Ovary transcriptome profiling in high- and low-yielding Chinese Chahua laying chickens

https://doi.org/10.17221/31/2022-CJASCitation:

Du Y.L., Liu L.L., Liu Y., Wang K., Shi H.M., He Y., Long Y.X., Sun D.W., Wu H., Zi X.N., Li X.Z., Huang W., Zhang R., Ge C.R. (2022): Ovary transcriptome profiling in high- and low-yielding Chinese Chahua laying chickens. Czech J. Anim. Sci., 67: 327–338.

supplementary materialdownload PDF

This study aimed to explore the underlying reasons for the differences in egg production in Chinese Chahua chickens. The Chahua chicken population was divided into two groups, namely a high-yielding group (H) and a low-yielding group (L). The egg-laying performance, ovarian morphology, histological characteristics, and serum hormone concentrations in the H and L groups were analysed. The results revealed that there were significant differences (P < 0.01) between the two groups for the age at the first egg and the number of eggs. The H group showed significantly more (P < 0.01) hierarchical follicles and small yellow follicles than the L group. While several secondary follicles and primary follicles were observed in the ovaries of the H group, only a few secondary follicles were observed in the ovaries of the L group. The serum concentrations of the follicle-stimulating hormone, the luteinising hormone, and oestradiol were significantly higher in the H group compared to that in the L group (P < 0.01). Next, we sequenced and analysed the ovarian expression profiles in the two groups using RNA-seq. The transcriptome sequencing revealed 875 differentially expressed genes (DEGs) between the H and L groups. Of the 875 DEGs, 624 were up-regulated, and 251 were down-regulated. The DEGs were mapped to 31 Gene Ontology (GO) terms and 15 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways for the ovarian tissue. The KEGG pathway analysis mainly revealed the involvement of focal adhesion, cytokine-cytokine receptor interaction, and the TGF-beta signalling pathway, while the GO analysis mainly showed involvement of the hormonal activity, extracellular matrix, and extracellular region. Our results showed that understanding the differences in the gene expressions between the ovarian tissues of high- and low-yielding hens may provide a useful reference for improving the egg-laying performance in Chahua chickens.

References:
Azmal SA, Bhuiyan AA, Omar AI, Ma S, Sun C, Han Z, Zhang M, Zhao S, Li S. Novel polymorphisms in RAPGEF6 gene associated with egg-laying rate in Chinese Jing Hong chicken using genome-wide SNP scan. Genes. 2019 May 20;10(5): 21 p.  https://doi.org/10.3390/genes10050384
 
Bedecarrats GY, Baxter M, Sparling B. An updated model to describe the neuroendocrine control of reproduction in chickens. Gen Comp Endocrinol. 2016 Feb 1;227:58-63.
 
Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc B. 1995 May;57(1):289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
 
Chen H, Huang RL, Zhang HX, Di KQ, Pan D, Hou YG. Effects of photoperiod on ovarian morphology and carcass traits at sexual maturity in pullets. Poult Sci. 2007 May 1;86(5):917-20.
 
Curry TJ, Osteen KG. The matrix metalloproteinase system: Changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev. 2003 Aug 1;24(4):428-65. https://doi.org/10.1210/er.2002-0005
 
Du X, Zhang L, Li X, Pan Z, Liu H, Li Q. TGF-β signaling controls FSHR signaling-reduced ovarian granulosa cell apoptosis through the SMAD4/miR-143 axis. Cell Death Dis. 2016 Nov;7(11): 12 p.  https://doi.org/10.1038/cddis.2016.379
 
Du Y, Liu L, He Y, Dou T, Jia J, Ge C. Endocrine and genetic factors affecting egg laying performance in chickens: A review. Br Poult Sci. 2020 Sep 2;61(5):538-49.
 
Edwards SJ, Reader KL, Lun S, Western A, Lawrence S, McNatty KP, Juengel JL. The cooperative effect of growth and differentiation factor-9 and bone morphogenetic protein (BMP)-15 on granulosa cell function is modulated primarily through BMP receptor II. Endocrinology. 2008 Mar 1;149(3):1026-30.  https://doi.org/10.1210/en.2007-1328
 
Ghanem K, Johnson AL. Follicle dynamics and granulosa cell differentiation in the turkey hen ovary. Poult Sci. 2018 Oct 1;97(10):3755-61. https://doi.org/10.3382/ps/pey224
 
Gosden R, Spears N. Programmed cell death in the reproductive system. Br Med Bull. 1997 Jan 1;53(3):644-61.  https://doi.org/10.1093/oxfordjournals.bmb.a011636
 
Guo X, Wang Y, Chen Q, Yuan Z, Chen Y, Guo M, Kang L, Sun Y, Jiang Y. The role of PTHLH in ovarian follicle selection, its transcriptional regulation and genetic effects on egg laying traits in hens. Front Genet. 2019 May 14;10: 15 p.
 
Hocking PM. Biology of breeding poultry. Bodmin, UK: CAB International; 2009. 75 p.
 
Ingman WV, Owens PC, Armstrong DT. Differential regulation by FSH and IGF-I of extracellular matrix IGFBP-5 in bovine granulosa cells: effect of association with the oocyte. Mol Cell Endocrinol. 2000 Jun 20;164(1-2):53-8.
 
