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Genetic improvement of economic traits in Murrah buffalo using significant SNPs from genome-wide association study

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Abstract

GWAS helps to identify QTL and candidate genes of specific traits. Buffalo breeding has primarily focused on milk production, but its negative correlation with reproduction traits resulted in unfavorable decline of reproductive performance among buffaloes. A genome wide scan was performed on a total of 120 Murrah buffaloes genotyped by ddRAD sequencing for 13 traits related to female fertility, production, and growth. The identified 25 significant single nucleotide polymorphisms (SNPs) (P <1×106) are associated with age at first calving (AFC), age at first service (AFS), period from calving to 1st Artifical Insemination (AI), service period (SP) and 6 month body weight (6M). Fifteen genetic variants overlapped with different QTL regions of reported studies. Among the associated loci, outstanding candidate genes for fertility, including AQP1, TRNAE-CUC, NRIP1, CPNE4, and VOPP1, have effect in different fertility traits. AQP1 gene is expressed in ovulatory phase and various stages of pregnancy. TRNAE-CUC gene is associated with AFC and number . of calvings after 4 years of age. Glycogen content–associated gene CPNE4 regulates muscle glycogen and is upregulated during early pregnancy. NRIP1 generegulates ovulation, corpus luteum at pregnancy, and mammary gland development. The objective is to identify potential genomic regions and genetic variants associated with economic traits and to select the most significant SNP which have positive effect on all the traits.

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Data availability

The data set generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Amaral ME, Grant JR, Riggs PK, Stafuzza NB, Goldammer T, Weikard R, Brunner RM, Kochan KJ, Greco AJ, Jeong J, Cai Z. A first generation whole genome RH map of the river buffalo with comparison to domestic cattle. BMC genomics. 2008;9(1):1-1.

    Article  Google Scholar 

  • Abo-Ismail MK, Brito LF, Miller SP, Sargolzaei M, Grossi DA, Moore SS, Plastow G, Stothard P, Nayeri S, Schenkel FS. Genome-wide association studies and genomic prediction of breeding values for calving performance and body conformation traits in Holstein cattle. Genetics Selection Evolution. 2017;49(1):1-29.

    Article  Google Scholar 

  • Aliloo H, Pryce JE, González-Recio O, Cocks BG, Hayes BJ. Validation of kers with non-additive effects on milk yield and fertility in Holstein and Jersey cows. BMC genetics. 2015;16(1):1-6.

    Article  CAS  Google Scholar 

  • Andrews S. FastQC: A quality control tool for high throughput sequence data. Available: https://www.bioinformatics.babraham.ac.uk/projects/fastqc. 2010.

  • Ayuso M, Fernandez A, Nunez Y, Benitez R, Isabel B, Fernandez AI, Rey AI, Gonzalez-Bulnes A, Medrano JF, Cánovas Á, Lopez-Bote CJ. Developmental stage, muscle and genetic type modify muscle transcriptome in pigs: effects on gene expression and regulatory factors involved in growth and metabolism. PloS one. 2016;11(12):e0167858.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbato M, Hailer F, Upadhyay M, Del Corvo M, Colli L, Negrini R, Kim ES, Crooijmans RP, Sonstegard T, Ajmone-san P. Adaptive introgression from indicine cattle into white cattle breeds from Central Italy. Scientific reports. 2020;10(1):1-1.

    Article  Google Scholar 

  • Browning BL, Browning SR. Genotype imputation with millions of reference samples. The American Journal of Human Genetics. 2016;98(1):116-26.

    Article  CAS  PubMed  Google Scholar 

  • Buaban S, Lengnudum K, Boonkum W, Phakdeedindan P. Genome-wide association study on milk production and somatic cell score for Thai dairy cattle using weighted single-step approach with random regression test-day model. Journal of Dairy Science. 2022;105(1):468-94.

    Article  CAS  PubMed  Google Scholar 

  • Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA. Stacks: an analysis tool set for population genomics. Molecular ecology. 2013 :22(11):3124-40.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen SY, Schenkel FS, Melo AL, Oliveira HR, Pedrosa VB, Araujo AC, Melka MG, Brito LF. Identifying pleiotropic variants and candidate genes for fertility and reproduction traits in Holstein cattle via association studies based on imputed whole-genome sequence genotypes. BMC genomics. 2022;23(1):1-22.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cochran SD, Cole JB, Null DJ, Hansen PJ. Discovery of single nucleotide polymorphisms in candidate genes associated with fertility and production traits in Holstein cattle. BMC genetics. 2013;14(1):1-23.

