certain population. In this study, HSP90AB1 gene associated with heat tolerance was investigated in four cattle breeds known as Zavot (ZAV), Sout Anatolian Yellow (SAY), South Anatolian Red (SAR), and Brown Swiss (BS) reared in Türkiye via Allele-Specific Polymerase Chain Reaction (AS-PCR). 4338T>C mutation of the HSP90AB1 gene yielded a total of three genotypes (CC, CT, and TT) across all cattle breeds in which C allele frequency ranged from 0.34 (SAY) to 0.73 (BS), while T allele frequency varied between 0.27 (BS) and 0.66 (SAY). In BS, CC was the genotype with the highest frequency (0.50), whereas the frequency of CC was lower than CT and TT in the Anatolian breed (ZAV, SAR, and SAY). Similarly, the frequency of TT was higher in native Anatolian breeds than BS (0.05). All the populations studied were in Hardy-Weinberg Equilibrium (HWE) in terms of the HSP90AB1 gene. This study confirmed that the HSP90AB1 gene was polymorphic in four cattle breeds reared in Türkiye. This polymorphism has the potential to allow for improving heat tolerance to maintain animal production in the future via suitable selection studies. Therefore, this polymorphism should be conserved in Anatolian cattle breeds, while other genes related to different environmental stressors may be monitored by further studies.