Kim MH, Seo DS, Ko Y. Relationship between egg productivity and insulin-like growth factor-I genotypes in Korean native Ogol chickens. Poult Sci. 2004 Jul;83(7):1203-8.
 
Liu Y, Zi XN, Du YL, Li ZJ, Kang JJ, Gao ZD, Wang K, Dou TF, Jia JJ, Ge CR. Correlation analysis of egg laying performance and curve fitting of egg production rate and cumulative egg production of Chahua chickens. Fujian J Agric Sci. 2021 Dec 28;36(12):1387-94. Chinese with English abstract.
 
Luc KM, Miyoshi S, Suzuki M, Mitsumoto T. Heritability estimates of some clutch traits in the laying hen. Jap Poul Sci. 1996 Jan 25;33(1):23-8.
 
Mishra SK, Chen B, Zhu Q, Xu Z, Ning C, Yin H, Wang Y, Zhao X, Fan X, Yang M, Yang D, Ni Q, Li Y, Zhang M, Li D. Transcriptome analysis reveals differentially expressed genes associated with high rates of egg production in chicken hypothalamic-pituitary-ovarian axis. Sci Rep. 2020 Apr 6;10(1): 8 p.
 
Mu R, Yu YY, Gegen T, Wen D, Wang F, Chen Z, Xu WB. Transcriptome analysis of ovary tissues from low-and high-yielding Changshun green-shell laying hens. BMC Genom. 2021 Dec;22(1): 11 p.
 
Onagbesan O, Bruggeman V, Decuypere E. Intra-ovarian growth factors regulating ovarian function in avian species: A review. Anim Reprod Sci. 2009 Apr 1;111(2-4):121-40.
 
Qin N, Liu Q, Zhang YY, Fan XC, Xu XX, Lv ZC, Wei ML, Jing Y, Mu F, Xu RF. Association of novel polymorphisms of forkhead box L2 and growth differentiation factor-9 genes with egg production traits in local Chinese Dagu hens. Poult Sci. 2015 Jan 1;94(1):88-95. https://doi.org/10.3382/ps/peu023
 
Qin N, Tyasi TL, Sun X, Chen X, Zhu H, Zhao J, Xu R. Determination of the roles of GREM1 gene in granulosa cell proliferation and steroidogenesis of hen ovarian prehierarchical follicles. Theriogenology. 2020 Jul 15;151:28-40.
 
Regan SLP, Knight PG, Yovich JL, Leung Y, Arfuso F, Dharmarajan A. Involvement of bone morphogenetic proteins (BMP) in the regulation of ovarian function. Vitam Horm. 2018 Jan 1;107:227-61.
 
Sun Y, Wu Q, Pan J, Li T, Liu L, Chen D, Zhang X, Chen H, Li Y, Lin R. Identification of differentially expressed genes and signalling pathways in the ovary of higher and lower laying ducks. Br Poult Sci. 2020 Nov 1;61(6):609-14.
 
Tahir MS, Porto-Neto LR, Gondro C, Shittu OB, Wockner K, Tan AWL, Smith HR, Gouveia GC, Kour J, Fortes MRS. Meta-analysis of heifer traits identified reproductive pathways in Bos indicus cattle. Genes. 2021 May 18;12(5): 27 p.
 
Uzumcu M, Pan Z, Chu Y, Kuhn PE, Zachow R. Immunolocalization of the hepatocyte growth factor (HGF) system in the rat ovary and the anti-apoptotic effect of HGF in rat ovarian granulosa cells in vitro. Reproduction. 2006 Aug;132(2):291-9. https://doi.org/10.1530/rep.1.00989
 
Wang C, Ma W. Hypothalamic and pituitary transcriptome profiling using RNA-sequencing in high-yielding and low-yielding laying hens. Sci Rep. 2019 Jul 16;9(1): 11 p.
 
Yang YZ, Yao Y, Cao ZF, Gu TT, Xu Q, Chen GH. Histological characteristics of follicles and reproductive hormone secretion during ovarian follicle development in laying geese. Poult Sci. 2019 Nov 1;98(11):6063-70. https://doi.org/10.3382/ps/pez278
 
Yu G, Wang LG, Han Y, He QY. ClusterProfiler: An R package for comparing biological themes among gene clusters. OMICS. 2012 May 1;16(5):284-7.  https://doi.org/10.1089/omi.2011.0118
 
Zhang T, Chen L, Han K, Zhang X, Zhang G, Dai G, Wang J, Xie K. Transcriptome analysis of ovary in relatively greater and lesser egg producing Jinghai yellow chicken. Anim Reprod Sci. 2019 Sep 1;208: 106114. https://doi.org/10.1016/j.anireprosci.2019.106114
 
Zhu W, Yang M, Shang J, Xu Y, Wang Y, Tao Q, Zhang L, Ding Y, Chen Y, Zhao D, Wang C, Chu M, Yin Z, Zhang X. MiR-222 inhibits apoptosis in porcine follicular granulosa cells by targeting the THBS1 gene. Anim Sci J. 2019 Jun;90(6):719-27.
 
Zou K, Asiamah CA, Lu LL, Liu Y, Pan Y, Chen T, Zhao Z, Su Y. Ovarian transcriptomic analysis and follicular development of Leizhou black duck. Poult Sci. 2020 Nov 1;99(11):6173-87. https://doi.org/10.1016/j.psj.2020.08.008
 
supplementary materialdownload PDF

© 2022 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti