{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T17:40:24Z","timestamp":1791222024808,"version":"4.1.0"},"reference-count":58,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,7,8]],"date-time":"2024-07-08T00:00:00Z","timestamp":1720396800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,7,8]],"date-time":"2024-07-08T00:00:00Z","timestamp":1720396800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Genomics"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>The breeder rooster has played a pivotal role in poultry production by providing high-quality semen. Typically, fertility peaks between 30 and 40 weeks of age and then declines rapidly from 45 to 55 weeks of age. Research into improving fertility in aging roosters is essential to extend their productive life. While progress has been made, enhancing fertility in aging roosters remains a significant challenge.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>To identify the genes related to promoting sperm remodeling in aged Houdan roosters, we combined changes in testis and semen quality with transcriptome sequencing (RNA-seq) to analyze the synchrony of semen quality and testis development. In this study, 350-day-old Houdan breeder roosters were selected for RNA-seq analysis in testis tissues from induced molting roosters (D group) and non-induced molting roosters (47DG group). All analyses of differentially expressed genes (DEGs) and functional enrichment were performed. Finally, we selected six DEGs to verify the accuracy of the sequencing by qPCR.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Compared with the 47DG group, sperm motility (\n                      <jats:italic>P\u2009&lt;\u20090.05<\/jats:italic>\n                      ), sperm density (\n                      <jats:italic>P\u2009&lt;\u20090.01<\/jats:italic>\n                      ), and testis weight (\n                      <jats:italic>P\u2009&lt;\u20090.05<\/jats:italic>\n                      ) were significantly increased in roosters in the D group. Further RNA-seq analysis of the testis between the D group and 47DG group identified 61 DEGs, with 21 up-regulated and 40 down-regulated. Functional enrichment analysis showed that the DEGs were primarily enriched in the cytokine-cytokine receptor interaction, Wnt signaling pathway, MAPK signaling pathway, TGF-\u03b2 signaling pathway, and focal adhesion pathway. The qRT-PCR results showed that the expression trend of these genes was consistent with the sequencing results.\n                      <jats:italic>WNT5A<\/jats:italic>\n                      ,\n                      <jats:italic>FGFR3<\/jats:italic>\n                      ,\n                      <jats:italic>AGTR2<\/jats:italic>\n                      ,\n                      <jats:italic>TGF\u03b22<\/jats:italic>\n                      ,\n                      <jats:italic>ROMO1<\/jats:italic>\n                      , and\n                      <jats:italic>SLC26A7<\/jats:italic>\n                      may play a role in testis development and spermatogenesis. This study provides fundamental data to enhance the reproductive value of aging roosters.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12864-024-10544-3","type":"journal-article","created":{"date-parts":[[2024,7,8]],"date-time":"2024-07-08T16:21:55Z","timestamp":1720455715000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Dietary restriction promote sperm remodeling in aged roosters based on transcriptome