References

  • Atalay S, Kök S (2023) The Comparison of Polymorphisms in the Heat Shock Transcription Factor 1 Gene of Turkish Grey Cattle and Holstein Cattle. Kafkas Universitesi Veteriner Fakültesi Dergisi 29(5): 429-435.
  • Bayram A, Marvuglia A, Gutierrez TN, Weis J P, Conter G, Zimmer S (2023) Sustainable farming strategies for mixed crop-livestock farms in Luxembourg simulated with a hybrid agent-based and life-cycle assessment model. Journal of Cleaner Production 386: 135759.
  • Bilgen N, Cinar Kul B, Offord V, Werling D, Ertugrul O. (2016) Determination of genetic variations of Toll-like receptor (TLR) 2, 4, and 6 with next-generation sequencing in native cattle breeds of Anatolia and Holstein Friesian. Diversity 8(4): 23.
  • Çıldır ÖŞ, Özmen Ö (2019) Sıcak stresi ve termotolerans: Heat stress and thermotolerance: Molecular studies in cattle. Livestock Studies 59 (Ek Sayı): 117-129.
  • Çobanoğlu Ö, Ardicli S (2022) Genetic variation at the OLR1, ANXA9, MYF5, LTF, IGF1, LGB, CSN3, PIT1, MBL1, CACNA2D1, and ABCG2 loci in Turkish Grey Steppe, Anatolian Black, and EastAnatolian Red cattle. Turkish Journal of Veterinary and Animal Sciences 46(3): 494-504.
  • Demir E, Bilginer U, Balcioglu MS, Karsli T (2021a) Direct and indirect contributions of molecular genetics to farm animal welfare: a review. Animal Health Research Reviews 22(2): 177-186.
  • Demir E, Karsli T, Balcıoğlu MS (2021b) A comprehensive review on genetic diversity and phylogenetic relationships amongnative Turkish cattle breeds based on microsatellite markers. Turkish Journal of Veterinary and Animal Sciences 45(1): 1-10.
  • Demir E, Ceccobelli S, Bilginer U, Pasquini M, Attard G, Karsli T (2022a) Conservation and selection of genes related to environmental adaptation in native small ruminant breeds: a review. Ruminants 2(2): 255-270.
  • Demir E, Moravčíková N, Karsli T, Kasarda R (2022b) Future perspective of NGS data for evaluation of population genetic structure in Turkish cattle. Acta fytotechnica et zootechnica ISSN 1336-9245-25(2).
  • Duangjinda M, Jindatajak, Y, Tipvong, W, Sriwarothai, J, Pattarajinda, V, Katawati S., Boonkum W (2013) Association of BoLA-DRB3 alleles with tick-borne disease tolerance in dairy cattle in a tropical environment. Veterinary Parasitology 196(3-4): 314-320.
  • El-Zarei MF, Alseaf AM, Alhaidary AA, Mousa EF, Okab AB, Samara E M, Abdoun KA (2019) Short-term heat shock proteins 70 and 90 mRNA expression profile and its relation to thermo-physiological parameters in goats exposed to heat stress. International journal of biometeorology 63: 459-465.
  • Gaughan JB, Mader TL, Holt SM, Sullivan ML, Hahn GL. (2010) Assessing the heat tolerance of 17 beef cattle genotypes. International Journal of Biometerology 54: 617-627.
  • GDARP (2009) Introduction catalogue of Turkish domestic animal genetic resources (in Turkish). https://www.tarimorman.gov.tr/TAGEM/Belgeler/yayin/Katalog%20T%C3%BCrk%C3%A7e.pdf. Accessed 28 November, 2023.
  • Guzmán LF, Martínez-Velázquez G, Villaseñor-González F, Vega-Murillo VE, Palacios-Fránquez JA, Ríos-Utrera Á, Montaño-Bermúdez M (2023) Expression of heat shock protein genes in Simmental cattle exposed to heat stress. doi: 10.5713/ab.22.0266.
  • Hariyono DNH, Prihandini P W. (2022) Association of selected gene polymorphisms with thermotolerance traits in cattle–A review. Animal Bioscience 35(11): 1635.
  • Irivboje YI, Sanni MT, Fafiolu AO, Olowofeso O, Ikeobi CON (2020) Genetic polymorphisms in part of intron 7 and exon 8 of HSP90AA1 gene and its association with heat tolerance traits in two exotic layer chicken strains. Tropical animal health and production 52: 969-977.
  • Jia P, Cai C, Qu K, Chen N, Jia Y. Hanif Q, Liu J, Zhang J, Chen H, Huang B, Lei, C (2019). Four novel SNPs of MYO1A gene associated with heat-tolerance in Chinese cattle. Animals 9(11): 964.
  • Karayel F, Karslı T (2022) Genotypic structure of four cattle breeds raised in Turkey by loci related to several diseases. Mediterranean Agricultural Sciences 35(1): 39-45.
  • Kumar R, Gupta ID, Verma A, Singh S, Kumari R, Verma N (2022) Genetic polymorphism in HSPB6 gene and their association with heat tolerance traits in Indian Karan Fries (Bos taurus x Bos indicus) cattle. Animal Biotechnology 33(7): 1416-1427.
  • Lu H, Guan Y, He L, Adhikari H, Pellikka P, Heiskanen J, Maeda E (2020) Patch aggregation trends of the global climate landscape under future global warming scenario. International Journal of Climatology 40(5): 2674-2685.
  • Malhi GS, Kaur M, Kaushik P (2021) Impact of climate change on agriculture and its mitigation strategies: A review. Sustainability 13(3): 1318.
  • Miller S, Dykes D, Plesky HA (1988) Simple Salting out Procedure for Extracting DNA from Human Cells Nucleic Acids Research 16: 1215.
  • Mohanarao GJ, Mukherjee A, Banerjee D, Gohain M, Dass, G, Brahma B, De S (2014) HSP70 family genes and HSP27 expression in response to heat and cold stress in vitro in peripheral blood mononuclear cells of goat (Capra hircus). Small Ruminant Research 116(2-3): 94-99.
  • Öner Y, Keskin A, Üstüner H, Soysal D, Karakaş V (2017) Genetic diversity of the 3ꞌ and 5ꞌ untranslated regions of the HSP70. 1 gene between native Turkish and Holstein Friesian cattle breeds. South African Journal of Animal Science 47(4): 424-439.
  • Prastowo S, Adzdzakiy MM, Vanessa R, Pambuko G, Susilowati A (2021) Polymorphism scanning of HSP90AB1 gene in local Friesian Holstein as molecular marker for heat stress resistance. In E3S Web of Conferences EDP Sciences 306, 05016.
  • Rawash RAA, Sharaby MA, Hassan GEDA, Elkomy AE, Hafez EE, Hafsa SHA, Salem MM (2022) Expression profiling of HSP 70 and interleukins 2, 6 and 12 genes of Barki sheep during summer and winter seasons in two different locations. International Journal of Biometeorology 66(10): 2047-2053.
  • Sajjanar B, Deb R, Singh U, Kumar S, Brahmane M, Nirmale A, Bal SK, Minhas P (2015) Identification of SNP in HSP90AB1 and its association with the relative thermotolerance and milk production traits in Indian dairy cattle. Animal Biotechnology 26(1): 45-50.
  • Şenel A, Duman E, Türel ÖO (2019) Genetic adaptation mechanisms against changing climate conditions on farm animals. Gaziosmanpaşa Üniversitesi Tıp Fakültesi Dergisi 11(1): 1-23.
  • Sheraiba N, Hemeda S, Mahboub H (2019) HSP70 and HSP90β genes polymorphism and its association with thermotolerance in Fayoumi and Leghorn chicken breeds. Journal of Current Veterinary Research 1(2): 56-62.
  • Sheraz M, ud Din F, Un Nabi MS, Rao S, Shafiq B, Murtaza G, Farooq M, Iqbal F (2023). Association of single nucleotide polymorphisms in heat stress protein 70 (HSP70) and 90 (HSP90) with the susceptibility of Pakistani sheep breeds to hemoparasitic infections. Animal Biotechnology 1-8.
  • TUIK (2022) Statistical Tables, Number of Bovine Animals, https://data.tuik.gov.tr/Kategori/GetKategori?p=tarim-111&dil=1. Accessed: 28 November, 2023.
  • UNEP (2022) United Nations Environment Programme, Emissions gap report, The closing window-Climate crisis calls for rapid transformation of societies, Nairobi.
  • Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, The user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada.
  • Yer EN (2017) Genome-Wıde survey of heat shock proteıns (hsp) and expressıon analysıs of hsp genes under abıotıc stress condıtıons ın some Populus taxons. PhD Thesis, Kastamonu Üniversitesi, Fen Bilimleri Enstitüsü, Kastamonu.
  • Yurdagül KG, Sude A, Bilginer Ü, Karslı T, Demir E (2023) Genetic variations in HSP90AA1 gene region in Pırlak sheep breed. Hayvansal Üretim 64(1): 12-16.
  • Zhang M, Wu D, Ahmed Z, Liu X, Chen J, Ma, J, Wang M, Liu J, Zhang J, Huang B, Lei C (2023) The genetic secrets of adaptation: decoding the significance of the 30-bp insertion in the KRT77 gene for Chinese cattle. Animal Biotechnology 1-8.
There are 36 citations in total.