    Article  Google Scholar 

  • Costa-Urrutia P, Colistro V, Jiménez-Osorio AS, Cárdenas-Hernández H, Solares-Tlapechco J, Ramirez-Alcántara M, Granados J, Ascencio-Montiel ID, Rodríguez-Arellano ME. Genome-wide association study of body mass index and body fat in Mexican-Mestizo children. Genes. 2019;10(11):945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Da Cruz AS, Silva DC, Minasi LB, de Farias Teixeira LK, Rodrigues FM, da Silva CC, do Carmo AS, da Silva MV, Utsunomiya YT, Garcia JF, da Cruz AD. Single-Nucleotide Polymorphism variations associated with specific genes putatively identified enhanced genetic predisposition for 305-day milk yield in the Girolando crossbreed. Frontiers in Genetics. 2021:1720.

  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic ker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics. 2011;12(7):499-510.

    Article  CAS  PubMed  Google Scholar 

  • de Araujo Neto FR, Takada L, Dos Santos DJ, Aspilcueta-Borquis RR, Cardoso DF, do Nascimento AV, Leão KM, de Oliveira HN, Tonhati H. Identification of genomic regions related to age at first calving and first calving interval in water buffalo using single-step GBLUP. Reproduction in Domestic Animals. 2020;55(11):1565-72.

    Article  PubMed  Google Scholar 

  • Du C, Deng T, Zhou Y, Ye T, Zhou Z, Zhang S, Shao B, Wei P, Sun H, Khan FA, Yang L. Systematic analyses for candidate genes of milk production traits in water buffalo (Bubalus Bubalis). Animal Genetics. 2019;50(3):207-16.

    Article  CAS  PubMed  Google Scholar 

  • Du Puy L, Beqqali A, Monshouwer-Kloots J, Haagsman HP, Roelen BA, Passier R. CAZIP, a novel protein expressed in the developing heart and nervous system. Developmental Dynamics: An Official Publication of the American Association of Anatomists. 2009;238(11):2903-11.

    Article  PubMed  Google Scholar 

  • Duan X, An B, Du L, Chang T, Liang M, Yang BG, Xu L, Zhang L, Li J, E G, Gao H. Genome-wide association analysis of growth curve parameters in Chinese Simmental beef cattle. Animals. 2021;11(1):192.

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS one. 2011;6(5):e19379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marete A, Lund MS, Boichard D, Ramayo-Caldas Y. A system-based analysis of the genetic determinism of udder conformation and health phenotypes across three French dairy cattle breeds. PLoS One. 2018;13(7):e0199931.

    Article  PubMed  PubMed Central  Google Scholar 

  • Morammazi S, Torshizi R, Rouzbehan Y, Sayyadnejad MB. PosterEstimates of genetic parameters for production and reproduction traits in Khuzestan buffalos of Iran. Italian Journal of Animal Science. 2007;6(sup2):421-424. https://doi.org/10.4081/ijas.2007.s2.421

    Article  Google Scholar 

  • Fan H, Wu Y, Qi X, Zhang J, Li J, Gao X, Zhang L, Li J, Gao H. Genome-wide detection of selective signatures in Simmental cattle. Journal of applied genetics. 2014;55(3):343-51.

    Article  CAS  PubMed  Google Scholar 

  • Frischknecht M, Bapst B, Seefried FR, Signer-Hasler H, Garrick D, Stricker C, Fries R, Russ I, Sölkner J, Bieber A, Strillacci MG. Genome-wide association studies of fertility and calving traits in Brown Swiss cattle using imputed whole-genome sequences. BMC genomics. 2017;18(1):1-3.

    Article  Google Scholar 

  • Gobikrushanth M, Purfield DC, Canadas ER, Herlihy MM, Kenneally J, Murray M, Kearney FJ, Colazo MG, Ambrose DJ, Butler ST. Anti-Müllerian hormone in grazing dairy cows: Identification of factors affecting plasma concentration, relationship with phenotypic fertility, and genome-wide associations. Journal of dairy science. 2019 ;102(12):11622-35.

    Article  CAS  PubMed  Google Scholar 

  • Gordon I. Controlled Reproduction in Cattle and Buffalo. (CAB International) 1996; 438

    Google Scholar 

  • Gouveia JJ, Silva MV, Paiva SR, Oliveira SM. Identification of selection signatures in livestock species. Genetics and molecular biology. 2014;37:330-42.