analysis"],"prefix":"10.1186","volume":"25","author":[{"given":"Wenjie","family":"Liang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuehua","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tingqi","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Binbin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuangxing","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haishan","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pingquan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huayuan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donghua","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangtao","family":"Kang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenting","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2141-913X","authenticated-orcid":false,"given":"Guirong","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,7,8]]},"reference":[{"issue":"10","key":"10544_CR1","doi-asserted-by":"publisher","first-page":"102935","DOI":"10.1016\/j.psj.2023.102935","volume":"102","author":"T Zhu","year":"2023","unstructured":"Zhu T, Liang W, He Y, Zhang B, Liu C, Wang D, Deng L, Li D, Li W, Yan F, et al. Transcriptomic analysis of mechanism underlying the effect of induced molting on semen quality and reproductive performance in aged Houdan roosters. Poult Sci. 2023;102(10):102935.","journal-title":"Poult Sci"},{"issue":"3","key":"10544_CR2","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.domaniend.2013.01.002","volume":"44","author":"N Avital-Cohen","year":"2013","unstructured":"Avital-Cohen N, Heiblum R, Argov-Argaman N, Rosenstrauch A, Chaiseha Y, Mobarkey N, Rozenboim I. Age-related changes in gonadal and serotonergic axes of broiler breeder roosters. Domest Anim Endocrinol. 2013;44(3):145\u201350.","journal-title":"Domest Anim Endocrinol"},{"issue":"8","key":"10544_CR3","doi-asserted-by":"publisher","first-page":"102805","DOI":"10.1016\/j.psj.2023.102805","volume":"102","author":"LBT Oliveira","year":"2023","unstructured":"Oliveira LBT, Butolo JEG, Butolo EAF, Reis RS, Traven\u00e7olo BAN, Beletti ME. L-arginine supplementation minimizes aging-induced changes in the sperm chromatin of roosters. Poult Sci. 2023;102(8):102805.","journal-title":"Poult Sci"},{"issue":"10","key":"10544_CR4","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1071\/RD19420","volume":"32","author":"SD Johnston","year":"2020","unstructured":"Johnston SD, L\u00f3pez-Fern\u00e1ndez C, Pappin E, Hampe A, Doneley R, Lierz M, Gos\u00e1lvez J. Assessment of avian sperm DNA fragmentation using the sperm chromatin dispersion assay. Reprod Fertil Dev. 2020;32(10):948\u201352.","journal-title":"Reprod Fertil Dev"},{"key":"10544_CR5","doi-asserted-by":"publisher","first-page":"106967","DOI":"10.1016\/j.anireprosci.2022.106967","volume":"239","author":"Z Nemati","year":"2022","unstructured":"Nemati Z, Dehgani P, Besharati M, Amirdahri S. Dietary carob fruit (Ceratonia siliqua L.) supplementation improves spermatogenesis, semen quality and embryonic death via antioxidant effect in aging broiler breeder roosters. Anim Reprod Sci. 2022;239:106967.","journal-title":"Anim Reprod Sci"},{"issue":"2","key":"10544_CR6","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1111\/j.1439-0531.2012.02161.x","volume":"48","author":"J Sarabia Fragoso","year":"2013","unstructured":"Sarabia Fragoso J, Pizarro D\u00edaz M, Abad Moreno JC, Casanovas Infesta P, Rodriguez-Bertos A, Barger K. Relationships between fertility and some parameters in male broiler breeders (body and testicular weight, histology and immunohistochemistry of testes, spermatogenesis and hormonal levels). Reprod Domest Anim = Zuchthygiene. 2013;48(2):345\u201352.","journal-title":"Reprod Domest Anim = Zuchthygiene"},{"issue":"11\u201312","key":"10544_CR7","doi-asserted-by":"publisher","first-page":"1679","DOI":"10.1016\/j.exger.2004.06.021","volume":"39","author":"MA Ottinger","year":"2004","unstructured":"Ottinger MA, Abdelnabi M, Li Q, Chen K, Thompson N, Harada N, Viglietti-Panzica C, Panzica GC. The Japanese quail: a model for studying reproductive aging of hypothalamic systems. Exp Gerontol. 2004;39(11\u201312):1679\u201393.","journal-title":"Exp Gerontol"},{"issue":"2","key":"10544_CR8","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1016\/j.cell.2022.11.001","volume":"186","author":"C L\u00f3pez-Ot\u00edn","year":"2023","unstructured":"L\u00f3pez-Ot\u00edn C, Blasco MA, Partridge L, Serrano M, Kroemer G. Hallmarks of aging: an expanding universe. Cell. 2023;186(2):243\u201378.","journal-title":"Cell"},{"key":"10544_CR9","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.theriogenology.2021.12.032","volume":"181","author":"N Ye","year":"2022","unstructured":"Ye N, Lv Z, Huang Z, Cheng Y, Wei Q, Shi F. Dietary folic acid supplementation improves semen quality and spermatogenesis through altering autophagy and histone methylation in the testis of aged broiler breeder roosters. Theriogenology. 2022;181:8\u201315.","journal-title":"Theriogenology"},{"issue":"1","key":"10544_CR10","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1111\/rda.12804","volume":"52","author":"MA Lagares","year":"2017","unstructured":"Lagares MA, Ecco R, Martins N, Lara L, Rocha J, Vilela D, Barbosa VM, Mantovani PF, Braga J, Preis IS, et al. Detecting reproductive system abnormalities of broiler breeder roosters at different ages. Reprod Domest Anim = Zuchthygiene. 2017;52(1):67\u201375.","journal-title":"Reprod Domest Anim = Zuchthygiene"},{"key":"10544_CR11","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.theriogenology.2020.11.020","volume":"161","author":"H Adeldust","year":"2021","unstructured":"Adeldust H, Farzinpour A, Farshad A, Rostamzadeh J, L\u00f3pez B\u00e9jar M. Effect of orally administrated letrozole on reproduction performance and gene expression of FOXJ1, LPR2 and PVRL3 in reproductive tract in aged roosters. Theriogenology. 2021;161:131\u20139.","journal-title":"Theriogenology"},{"issue":"10","key":"10544_CR12","doi-asserted-by":"publisher","first-page":"101908","DOI":"10.1016\/j.psj.2022.101908","volume":"101","author":"R Sabzian-Melei","year":"2022","unstructured":"Sabzian-Melei R, Zare-Shahneh A, Zhandi M, Yousefi AR, Rafieian-Naeini HR. Effects of dietary supplementation of different sources and levels of selenium on the semen quality and reproductive performance in aged broiler breeder roosters. Poult Sci. 2022;101(10):101908.","journal-title":"Poult Sci"},{"issue":"1","key":"10544_CR13","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1095\/biolreprod50.1.129","volume":"50","author":"A Rosenstrauch","year":"1994","unstructured":"Rosenstrauch A, Degen AA, Friedl\u00e4nder M. Spermatozoa retention by sertoli cells during the decline in fertility in aging roosters. Biol Reprod. 1994;50(1):129\u201336.","journal-title":"Biol Reprod"},{"issue":"5","key":"10544_CR14","doi-asserted-by":"publisher","first-page":"1738","DOI":"10.3382\/ps\/pex448","volume":"97","author":"FD Wilson","year":"2018","unstructured":"Wilson FD, Johnson DI, Magee DL, Hoerr FJ. Testicular histomorphometrics including sertoli cell quantitation for evaluating hatchability and fertility issues in commercial breeder-broiler roosters. Poult Sci. 2018;97(5):1738\u201347.","journal-title":"Poult Sci"},{"key":"10544_CR15","doi-asserted-by":"crossref","unstructured":"Gao S, Zhao BX, Long C, Heng N, Guo Y, Sheng XH, Wang XG, Xing K, Xiao LF, Ni HM et al. Natural Astaxanthin Improves Testosterone Synthesis and Sperm Mitochondrial Function in Aging Roosters. Antioxidants (Basel, Switzerland) 2022, 11(9).","DOI":"10.3390\/antiox11091684"},{"issue":"Suppl 4","key":"10544_CR16","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1111\/rda.13058","volume":"52","author":"H Adeldust","year":"2017","unstructured":"Adeldust H, Farzinpour A, Farshad A, Rostamzadeh J, Lopez-Bejar M. Increased sperm cell production in ageing roosters by an oral treatment with an aromatase inhibitor and a natural herbal extract designed for improving fertility. Reprod Domest Anim = Zuchthygiene. 