Details

Primary Language English
Subjects Animal Biotechnology in Agriculture, Animal Science, Genetics and Biostatistics
Journal Section Makaleler
Authors

Bahar Argun Karslı 0000-0002-1762-9847

Publication Date April 17, 2024
Submission Date December 22, 2023
Acceptance Date March 20, 2024
Published in Issue Year 2024 Volume: 37 Issue: 1

Cite

APA Argun Karslı, B. (2024). HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye. Mediterranean Agricultural Sciences, 37(1), 51-55. https://doi.org/10.29136/mediterranean.1408404
AMA Argun Karslı B. HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye. Mediterranean Agricultural Sciences. April 2024;37(1):51-55. doi:10.29136/mediterranean.1408404
Chicago Argun Karslı, Bahar. “HSP90AB1 (SNP-4338T>C) Gene Polymorphism Associated With Thermo-Tolerance in Some Cattle Breeds in Türkiye”. Mediterranean Agricultural Sciences 37, no. 1 (April 2024): 51-55. https://doi.org/10.29136/mediterranean.1408404.
EndNote Argun Karslı B (April 1, 2024) HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye. Mediterranean Agricultural Sciences 37 1 51–55.
IEEE B. Argun Karslı, “HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye”, Mediterranean Agricultural Sciences, vol. 37, no. 1, pp. 51–55, 2024, doi: 10.29136/mediterranean.1408404.
ISNAD Argun Karslı, Bahar. “HSP90AB1 (SNP-4338T>C) Gene Polymorphism Associated With Thermo-Tolerance in Some Cattle Breeds in Türkiye”. Mediterranean Agricultural Sciences 37/1 (April 2024), 51-55. https://doi.org/10.29136/mediterranean.1408404.
JAMA Argun Karslı B. HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye. Mediterranean Agricultural Sciences. 2024;37:51–55.
MLA Argun Karslı, Bahar. “HSP90AB1 (SNP-4338T>C) Gene Polymorphism Associated With Thermo-Tolerance in Some Cattle Breeds in Türkiye”. Mediterranean Agricultural Sciences, vol. 37, no. 1, 2024, pp. 51-55, doi:10.29136/mediterranean.1408404.
Vancouver Argun Karslı B. HSP90AB1 (SNP-4338T>C) gene polymorphism associated with thermo-tolerance in some cattle breeds in Türkiye. Mediterranean Agricultural Sciences. 2024;37(1):51-5.

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