    Article  Google Scholar 

  • Harvey WR. User's Guide for LSMLMW. Mixed model least squares and maximum likelihood computer program. PC-Version. 1990;2.

  • Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proceedings of the National Academy of Sciences. 2009;106(23):9362-7.

    Article  CAS  Google Scholar 

  • Hoglund JK, Guldbrandtsen B, Lund MS, Sahana G. Analyzes of genome-wide association follow-up study for calving traits in dairy cattle. Bmc Genetics. 2012;13(1):1-9.

    Article  Google Scholar 

  • Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, Guan J, Fan D, Weng Q, Huang T, Dong G. High-throughput genotyping by whole-genome resequencing. Genome research. 2009;19(6):1068-76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahuey-Martínez FJ, Parra-Bracamonte GM, Sifuentes-Rincón AM, Martínez-González JC, Gondro C, García-Pérez CA, López-Bustamante LA. Genomewide association analysis of growth traits in Charolais beef cattle. Journal of animal science. 2016;94(11):4570-82.

    Article  PubMed  Google Scholar 

  • Jiang BJ, Zhan XL, Fu CZ, Wang HB, Cheng G, Zan LS. Identification of ANAPC13 gene polymorphisms associated with body measurement traits in Bos taurus. Genet Mol Res. 2012;11(3):2862-70.

    Article  CAS  PubMed  Google Scholar 

  • Jost P, Fasshauer M, Kahn CR, Benito M, Meyer M, Ott V, Lowell BB, Klein HH, Klein J. Atypical β-adrenergic effects on insulin signaling and action in β3-adrenoceptor-deficient brown adipocytes. American Journal of Physiology-Endocrinology and Metabolism. 2002 ;283(1):E146-53.

    Article  CAS  PubMed  Google Scholar 

  • Kadarmideen HN, Simm G. Selection responses expected from index selection including disease resistance, fertility and longevity in dairy cattle. InProceedings of The Seventh World Congress on Genetics Applied to Livestock Production (WCGALP) 2002;119-122.

  • Krawczak M, Zschocke J. A role for overdominant selection in phenylketonuria? Evidence from molecular data. Human mutation. 2003 ;21(4):394-7.

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature methods. 2012 ;9(4):357-9..

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KT, Byun MJ, Kang KS, Park EW, Lee SH, Cho S, Kim H, Kim KW, Lee T, Park JE, Park W. Neuronal genes for subcutaneous fat thickness in human and pig are identified by local genomic sequencing and combined SNP association study. PloS one. 2011 6(2):e16356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonardsson G, Jacobs MA, White R, Jeffery R, Poulsom R, Milligan S, Parker M. Embryo transfer experiments and ovarian transplantation identify the ovary as the only site in which nuclear receptor interacting protein 1/RIP140 action is crucial for female fertility. Endocrinology. 2002;143(2):700-7.

    Article  CAS  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078-9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu A, Wang Y, Sahana G, Zhang Q, Liu L, Lund MS, Su G. Genome-wide association studies for female fertility traits in Chinese and Nordic Holsteins. Scientific reports. 2017;7(1):1-2.

    Google Scholar 

  • Liu H, Koukoulas I, Ross MC, Wang S, Wintour EM. Quantitative comparison of placental expression of three aquaporin genes. Placenta. 2004;25(6):475-8.

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Liang A, Campanile G, Plastow G, Zhang C, Wang Z, Salzano A, Gasparrini B, Yang L. Genome-wide association studies for milk production traits in Mediterranean water buffalo. Revista CES Medicina Veterinaria y Zootecnia. 2016;11(3):198-9.

    Google Scholar 

  • Liu JJ, Liang AX, Campanile G, Plastow G, Zhang C, Wang Z, Salzano A, Gasparrini B, Cassandro M, Yang LG. Genome-wide association studies to identify quantitative trait loci affecting milk production traits in water buffalo. Journal of dairy science. 2018 ;101(1):433-44.

    Article  CAS  PubMed  Google Scholar 

  • Lu D, Miller S, Sargolzaei M, Kelly M, Vander Voort G, Caldwell T, Wang Z, Plastow G, Moore S. Genome-wide association analyses for growth and feed efficiency traits in beef cattle. Journal of animal science. 2013;91(8):3612-33.

    Article  CAS  PubMed  Google Scholar 

  • Medeiros de Oliveira Silva R, Bonvino Stafuzza N, de Oliveira Fragomeni B, Miguel Ferreira de Cago G, Matos Ceacero T, Noely dos Santos Gonçalves Cyrillo J, Baldi F, Augusti Boligon A, Zerlotti Mercadante ME, Lino Lourenco D, Misztal I. Genome-wide association study for carcass traits in an experimental Nelore cattle population. PLoS One. 2017 ; 12(1):e0169860.

    Article  Google Scholar 

  • Melo TP, De Cago GM, De Albuquerque LG, Carvalheiro R. Genome-wide association study provides strong evidence of genes affecting the reproductive performance of Nellore beef cows. PLoS One. 2017 ;12(5):e0178551.

    Article  PubMed  PubMed Central  Google Scholar 

  • Michelizzi VN, Dodson MV, Pan Z, Aal ME, Michal JJ, McLean DJ, Womack JE, Jiang Z. Water buffalo genome science comes of age. International journal of biological sciences. 2010;6(4):333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mota RR, Guiães SE, Fortes MR, Hayes B, Silva FF, Verardo LL, Kelly MJ, de Campos CF, Guiães JD, Wenceslau RR, Penitente-Filho JM. Genome-wide association study and annotating candidate gene networks affecting age at first calving in Nellore cattle. Journal of Animal Breeding and Genetics. 2017;134(6):484-92.

    Article  CAS  PubMed  Google Scholar 

  • Mu T, Hu H, Ma Y, Wen H, Yang C, Feng X, Wen W, Zhang J, Gu Y. Identifying key genes in milk fat metabolism by weighted gene co-expression network analysis. Scientific reports. 2022;12(1):1-3.

    Article  Google Scholar 

  • Muller MP, Rothammer S, Seichter D, Russ I, Hinrichs D, Tetens J, Thaller G, Medugorac I. Genome-wide mapping of 10 calving and fertility traits in Holstein dairy cattle with special regard to chromosome 18. Journal of dairy science. 2017;100(3):1987-2006.

    Article  PubMed  Google Scholar 

  • Nautiyal J, Steel JH, Mane MR, Oduwole O, Poliandri A, Alexi X, Wood N, Poutanen M, Zwart W, Stingl J, Parker MG. The transcriptional co-factor RIP140 regulates mamy gland development by promoting the generation of key mitogenic signals. Development. 2013;140(5):1079-89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira HR, Cant JP, Brito LF, Feitosa FL, Chud TC, Fonseca PA, Jamrozik J, Silva FF, Lourenco DA, Schenkel FS. Genome-wide association for milk production traits and somatic cell score in different lactation stages of Ayrshire, Holstein, and Jersey dairy cattle. Journal of dairy science. 2019;102(9):8159-74.

    Article  CAS  PubMed  Google Scholar 

  • Olives B, Martial S, Mattei MG, Matassi G, Rousselet G, Ripoche P, Cartron JP, Bailly P. Molecular characterization of a new urea transporter in the human kidney. S letters. 1996;386(2-3):156-60.

    Google Scholar 

  • Pedrosa VB, Schenkel FS, Chen SY, Oliveira HR, Casey TM, Melka MG, Brito LF. Genomewide Association Analyses of Lactation Persistency and Milk Production Traits in Holstein Cattle Based on Imputed Whole-Genome Sequence Data. Genes. 2021;12(11):1830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters SO, Kizilkaya K, Garrick DJ, Fernando RL, Reecy JM, Weaber RL, Silver GA, Thomas MG. Bayesian genome-wide association analysis of growth and yearling ultrasound measures of carcass traits in Brangus heifers. Journal of animal science. 2012; 90(10):3398-409.

    Article  CAS  PubMed  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PloS one. 2012; 7(5):e37135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pokharel K, Peippo J, Weldenegodguad M, Honkatukia M, Li MH, Kantanen J. Gene expression profiling of corpus luteum reveals the importance of immune system during early pregnancy in domestic sheep. bioRxiv. 2019:673558.

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American journal of human genetics. 2007;81(3):559-75.

    Article  CAS  PubMed  Google Scholar 

  • Ramos AD, Malhado CH, Carneiro PL, Gonçalves HC, Azevedo DM. Phenotypic and genetic characterization of the milk yield and calving interval in buffalo of the Murrah breed. Pesquisa Agropecuária Brasileira. 2006;41:1261-7.

    Article  Google Scholar 

  • Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J. g: Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic acids research. 2019 ;47(W1):W191-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roxström A, Strandberg E. Genetic analysis of functional, fertility-, mastitis-, and production-determined length of productive life in Swedish dairy cattle. Livestock Production Science. 2002;74(2):125-35.

    Article  Google Scholar 

  • Saatchi M, Schnabel RD, Taylor JF, Garrick DJ. Large-effect pleiotropic or closely linked QTL segregate within and across ten US cattle breeds. BMC genomics. 2014;15(1):1-7.

    Article  Google Scholar 

  • Sahana G, Guldbrandtsen B, Lund MS. Genome-wide association study for calving traits in Danish and Swedish Holstein cattle. Journal of Dairy Science. 2011;94(1):479-86.

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW. Purification of nucleic acids by extraction with phenol: chloroform. Cold Spring Harbor Protocols. 2006 ;2006(1):pdb-rot4455.

    Google Scholar 

  • Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao B, Sun H, Ahmad MJ, Ghanem N, Abdel-Shafy H, Du C, Deng T, Mansoor S, Zhou Y, Yang Y, Zhang S. Genetic Features of Reproductive Traits in Bovine and Buffalo: Lessons From Bovine to Buffalo. Frontiers in genetics. 2021;12:617128..

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Lee JS, Dang CG, Sudrajad P, Kim HC, Yeon SH, Kang HS, Lee SH. Stories and challenges of genome wide association studies in livestock—a review. Asian-Australasian journal of animal sciences. 2015;28(10):1371.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shirasawa K, Hirakawa H, Isobe S. Analytical workflow of double-digest restriction site-associated DNA sequencing based on empirical and in silico optimization in tomato. DNA research. 2016;23(2):145-53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigdel A, Bisinotto RS, Peñagaricano F. Genes and pathways associated with pregnancy loss in dairy cattle. Scientific reports. 2021;11(1):1-1.

    Article  Google Scholar 

  • Skowronski MT, Kwon TH, Nielsen S. Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. Journal of Histochemistry & Cytochemistry. 2009;57(1):61-7.

    Article  CAS  Google Scholar 

  • Stafuzza NB, Costa e Silva EV, Silva RM, Costa Filho LC, Barbosa FB, Macedo GG, Lobo RB, Baldi F. Genome-wide association study for age at puberty in young Nelore bulls. Journal of Animal Breeding and Genetics. 2020 ;137(2):234-44.

    Article  CAS  PubMed  Google Scholar 

  • Stulc J. Placental transfer of inorganic ions and water. Physiological reviews. 1997;77(3):805-36.

    Article  CAS  PubMed  Google Scholar 

  • Sudrajad P, Sharma A, Dang CG, Kim JJ, Kim KS, Lee JH, Kim S, Lee SH. Validation of single nucleotide polymorphisms associated with carcass traits in a commercial Hanwoo population. Asian-Australasian journal of animal sciences. 2016;29(11):1541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terakado AP, Costa RB, De Cago GM, Irano N, Bresolin T, Takada L, Carvalho CV, Oliveira HN, Carvalheiro R, Baldi F, De Albuquerque LG. Genome-wide association study for growth traits in Nelore cattle. Animal. 2018;12(7):1358-62.

    Article  CAS  PubMed  Google Scholar 

  • Thiruvenkadan AK, Panneerselvam S, Ramanujam R, Murali N. Analysis on the productive and reproductive traits of Murrah buffalo cows maintained in the coastal region of India. Applied Animal Husbandry & Rural Development. 2010;3:1-5.

    Google Scholar 

  • Thoroddsen A, Dahm-Kähler P, Lind AK, Weijdegård B, Lindenthal B, Müller J, Brännström M. The water permeability channels aquaporins 1–4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation. The Journal of Clinical Endocrinology & Metabolism. 2011;96(4):1021-8.

    Article  CAS  Google Scholar 

  • Todd JA, Walker NM, Cooper JD, Smyth DJ, Downes K, Plagnol V, Bailey R, Nejentsev S, Field SF, Payne F, Lowe CE. Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nature genetics. 2007;39(7):857-64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venturini GC, Cardoso DF, Baldi F, Freitas AC, Aspilcueta-Borquis RR, Santos DJ, Cago GM, Stafuzza NB, Albuquerque LG, Tonhati H. Association between single-nucleotide polymorphisms and milk production traits in buffalo. Genet. Mol. Res. 2014;13(4):10256-68.

    Article  CAS  PubMed  Google Scholar 

  • Vohra V, Chhotaray S, Gowane G, Alex R, Mukherjee A, Verma A, Deb SM. Genome-wide association studies in Indian Buffalo revealed genomic regions for lactation and fertility. Frontiers in Genetics. 2021;12.

  • Wang J, Hua LS, Pan H, Zhang LZ, Li MX, Huang YZ, Li ZJ, Lan XY, Lei CZ, Li CJ, Chen H. Haplotypes in the promoter region of the CIDEC gene associated with growth traits in Nanyang cattle. Scientific reports. 2015;5(1):1-8.

    Google Scholar 

  • Ward T, Wang M, Liu X, Wang Z, Xia P, Chu Y, Wang X, Liu L, Jiang K, Yu H, Yan M. Regulation of a dynamic interaction between two microtubule-binding proteins, EB1 and TIP150, by the mitotic p300/CBP-associated factor (PCAF) orchestrates kinetochore microtubule plasticity and chromosome stability during mitosis. Journal of Biological Chemistry. 2013;288(22):15771-85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson BA, Feenstra JM, Van Arsdale JM, Rai-Bhatti KS, Kim DJ, Coggins AS, Mattison GL, Yoo S, Steinman ED, Pira CU, Gongol BR. LHX2 mediates the FGF-to-SHH regulatory loop during limb development. Journal of developmental biology. 2018;6(2):13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wenzel JJ, Kaminski WE, Piehler A, Heimerl S, Langmann T, Schmitz G. ABCA10, a novel cholesterol-regulated ABCA6-like ABC transporter. Biochemical and biophysical research communications. 2003;306(4):1089-98.

    Article  CAS  PubMed  Google Scholar 

  • Williams JL, Iatino D, Pruitt KD, Sonstegard T, Smith TP, Low WY, Biagini T, Bomba L, Capomaccio S, Castiglioni B, Coletta A. Genome assembly and transcriptome resource for river buffalo, Bubalus bubalis (2 n= 50). Gigascience. 2017;6(10):gix088.

  • Woolf LI, McBean MS, Woolf FM, Cahalane SF. Phenylketonuria as a balanced polymorphism: the nature of the heterozygote advantage. Annals of Human Genetics. 1975;38(4):461-9.

    Article  CAS  PubMed  Google Scholar 

  • Ye D, Hoekstra M, Out R, Meurs I, Kruijt JK, Hildebrand RB, Van Berkel TJ, Van Eck M. Hepatic cell-specific ATP-binding cassette (ABC) transporter profiling identifies putative novel candidates for lipid homeostasis in mice. Atherosclerosis. 2008;196(2):650-8.

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Batista JL, Núñez-Domínguez R, Ramírez-Valverde R, Jahuey-tínez FJ, Herrera-Ojeda JB, Parra-Bracamonte GM. Discovering of genomic variations associated to growth traits by gwas in braunvieh cattle. Genes. 2021;12(11):1666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XQ, Jiang SS, Zhu XJ, Zou SW, Wang YH, Hu YC. Expression of aquaporin 1 and aquaporin 3 in fetal membranes and placenta in human term pregnancies with oligohydramnios. Placenta. 2009;30(8):670-6.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to the Director and Head Animal Genetics and Breeding, ICAR-NDRI, Karnal for providing necessary facilities and funds for DNA sequencing and all. We deeply acknowledge the support from in-charge of record room and livestock production management section for maintaining farm records.

Funding

ICAR-NDRI granted the required fund for this study

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Authors and Affiliations

  1. Division of Animal Genetics and Breeding, ICAR- National Dairy Research Institute, Karnal, Haryana, 132001, India

    Linda George, Rani Alex, Nidhi Sukhija, Komal Jaglan, Vikas Vohra, Ravi Kumar & Archana Verma

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  1. Linda George
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  2. Rani Alex
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George and Alex designed the research. George, Sukhija, and Jaglan conducted the bioinformatics studies of sequence quality control. Kumar and Vohra contributed the DNA sequences. Verma contributed the data and funding for DNA sequencing. George conducted the analysis and wrote the manuscript.

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Correspondence to Linda George.

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The experimental plan was approved by ICAR-NDRI Institutional Animal Ethics Committee (IAEC) constituted as per the article number 13 of the CPCSEA rules laid down by the Government of India.

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The authors declare no competing interest.

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George, L., Alex, R., Sukhija, N. et al. Genetic improvement of economic traits in Murrah buffalo using significant SNPs from genome-wide association study. Trop Anim Health Prod 55, 199 (2023). https://doi.org/10.1007/s11250-023-03606-3

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