2017;52(Suppl 4):58\u201360.","journal-title":"Reprod Domest Anim = Zuchthygiene"},{"issue":"1","key":"10544_CR17","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1006\/gcen.1999.7276","volume":"115","author":"S Weil","year":"1999","unstructured":"Weil S, Rozenboim I, Degen AA, Dawson A, Friedl\u00e4nder M, Rosenstrauch A. Fertility decline in aging roosters is related to increased testicular and plasma levels of estradiol. Gen Comp Endocrinol. 1999;115(1):23\u20138.","journal-title":"Gen Comp Endocrinol"},{"issue":"1","key":"10544_CR18","doi-asserted-by":"publisher","first-page":"2540","DOI":"10.1038\/s41467-019-10452-1","volume":"10","author":"Y Kiat","year":"2019","unstructured":"Kiat Y, Vortman Y, Sapir N. Feather moult and bird appearance are correlated with global warming over the last 200 years. Nat Commun. 2019;10(1):2540.","journal-title":"Nat Commun"},{"issue":"6","key":"10544_CR19","doi-asserted-by":"publisher","first-page":"971","DOI":"10.1093\/ps\/82.6.971","volume":"82","author":"WD Berry","year":"2003","unstructured":"Berry WD. The physiology of induced molting. Poult Sci. 2003;82(6):971\u201380.","journal-title":"Poult Sci"},{"issue":"5","key":"10544_CR20","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1080\/00071668.2022.2059339","volume":"63","author":"R Mishra","year":"2022","unstructured":"Mishra R, Mishra B, Kim YS, Jha R. Practices and issues of moulting programs for laying hens: a review. Br Poult Sci. 2022;63(5):720\u20139.","journal-title":"Br Poult Sci"},{"key":"10544_CR21","doi-asserted-by":"crossref","unstructured":"Zhang T, Chen Y, Wen J, Jia Y, Wang L, Lv X, Yang W, Qu C, Li H, Wang H et al. Transcriptomic analysis of laying hens revealed the role of aging-related genes during forced molting. Genes 2021, 12(11).","DOI":"10.3390\/genes12111767"},{"issue":"3\u20134","key":"10544_CR22","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/j.anireprosci.2011.06.007","volume":"126","author":"L Laporta","year":"2011","unstructured":"Laporta L, Micera E, Surdo NC, Moramarco AM, Di Modugno G, Zarrilli A. A functional study on L-type calcium channels in granulosa cells of small follicles in laying and forced molt hens. Anim Reprod Sci. 2011;126(3\u20134):265\u201370.","journal-title":"Anim Reprod Sci"},{"issue":"5","key":"10544_CR23","doi-asserted-by":"publisher","first-page":"2757","DOI":"10.1016\/j.psj.2019.12.053","volume":"99","author":"S Huo","year":"2020","unstructured":"Huo S, Li Y, Guo Y, Zhang S, Li P, Gao P. Improving effects of Epimedium flavonoids on the selected reproductive features in layer hens after forced molting. Poult Sci. 2020;99(5):2757\u201365.","journal-title":"Poult Sci"},{"issue":"11","key":"10544_CR24","doi-asserted-by":"publisher","first-page":"1715","DOI":"10.5713\/ajas.19.0180","volume":"32","author":"GP Han","year":"2019","unstructured":"Han GP, Lee KC, Kang HK, Oh HN, Sul WJ, Kil DY. Analysis of excreta bacterial community after forced molting in aged laying hens. Asian-Australasian J Anim Sci. 2019;32(11):1715\u201324.","journal-title":"Asian-Australasian J Anim Sci"},{"issue":"6","key":"10544_CR25","doi-asserted-by":"publisher","first-page":"3713","DOI":"10.1007\/s11250-020-02409-0","volume":"52","author":"EE Onba\u015f\u0131lar","year":"2020","unstructured":"Onba\u015f\u0131lar EE, Kahraman M, G\u00fcng\u00f6r \u00d6F, Kocakaya A, Karakan T, Pirpanahi M, Do\u011fan B, Metin D, Akan M, \u015eehu A, et al. Effects of cage type on performance, welfare, and microbiological properties of laying hens during the molting period and the second production cycle. Trop Anim Health Prod. 2020;52(6):3713\u201324.","journal-title":"Trop Anim Health Prod"},{"issue":"5","key":"10544_CR26","doi-asserted-by":"publisher","first-page":"102589","DOI":"10.1016\/j.psj.2023.102589","volume":"102","author":"MM Meyer","year":"2023","unstructured":"Meyer MM, Bobeck EA. Dietary inositol-stabilized arginine silicate numerically reduced woody breast severity in male Ross 708 broilers without altering growth. Poult Sci. 2023;102(5):102589.","journal-title":"Poult Sci"},{"issue":"4","key":"10544_CR27","doi-asserted-by":"publisher","first-page":"102516","DOI":"10.1016\/j.psj.2023.102516","volume":"102","author":"X Sun","year":"2023","unstructured":"Sun X, Wang Y, Wang C, Wang Y, Ren Z, Yang X, Yang X, Liu Y. Genome analysis reveals hepatic transcriptional reprogramming changes mediated by enhancers during chick embryonic development. Poult Sci. 2023;102(4):102516.","journal-title":"Poult Sci"},{"key":"10544_CR28","doi-asserted-by":"publisher","first-page":"870451","DOI":"10.3389\/fphys.2022.870451","volume":"13","author":"C Surugihalli","year":"2022","unstructured":"Surugihalli C, Farley LS, Beckford RC, Kamkrathok B, Liu HC, Muralidaran V, Patel K, Porter TE, Sunny NE. Remodeling of Hepatocyte Mitochondrial Metabolism and De Novo Lipogenesis during the embryonic-to-neonatal transition in chickens. Front Physiol. 2022;13:870451.","journal-title":"Front Physiol"},{"key":"10544_CR29","doi-asserted-by":"publisher","first-page":"145077","DOI":"10.1016\/j.gene.2020.145077","volume":"766","author":"LX Guo","year":"2021","unstructured":"Guo LX, Nie FR, Huang AQ, Wang RN, Li MY, Deng HY, Zhou YZ, Zhou XM, Huang YK, Zhou J, et al. Transcriptomic analysis of chicken immune response to infection of different doses of Newcastle disease vaccine. Gene. 2021;766:145077.","journal-title":"Gene"},{"issue":"3","key":"10544_CR30","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1038\/s42255-021-00356-0","volume":"3","author":"K Han","year":"2021","unstructured":"Han K, Singh K, Rodman MJ, Hassanzadeh S, Wu K, Nguyen A, Huffstutler RD, Seifuddin F, Dagur PK, Saxena A, et al. Fasting-induced FOXO4 blunts human CD4(+) T helper cell responsiveness. Nat Metabolism. 2021;3(3):318\u201326.","journal-title":"Nat Metabolism"},{"key":"10544_CR31","doi-asserted-by":"crossref","unstructured":"Ezzati A, Rosenkranz SK, Horne BD. Importance of intermittent fasting regimens and selection of adequate therapy on inflammation and oxidative stress in SARS-CoV-2 infection. Nutrients 2022, 14(20).","DOI":"10.3390\/nu14204299"},{"issue":"3","key":"10544_CR32","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1093\/ps\/78.3.419","volume":"78","author":"RP Amann","year":"1999","unstructured":"Amann RP. Lessons for the poultry industry gleaned from experiences with other commodity species. Poult Sci. 1999;78(3):419\u201327.","journal-title":"Poult Sci"},{"key":"10544_CR33","doi-asserted-by":"publisher","first-page":"106573","DOI":"10.1016\/j.domaniend.2020.106573","volume":"74","author":"AA Elokil","year":"2021","unstructured":"Elokil AA, Abouzaid M, Magdy M, Xiao T, Liu H, Xu R, Li S. Testicular transcriptome analysis under the dietary inclusion of l-carnitine reveals potential key genes associated with oxidative defense and the semen quality factor in aging roosters. Domest Anim Endocrinol. 2021;74:106573.","journal-title":"Domest Anim Endocrinol"},{"issue":"4","key":"10544_CR34","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/j.cytogfr.2009.07.007","volume":"20","author":"MW Li","year":"2009","unstructured":"Li MW, Mruk DD, Lee WM, Cheng CY. Cytokines and junction restructuring events during spermatogenesis in the testis: an emerging concept of regulation. Cytokine Growth Factor Rev. 2009;20(4):329\u201338.","journal-title":"Cytokine Growth Factor Rev"},{"issue":"4","key":"10544_CR35","doi-asserted-by":"publisher","first-page":"e1265042","DOI":"10.1080\/21688370.2016.1265042","volume":"4","author":"Q Wen","year":"2016","unstructured":"Wen Q, Tang EI, Xiao X, Gao Y, Chu DS, Mruk DD, Silvestrini B, Cheng CY. Transport of germ cells across the seminiferous epithelium during spermatogenesis-the involvement of both actin- and microtubule-based cytoskeletons. Tissue Barriers. 2016;4(4):e1265042.","journal-title":"Tissue Barriers"},{"issue":"2","key":"10544_CR36","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1093\/humupd\/dms049","volume":"19","author":"X Xiao","year":"2013","unstructured":"Xiao X, Mruk DD, Cheng CY. Intercellular adhesion molecules (ICAMs) and spermatogenesis. Hum Reprod Update. 2013;19(2):167\u201386.","journal-title":"Hum Reprod Update"},{"issue":"1","key":"10544_CR37","first-page":"67","volume":"7","author":"BP Mullaney","year":"1993","unstructured":"Mullaney BP, Skinner MK. Transforming growth factor-beta (beta 1, beta 2, and beta 3) gene expression and action during pubertal development of the seminiferous tubule: potential role at the onset of spermatogenesis. Mol Endocrinol (Baltimore Md). 1993;7(1):67\u201376.","journal-title":"Mol Endocrinol (Baltimore Md)"},{"issue":"1","key":"10544_CR38","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1210\/me.2012-1219","volume":"27","author":"R Hazra","year":"2013","unstructured":"Hazra R, Corcoran L, Robson M, McTavish KJ, Upton D, Handelsman DJ, Allan CM. Temporal role of sertoli cell androgen receptor expression in spermatogenic development. Mol Endocrinol (Baltimore Md). 2013;27(1):12\u201324.","journal-title":"Mol Endocrinol (Baltimore Md)"},{"issue":"1","key":"10544_CR39","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1128\/MMBR.00031-10","volume":"75","author":"M Cargnello","year":"2011","unstructured":"Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biology Reviews: MMBR. 2011;75(1):50\u201383.","journal-title":"Microbiol Mol Biology Reviews: MMBR"},{"issue":"2","key":"10544_CR40","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1152\/physrev.00028.2011","volume":"92","author":"JM Kyriakis","year":"2012","unstructured":"Kyriakis JM, Avruch J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev. 2012;92(2):689\u2013737.","journal-title":"Physiol Rev"},{"key":"10544_CR41","doi-asserted-by":"crossref","unstructured":"Luo D, He Z, Yu C, Guan Q. Role of p38 MAPK Signalling in Testis Development and Male Fertility. Oxidative medicine and cellular longevity 2022, 2022:6891897.","DOI":"10.1155\/2022\/6891897"},{"key":"10544_CR42","doi-asserted-by":"publisher","first-page":"1088249","DOI":"10.3389\/fendo.2023.1088249","volume":"14","author":"D Luo","year":"2023","unstructured":"Luo D, Qi X, Xu X, Yang L, Yu C, Guan Q. Involvement of p38 MAPK in Leydig cell aging and age-related decline in testosterone. Front Endocrinol. 2023;14:1088249.","journal-title":"Front Endocrinol"},{"key":"10544_CR43","doi-asserted-by":"publisher","first-page":"1083401","DOI":"10.3389\/fcell.2023.1083401","volume":"11","author":"C Anerillas","year":"2023","unstructured":"Anerillas C, Alt\u00e9s G, Gorospe M. MAPKs in the early steps of senescence implemEMTation. Front cell Dev Biology. 2023;11:1083401.","journal-title":"Front cell Dev Biology"},{"issue":"3","key":"10544_CR44","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1002\/wdev.176","volume":"4","author":"DM Ornitz","year":"2015","unstructured":"Ornitz DM, Itoh N. The fibroblast growth factor signaling pathway. Wiley Interdisciplinary Reviews Dev Biology. 2015;4(3):215\u201366.","journal-title":"Wiley Interdisciplinary Reviews Dev Biology"},{"issue":"2","key":"10544_CR45","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1016\/j.ydbio.2005.12.034","volume":"291","author":"DP Poladia","year":"2006","unstructured":"Poladia DP, Kish K, Kutay B, Hains D, Kegg H, Zhao H, Bates CM. Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev Biol. 2006;291(2):325\u201339.","journal-title":"Dev Biol"},{"key":"10544_CR46","doi-asserted-by":"crossref","unstructured":"Escasany E, Lanz\u00f3n B, Garc\u00eda-Carrasco A, Izquierdo-Lahuerta A, Torres L, Corrales P, Rodr\u00edguez Rodr\u00edguez AE, Luis-Lima S et al. Mart\u00ednez \u00c1lvarez C, Javier Ruperez F : Transforming growth factor \u03b23 deficiency promotes defective lipid metabolism and fibrosis in murine kidney. Disease models & mechanisms 2021, 14(9).","DOI":"10.1242\/dmm.048249"},{"issue":"1","key":"10544_CR47","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1159\/000510778","volume":"65","author":"F Yang","year":"2022","unstructured":"Yang F, Sun Y, Bai Y, Li S, Huang L, Li X. Asthma promotes Choroidal Neovascularization via the transforming growth factor Beta1\/Smad Signalling Pathway in a mouse model. Ophthalmic Res. 2022;65(1):14\u201329.","journal-title":"Ophthalmic Res"},{"issue":"1","key":"10544_CR48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1095\/biolreprod.111.095232","volume":"86","author":"K Chawengsaksophak","year":"2012","unstructured":"Chawengsaksophak K, Svingen T, Ng ET, Epp T, Spiller CM, Clark C, Cooper H, Koopman P. Loss of Wnt5a disrupts primordial germ cell migration and male sexual development in mice. Biol Reprod. 2012;86(1):1\u201312.","journal-title":"Biol Reprod"},{"issue":"22","key":"10544_CR49","doi-asserted-by":"publisher","first-page":"2517","DOI":"10.1101\/gad.1957710","volume":"24","author":"L Grumolato","year":"2010","unstructured":"Grumolato L, Liu G, Mong P, Mudbhary R, Biswas R, Arroyave R, Vijayakumar S, Economides AN, Aaronson SA. Canonical and noncanonical wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 2010;24(22):2517\u201330.","journal-title":"Genes Dev"},{"issue":"12","key":"10544_CR50","doi-asserted-by":"publisher","first-page":"3121","DOI":"10.1073\/pnas.1701464114","volume":"114","author":"K Kessenbrock","year":"2017","unstructured":"Kessenbrock K, Smith P, Steenbeek SC, Pervolarakis N, Kumar R, Minami Y, Goga A, Hinck L, Werb Z. Diverse regulation of mammary epithelial growth and branching morphogenesis through noncanonical wnt signaling. Proc Natl Acad Sci USA. 2017;114(12):3121\u20136.","journal-title":"Proc Natl Acad Sci USA"},{"issue":"2","key":"10544_CR51","doi-asserted-by":"publisher","first-page":"1689","DOI":"10.1002\/jcb.26329","volume":"119","author":"N He","year":"2018","unstructured":"He N, Wang Y, Zhang C, Wang M, Wang Y, Zuo Q, Zhang Y, Li B. Wnt signaling pathway regulates differentiation of chicken embryonic stem cells into spermatogonial stem cells via Wnt5a. J Cell Biochem. 2018;119(2):1689\u2013701.","journal-title":"J Cell Biochem"},{"issue":"4","key":"10544_CR52","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1002\/(SICI)1097-0177(199808)212:4<522::AID-AJA5>3.0.CO;2-J","volume":"212","author":"E Oreal","year":"1998","unstructured":"Oreal E, Pieau C, Mattei MG, Josso N, Picard JY, Carr\u00e9-Eus\u00e8be D, Magre S. Early expression of AMH in chicken embryonic gonads precedes testicular SOX9 expression. Dev Dynamics: Official Publication Am Association Anatomists. 1998;212(4):522\u201332.","journal-title":"Dev Dynamics: Official Publication Am Association Anatomists"},{"key":"10544_CR53","doi-asserted-by":"crossref","unstructured":"Estermann MA, Major AT, Smith CA. Genetic regulation of Avian Testis Development. Genes 2021, 12(9).","DOI":"10.3390\/genes12091459"},{"issue":"1\u20132\u20133","key":"10544_CR54","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1387\/ijdb.170319cs","volume":"62","author":"CE Hirst","year":"2018","unstructured":"Hirst CE, Major AT, Smith CA. Sex determination and gonadal sex differentiation in the chicken model. Int J Dev Biol. 2018;62(1\u20132\u20133):153\u201366.","journal-title":"Int J Dev Biol"},{"key":"10544_CR55","doi-asserted-by":"crossref","unstructured":"Ortiz-Garc\u00eda CI, Salgado-Lucio ML, Roa-Espitia AL, Mu\u00f1oz-S\u00e1nchez AA, Cordero-Mart\u00ednez J, Hern\u00e1ndez-Gonz\u00e1lez EO. Calpain regulates reactive Oxygen species production during Capacitation through the activation of NOX2 and NOX4. Int J Mol Sci 2023, 24(4).","DOI":"10.3390\/ijms24043980"},{"key":"10544_CR56","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1016\/j.redox.2015.09.009","volume":"6","author":"RM Liu","year":"2015","unstructured":"Liu RM, Desai LP. Reciprocal regulation of TGF-\u03b2 and reactive oxygen species: a perverse cycle for fibrosis. Redox Biol. 2015;6:565\u201377.","journal-title":"Redox Biol"},{"issue":"1","key":"10544_CR57","doi-asserted-by":"publisher","first-page":"50","DOI":"10.2164\/jandrol.106.000182","volume":"28","author":"A Jankowska","year":"2007","unstructured":"Jankowska A, Burczynska B, Duda T, Warchol JB, Sharma RK. Calcium-modulated rod outer segment membrane guanylate cyclase type 1 transduction machinery in the testes. J Androl. 2007;28(1):50\u20138.","journal-title":"J Androl"},{"issue":"4","key":"10544_CR58","first-page":"1105","volume":"7","author":"L Xu","year":"2021","unstructured":"Xu L, Sun X, Wan X, Li K, Jian F, Li W, Jiang R, Han R, Li H, Kang X, et al. Dietary supplementation with Clostridium butyricum improves growth performance of broilers by regulating intestinal microbiota and mucosal epithelial cells. Anim Nutr (Zhongguo Xu Mu Shou Yi Xue Hui). 2021;7(4):1105\u201314.","journal-title":"Anim Nutr (Zhongguo Xu Mu Shou Yi Xue Hui)"}],"container-title":["BMC Genomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-024-10544-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12864-024-10544-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-024-10544-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,8]],"date-time":"2024-07-08T17:01:37Z","timestamp":1720458097000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcgenomics.biomedcentral.com\/articles\/10.1186\/s12864-024-10544-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,8]]},"references-count":58,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["10544"],"URL":"https:\/\/doi.org\/10.1186\/s12864-024-10544-3","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-4287114\/v1","asserted-by":"object"}]},"ISSN":["1471-2164"],"issn-type":[{"value":"1471-2164","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,8]]},"assertion":[{"value":"18 April 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 June 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 July 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All animal experiments were performed according to the Regulations for the Administration of Affairs Concerning Experimental Animals (Ministry of Science and Technology, China, 2004). The protocols and guidelines were approved by the Institutional Animal Care and Use Committee of Henan Agricultural University, China. All sections of this study adhere to the ARRIVE Guidelines for reporting animal research.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"There are no conflicts of interest.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}],"article-number":"680"}}