Exploring differentially expressed genes in the ovaries of estrous and anestrous Qira black sheep using RNA-seq technique
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Keywords:
Anestrous, Differentially expressed genes, Estrous, Ovary, Qira black sheepAbstract
Ovary is the main functional organ in reproduction and has obvious difference in the biological activity during the estrous cycle. To investigate the genes associated with follicular development, ovulation, or non-season reproduction, gene expression differences in the ovaries of Qira black sheep estrous stage and anestrous stage in May were assessed using RNA-seq technology. This analysis obtained approximately 1.17 Gb and 1.22 Gb clean reads in Qira black sheep anestrous stage and estrous stage libraries, respectively. Six hundred and fifty one differentially expressed genes (DEGs) were identified, in which 400 genes were up-regulated and 251 genes were down-regulated in the anestrous stage samples compared with estrous stage samples. GO enrichment analysis revealed that these DEGs were significantly enriched in 52 functional groups for the 3 GO categories. Using KEGG pathway analysis, 35 significant signaling pathways were enriched, including calcium signaling pathway, steroid biosynthesis, cell adhesion molecules, and steroid hormone biosynthesis. This study will provide a list of candidate genes for the future research in sheep reproduction.
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Abdou H S, Villeneuve G and Tremblay J J. 2013. The calcium signaling pathway regulates leydig cell steroidogenesis through a transcriptional cascade involving the nuclear receptor NR4A1 and the steroidogenic acute regulatory protein. Endocrinology 154 (1): 511–20. DOI: https://doi.org/10.1210/en.2012-1767
Adib A, Freret S, Touze J L, Lomet D, Lardic L, Chesneau D, Estienne A, Papillier P, Monniaux D and Pellicer-Rubio M T. 2014. Progesterone improves the maturation of male- induced preovulatory follicles in anoestrous ewes. Reproduction 148 (4): 403–16. DOI: https://doi.org/10.1530/REP-14-0263
Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Issel-Tarver L, Kasarskis A, Lewis S, Matese J C, Richardson J E, Ringwald M, Rubin G M and Sherlock G. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25 (1): 25–29. DOI: https://doi.org/10.1038/75556
Audic S and Claverie J M. 1997. The significance of digital gene expression profiles. Genome Research 7(10): 986–95. DOI: https://doi.org/10.1101/gr.7.10.986
Bartlewski P M, Baby T E and Gifin J L. 2011. Reproductive cycles in sheep. Animal Reproduction Science 124 (3–4): 259–68. DOI: https://doi.org/10.1016/j.anireprosci.2011.02.024
Bonnet A, Bevilacqua C, Benne F, Bodin L, Cotinot C, Liaubet L, Sancristobal M, Sarry J, Terenina E, Martin P, Tosser-Klopp G and Mandon-Pepin B. 2011. Transcriptome profiling of sheep granulosa cells and oocytes during early follicular development obtained by Laser Capture Microdissection. BMC Genomics 12: 417. DOI: https://doi.org/10.1186/1471-2164-12-417
Chen H Y, Shen H, Jia B, Zhang Y S, Wang X H and Zeng X C. 2015. Differential gene expression in ovaries of Qira Black sheep and Hetian sheep using RNA-Seq technique. Plos One 10 (3): e0120170. DOI: https://doi.org/10.1371/journal.pone.0120170
Chitwood J L, Rincon G, Kaiser G G, Medrano J F and Ross P J. 2013. RNA-seq analysis of single bovine blastocysts. BMC Genomics 14: 350. DOI: https://doi.org/10.1186/1471-2164-14-350
Garosi P, De Filippo C, van Erk M, Rocca-Serra P, Sansone S A and Elliott R. 2005. Defining best practice for microarray analyses in nutrigenomic studies. British Journal of Nutrition 93 (4): 425–32. DOI: https://doi.org/10.1079/BJN20041385
Hatzirodos N, Irving-Rodgers H F, Hummitzsch K, Harland M L, Morris S E and Rodgers R J. 2014. Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics 15: 24. DOI: https://doi.org/10.1186/1471-2164-15-24
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T and Yamanishi Y. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Research 36 (Database issue): D480–84. DOI: https://doi.org/10.1093/nar/gkm882
Ling Y H, Xiang H, Li Y S, Liu Y, Zhang Y H, Zhang Z J, Ding J P and Zhang X R. 2014. Exploring differentially expressed genes in the ovaries of uniparous and multiparous goats using the RNA-Seq (Quantiûcation) method. Gene 550: 148–53. DOI: https://doi.org/10.1016/j.gene.2014.08.008
Li R, Yu C, Li Y, Lam T W, Yiu S M, Kristiansen K and Wang J 2009. SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics 25 (15): 1966–67. DOI: https://doi.org/10.1093/bioinformatics/btp336
Miao X and Luo Q. 2013. Genome-wide transcriptome analysis between small-tail Han sheep and the Surabaya fur sheep using high-throughput RNA sequencing. Reproduction 145 (6): 587–96. DOI: https://doi.org/10.1530/REP-12-0507
Navanukraw C, Thammasiri J, Moonmanee T and Natthakornkul J. 2014. Expression of vascular endothelial growth factor and hypoxia-inducible factor-1 alpha during the periovulatory period in goats. Turkish Journal of Veterinary and Animal Sciences 38: 699–706. DOI: https://doi.org/10.3906/vet-1404-54
Rico C, Dodelet-Devillers A, Paquet M, Tsoi M, Lapointe E, Carmeliet P and Boerboom D. 2014. HIF1 activity in granulosa cells is required for FSH-regulated Vegfa expression and follicle survival in mice. Biology of Reproduction 90 (6): 135. DOI: https://doi.org/10.1095/biolreprod.113.115634
Saint-Dizier M, Marnier C, Tahir M Z, Grimard B, Thoumire S, Chastant-Maillard S and Reynaud K. 2014. OVGP1 is expressed in the canine oviduct at the time and place of oocyte maturation and fertilization. Molecular Reproduction and Development 81 (11): 972–82. DOI: https://doi.org/10.1002/mrd.22417
Satchell L, Glister C, Bleach E C, Glencross R G, Bicknell A B, Dai Y, Anand-Ivell R, Ivell R and Knight P G. 2013. Ovarian expression of insulin-like peptide 3 (INSL3) and its receptor (RXFP2) during development of bovine antral follicles and corpora lutea and measurement of circulating INSL3 levels during synchronized estrous cycles. Endocrinology 154 (5): 1897–906. DOI: https://doi.org/10.1210/en.2012-2232
Simopoulou M, Nikolopoulou E, Dimakakos A, Charalabopoulos K and Koutsilieris M. 2014. Cell adhesion molecules and in vitro fertilization. In Vivo 28 (5): 683–90.
Sun M K and Xie W. 2012. Cell adhesion molecules in Drosophila synapse development and function. Science China-Life Sciences 55 (1): 20–26. DOI: https://doi.org/10.1007/s11427-012-4273-3
Thompson D L and Oberhaus E L. 2015. Prolactin in the horse: historical perspective, actions and reactions, and its role in reproduction. Journal of Equine Veterinary Science 35 (5): 343–53. DOI: https://doi.org/10.1016/j.jevs.2015.03.199
Wang L, Feng Z, Wang X, Wang X and Zhang X. 2010. DEGseq: an R package for identifying differentially expressed genes from RNA-Seq data. Bioinformatics 26 (1): 136–38. DOI: https://doi.org/10.1093/bioinformatics/btp612
Xue K, Kim J Y, Liu J Y and Tsang B K. 2014. Insulin-like 3– induced rat preantral follicular growth is mediated by growth differentiation factor 9. Endocrinology 155 (1): 156–67. DOI: https://doi.org/10.1210/en.2013-1491
Yang X, Zhao Y, Yang X and Kan F W. 2015. Recombinant hamster oviductin is biologically active and exerts positive effects on sperm functions and sperm-oocyte binding. Plos One 10 (4): e0123003. DOI: https://doi.org/10.1371/journal.pone.0123003
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L and Wang J. 2006. WEGO: a web tool for plotting GO annotations. Nucleic Acids Research 34: W293– 97. DOI: https://doi.org/10.1093/nar/gkl031
Ying S J, Xiao S H, Wang C L, Zhong B S, Zhang G M, Wang Z Y, He D Y, Ding X L, Xing H J and Wang F. 2013. Effect of nutrition on plasma lipid profile and mRNA levels of ovarian genes involved in steroid hormone synthesis in Hu sheep during luteal phase. Journal of Animal Science 91 (1): 5229–39. DOI: https://doi.org/10.2527/jas.2013-6450
Zhao Z Q, Wang L J, Sun X W, Zhang J J, Zhao Y J, Na R S, and Zhang J H. 2015. Transcriptome analysis of the Capra hircus ovary. Plos One 10 (3): e0121586. DOI: https://doi.org/10.1371/journal.pone.0121586
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