Pituitary transcriptome profile from laying period to incubation period of Changshun green-shell laying hens.
Changshun green-shell laying hens
Incubation period
Laying period
Pituitary
Transcriptome analysis
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
25 Mar 2024
25 Mar 2024
Historique:
received:
28
09
2023
accepted:
17
03
2024
medline:
26
3
2024
pubmed:
26
3
2024
entrez:
26
3
2024
Statut:
epublish
Résumé
Incubation behaviour, an instinct for natural breeding in poultry, is strictly controlled by the central nervous system and multiple neuroendocrine hormones and neurotransmitters, and is closely associated with the cessation of egg laying. Therefore, it is essential for the commercial poultry industry to clarify the molecular regulation mechanism of incubation behaviour. Here, we used high-throughput sequencing technology to examine the pituitary transcriptome of Changshun green-shell laying hen, a local breed from Guizhou province, China, with strong broodiness, in two reproductive stages, including egg-laying phase (LP) and incubation phase (BP). We also analyze the differences in gene expression during the transition from egg-laying to incubation, and identify critical pathways and candidate genes involved in controlling the incubation behaviour in the pituitary. In this study, we demonstrated that a total of 2089 differently expressed genes (DEGs) were identified in the pituitary, including 842 up-regulated and 1247 down-regulated genes. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that steroid biosynthesis pathway and neuroactive ligand-receptor interaction were significantly enriched based on DEGs commonly identified in pituitary. Further analysis revealed that SRC, ITGB4, ITGB3, PIK3R3 and DRD2 may play crucial roles in the regulation of incubation behaviour. We identified 2089 DEGs and the key signaling pathways which may be closely correlated with incubation in Changshun green-shell laying hens, and clarified the molecular regulation mechanism of incubation behaviour. Our results indicate the complexity and variety of differences in reproductive behaviour of different chicken breeds.
Sections du résumé
BACKGROUND
BACKGROUND
Incubation behaviour, an instinct for natural breeding in poultry, is strictly controlled by the central nervous system and multiple neuroendocrine hormones and neurotransmitters, and is closely associated with the cessation of egg laying. Therefore, it is essential for the commercial poultry industry to clarify the molecular regulation mechanism of incubation behaviour. Here, we used high-throughput sequencing technology to examine the pituitary transcriptome of Changshun green-shell laying hen, a local breed from Guizhou province, China, with strong broodiness, in two reproductive stages, including egg-laying phase (LP) and incubation phase (BP). We also analyze the differences in gene expression during the transition from egg-laying to incubation, and identify critical pathways and candidate genes involved in controlling the incubation behaviour in the pituitary.
RESULTS
RESULTS
In this study, we demonstrated that a total of 2089 differently expressed genes (DEGs) were identified in the pituitary, including 842 up-regulated and 1247 down-regulated genes. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that steroid biosynthesis pathway and neuroactive ligand-receptor interaction were significantly enriched based on DEGs commonly identified in pituitary. Further analysis revealed that SRC, ITGB4, ITGB3, PIK3R3 and DRD2 may play crucial roles in the regulation of incubation behaviour.
CONCLUSIONS
CONCLUSIONS
We identified 2089 DEGs and the key signaling pathways which may be closely correlated with incubation in Changshun green-shell laying hens, and clarified the molecular regulation mechanism of incubation behaviour. Our results indicate the complexity and variety of differences in reproductive behaviour of different chicken breeds.
Identifiants
pubmed: 38528494
doi: 10.1186/s12864-024-10233-1
pii: 10.1186/s12864-024-10233-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
309Subventions
Organisme : Guizhou Provincial Basic Research Program (Natural Science)
ID : ZK[2021]167
Organisme : Guizhou Provincial Basic Research Program (Natural Science)
ID : ZK[2023]455
Organisme : Natural Science Research Project of the Department of Education of Guizhou Province
ID : KY[2020]071
Organisme : Natural Science Research Project of the Department of Education of Guizhou Province
ID : KY[2022]093
Organisme : atural Science Research Project of the Department of Education of Guizhou Province
ID : Innovation team No.2023089
Informations de copyright
© 2024. The Author(s).
Références
Romanov MN, Talbot RT, Wilson PW, Sharp PJ. Genetic control of incubation behavior in the domestic hen. Poult Sci. 2002;81(7):928–31.
pubmed: 12162351
doi: 10.1093/ps/81.7.928
El Halawani ME, Burke WH, Millam JR, Fehrer SC, Hargis BM. Regulation of prolactin and its role in gallinaceous bird reproduction. J Exp Zool. 1984;232:521–9.
pubmed: 6240524
doi: 10.1002/jez.1402320319
Sharp PJ, Scanes CG, Williams JB, Harvey S, Chadwick A. Variations in concentrations of prolactin, luteinizing hormone, growth hormone and progesterone in the plasma of broody bantams (Gallus Domesticus). J Endocrinol. 1979;80:51–7.
pubmed: 429952
doi: 10.1677/joe.0.0800051
Sharp PJ, Macnamee MC, Sterling RJ, Lea RW, Pedersen HC. Relationships between prolactin, LH and broody behaviour in bantam hens. J Endocrinol. 1988;118:279–86.
pubmed: 3171469
doi: 10.1677/joe.0.1180279
Zadworny D, Shimada K, Ishida H, Sumi C, Sato K. Changes in plasma levels of prolactin and estradiol, nutrient intake, and time spent nesting during the incubation phase of broodiness in the Chabo hen (Japanese bantam). Gen Comp Endocrinol. 1988;71:406–12.
pubmed: 3192065
doi: 10.1016/0016-6480(88)90269-9
March JB, Sharp PJ, Wilson PW, Sang HM. Effect of active immunization against recombinant-derived chicken prolactin fusion protein on the onset of broodiness and photoinduced egg laying in bantam hens. J Reprod Fertil. 1994;101:227–33.
pubmed: 8064686
doi: 10.1530/jrf.0.1010227
Sharp PJ, Sterling RJ, Talbot RT, Huskisson NS. The role of hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: observations using passive immunization, radioimmunoassay and immunohistochemistry. J Endocrinol. 1989;122(1):5–13.
pubmed: 2769162
doi: 10.1677/joe.0.1220005
Richard-Yris MA, Sharp PJ, Wauters AM, Guémené D, Richard JP, Forasté M. Inffuence of stimuli from chicks on behavior and concentrations of plasma prolactin and luteinizing hormone in incubating hens. Horm Behav. 1998;33:139–48.
pubmed: 9647939
doi: 10.1006/hbeh.1998.1444
Opel H, Proudman JA. Plasma prolactin levels in incubating Turkey hens during pipping of the eggs and after introduction of poults into the nest. Biol Reprod. 1989;40:981–7.
pubmed: 2765621
doi: 10.1095/biolreprod40.5.981
Lea RW, Richard-Yris MA, Sharp PJ. The effect of ovariectomy on concentrations of plasma prolactin and LH and parental behavior in the domestic fowl. Gen Comp Endocrinol. 1996;101:115–21.
pubmed: 8713650
doi: 10.1006/gcen.1996.0013
Macnamee MC, Sharp PJ, Lea RW, Sterling RJ, Harvey S. Evidence that vasoactive intestinal polypeptide is a physiological prolactin-releasing factor in the bantam hen. Gen Comp Endocrinol. 1986;62:470–8.
pubmed: 3770438
doi: 10.1016/0016-6480(86)90057-2
Opel H, Proudman JA. Stimulation of prolactin release in turkeys by vasoactive intestinal peptide. Proc Soc Exp Biol Med. 1988;187:455–60.
pubmed: 3353394
doi: 10.3181/00379727-187-42688
El Halawani ME, Silsby JL, Mauro LJ. Vasoactive intestinal peptide is a hypothalamic prolactin-releasing neuropeptide in the Turkey (Meleagris gallopavo). Gen Comp Endocrinol. 1990;78:66–73.
pubmed: 2158920
doi: 10.1016/0016-6480(90)90048-Q
Rozenboim I, Silsby JL, Tabibzadeh C, Pitts GR, Youngren OM, el Halawani ME. Hypothalamic and posterior pituitary content of vasoactive intestinal peptide and gonadotropin-releasing hormones I and II in the Turkey hen. Biol Reprod. 1993;49(3):622–6.
pubmed: 8399858
doi: 10.1095/biolreprod49.3.622
Youngren OM, Pitts GR, Phillips RE, el Halawani ME. The stimulatory and inhibitory effects of dopamine on prolactin secretion in the Turkey. Gen Comp Endocrinol. 1995;98:111–7.
pubmed: 7781960
doi: 10.1006/gcen.1995.1049
Youngren OM, Pitts GR, Phillips RE, el Halawani ME. Dopaminergic control of prolactin secretion in the Turkey. Gen Comp Endocrinol. 1996;104:225–30.
pubmed: 8930613
doi: 10.1006/gcen.1996.0165
el Halawani ME, Youngren OM, Rozenboim I, Pitts GR, Silsby JL, Phillips RE. Serotonergic stimulation of prolactin secretion is inhibited by vasoactive intestinal peptide immunoneutralization in the Turkey. Gen Comp Endocrinol. 1995;99(1):69–74.
pubmed: 7657159
doi: 10.1006/gcen.1995.1086
Youngren OM, Silsby JL, Phillips RE, El Halawani ME. Dynorphin modulates prolactin secretion in the Turkey. Gen Comp Endocrinol. 1993;91:224–31.
pubmed: 8104840
doi: 10.1006/gcen.1993.1121
Punnett RC, Bailey PG. Genetic studies in poultry: II. Inheritance of egg-colour and broodiness. J Genet. 1920;10:277–92.
doi: 10.1007/BF02984299
Hays FA. Inheritance of broodiness in Rhode Island Reds. Mass Agr Exp Sta Bull. 1940;377:1–11.
Saeki Y. Inheritance of broodiness in Japanese Nagoya fowl, with special reference to sex-linkage and notice in breeding practice. Poult Sci. 1957;36:378–83.
doi: 10.3382/ps.0360378
Saeki Y, Inoue Y. Body growth, egg production, broodiness, age at ffrst age and egg size in red jungle fowls, and attempt at their genetic analyses by reciprocal crossing with White Leghorns. Jpn Poult Sci. 1979;16:121–5.
doi: 10.2141/jpsa.16.121
Basheer A, Haley CS, Law A, Windsor D, Morrice D, Talbot R, et al. Genetic loci inherited from hens lacking maternal behaviour both inhibit and paradoxically promote this behaviour. Genet Sel Evol. 2015;47:100.
pubmed: 26718134
pmcid: 4697313
doi: 10.1186/s12711-015-0180-y
Tang J, Liu J, Miao X, Li H, Han X, Li L, et al. Comparative study on Nutritional Components in Eggs of Yaoshan Chicken and Changshun Green-Shell Chicken. J Sichuan Agricultural Univ. 2021;57(11):235–8.
Liu H, Wang J, Li L, Han C, He H, Xu H. Transcriptome analysis revealed the possible regulatory pathways initiating female geese broodiness within the hypothalamic-pituitary-gonadal axis. PLoS ONE. 2018;13(2):e0191213.
pubmed: 29408859
pmcid: 5800542
doi: 10.1371/journal.pone.0191213
Ye P, Li M, Liao W, Ge K, Jin S, Zhang C, et al. Hypothalamic transcriptome analysis reveals the neuroendocrine mechanisms in controling broodiness of muscovy duck (Cairina moschata). PLoS ONE. 2019;14(5):e0207050.
pubmed: 31071089
pmcid: 6508920
doi: 10.1371/journal.pone.0207050
Ye P, Ge K, Li M, Yang L, Jin S, Zhang C, et al. Egg-laying and brooding stage-specific hormonal response and transcritptional regulation in pituitary of muscovy duck (Cairina moschata). Poult Sci. 2019;98(11):5287–96.
pubmed: 31376351
doi: 10.3382/ps/pez433
Mishra SK, Chen B, Zhu Q, Xu Z, Ning C, Yin H, et al. Transcriptome analysis reveals differentially expressed genes associated with high rates of egg production in chicken hypothalamic-pituitary-ovarian axis. Sci Rep. 2020;10(1):5976.
pubmed: 32249807
pmcid: 7136225
doi: 10.1038/s41598-020-62886-z
Wang C, Ma W. Hypothalamic and pituitary transcriptome profiling using RNA-sequencing in high-yielding and low-yielding laying hens. Sci Rep. 2019;9(1):10285.
pubmed: 31311989
pmcid: 6635495
doi: 10.1038/s41598-019-46807-3
Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60.
pubmed: 25751142
pmcid: 4655817
doi: 10.1038/nmeth.3317
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33(3):290–5.
pubmed: 25690850
pmcid: 4643835
doi: 10.1038/nbt.3122
Love MI, Huber W, Anders S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11(2):R14.
pubmed: 20132535
pmcid: 2872874
doi: 10.1186/gb-2010-11-2-r14
Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005;21(19):3787–93.
pubmed: 15817693
doi: 10.1093/bioinformatics/bti430
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504.
pubmed: 14597658
pmcid: 403769
doi: 10.1101/gr.1239303
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2– ∆∆CT method. Methods. 2001;25(4):402–8.
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Riddle O, Bates RW, Lahr EL. Prolactin induces broodiness in fowl. Am J Physiol. 1935;111:352–60.
doi: 10.1152/ajplegacy.1935.111.2.352
Riddle O, Bates RW, Dykshorn SW. The preparation, identification and assay of prolactin—a hormone of the anterior pituitary. Am J Physiol. 1933;105:191–216.
doi: 10.1152/ajplegacy.1933.105.1.191
Kuwayama T, Shimada K, Saito N, Ohkubo T, Sato K, Wada M, et al. Effects of removal of chicks from hens on concentrations of prolactin, luteinizing hormone and oestradiol in plasma of brooding Gifujidori hens. J Reprod Fertil. 1992;95(2):617–22.
pubmed: 1518016
doi: 10.1530/jrf.0.0950617
Porter TE, Hargis BM, Silsby JL, el Halawani ME. Enhanced progesterone and testosterone secretion and depressed estradiol secretion in vitro from small white follicle cells of incubating Turkey hens. Gen Comp Endocrinol. 1989;74(3):400–5.
pubmed: 2744409
doi: 10.1016/S0016-6480(89)80037-1
Lv C, Zheng H, Jiang B, Ren Q, Zhang J, Zhang X, et al. Characterization of relaxin 3 and its receptors in chicken: evidence for relaxin 3 acting as a novel pituitary hormone. Front Physiol. 2022;13:1010851.
pubmed: 36419837
pmcid: 9676923
doi: 10.3389/fphys.2022.1010851
Smith CM, Ryan PJ, Hosken IT, Ma S, Gundlach AL. Relaxin-3 systems in the brain–the first 10 years. J Chem Neuroanat. 2011;42(4):262–75.
pubmed: 21693186
doi: 10.1016/j.jchemneu.2011.05.013
Watanabe Y, Miyamoto Y, Matsuda T, Tanaka M. Relaxin-3/INSL7 regulates the stress-response system in the rat hypothalamus. J Mol Neurosci. 2010;43:169–74.
pubmed: 21072619
doi: 10.1007/s12031-010-9468-0
McGowan BM, Stanley SA, Ghatei MA, Bloom SR. Relaxin-3 and its role in neuroendocrine function. Ann N Y Acad Sci. 2009;1160:250–5.
pubmed: 19416197
doi: 10.1111/j.1749-6632.2008.03796.x
Higgins SE, Ellestad LE, Trakooljul N, McCarthy F, Saliba J, Cogburn LA, et al. Transcriptional and pathway analysis in the hypothalamus of newly hatched chicks during fasting and delayed feeding. BMC Genomics. 2010;11:162.
pubmed: 20214824
pmcid: 2848243
doi: 10.1186/1471-2164-11-162
McGowan BM, Stanley SA, Smith KL, White NE, Connolly MM, Thompson EL, et al. Central relaxin-3 administration cuasese hyperphagia in male Wistar rats. Endocrinology. 2005;146:3295–300.
pubmed: 15845619
doi: 10.1210/en.2004-1532
McGowan BM, Stanley SA, Smith KL, Minnion JS, Donovan J, Thompson EL, et al. Effects of acute and chronic relaxin-3 on food intake and energy expenditure in rats. Regul Pept. 2006;136:72–7.
pubmed: 16764952
doi: 10.1016/j.regpep.2006.04.009
Shen X, Bai X, Xu J, Zhou M, Xu H, Nie Q, et al. Transcriptome sequencing reveals genetic mechanisms underlying the transition between the laying and brooding phases and gene expression changes associated with divergent reproductive phenotypes in chickens. Mol Biol Rep. 2016;43(9):977–89.
pubmed: 27389590
doi: 10.1007/s11033-016-4033-8
McGowan BM, Stanley SA, Donovan J, Thompson EL, Patterson M, Semjonous NM, et al. Relaxin-3 stimulates the hypothalamic-pituitary-gonadal axis. Am J Physiol Endocrinol Metab. 2008;295(2):E278–86.
pubmed: 18492777
pmcid: 2519759
doi: 10.1152/ajpendo.00028.2008
Mo C, Huang L, Cui L, Lv C, Lin D, Song L, et al. Characterization of NMB, GRP and their receptors (BRS3, NMBR and GRPR) in chickens. J Mol Endocrinol. 2017;59(1):61–79.
pubmed: 28500250
doi: 10.1530/JME-17-0020
Tachibana T, Matsuda K, Khan SI, Ueda H, Cline MA. Feeding and drinking response following central administrations of bombesin-like peptides in chicks. Comp Biochem Physiol Mol Integr Physiol. 2010;156(4):394–9.
doi: 10.1016/j.cbpa.2010.03.008
Tachibana T, Matsuda K, Sawa H, Mikami A, Ueda H, Cline MA. Differential thresholds of neuromedins B-, C-, and bombesin-induced anorexia and crop-emptying rate in chicks. Gen Comp Endocrinol. 2010;169(2):144–50.
pubmed: 20727356
doi: 10.1016/j.ygcen.2010.08.006
Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature. 2007;448(7154):700–3.
pubmed: 17653196
doi: 10.1038/nature06029
Sun YG, Zhao ZQ, Meng XL, Yin J, Liu XY, Chen ZF. Cellular basis of itch sensation. Science. 2009;325(5947):1531–4.
pubmed: 19661382
doi: 10.1126/science.1174868
Campbell BJ, Garner A, Dockray GJ, Hughes J, Dimaline R. The mechanism of action of gastrin releasing peptide (GRP) in stimulating avian gastric acid secretion. Regul Pept. 1994;49(3):249–55.
pubmed: 8140277
doi: 10.1016/0167-0115(94)90147-3
Linari G, Linari MB. Effect of bombesin on pancreatic secretion and gall bladder motility of the chicken. Eur J Pharmacol. 1975;34(2):305–10.
pubmed: 1234549
doi: 10.1016/0014-2999(75)90256-3
Kallingal GJ, Mintz EM. Gastrin releasing peptide and neuropeptide Y exert opposing actions on circadian phase. Neurosci Lett. 2007;422(1):59–63.
pubmed: 17597298
pmcid: 1993851
doi: 10.1016/j.neulet.2007.06.003
Mallet D, Bretones P, Michel-Calemard L, Dijoud F, David M, Morel Y. Gonadal dysgenesis without adrenal insufficiency in a 46, XY patient heterozygous for the nonsense C16X mutation: a case of SF1 haploinsufficiency. J Clin Endocrinol Metab. 2004;89(10):4829–32.
pubmed: 15472171
doi: 10.1210/jc.2004-0670
Hasegawa T, Fukami M, Sato N, Katsumata N, Sasaki G, Fukutani K, et al. Testicular dysgenesis without adrenal insufficiency in a 46,XY patient with a heterozygous inactive mutation of steroidogenic factor-1. J Clin Endocrinol Metab. 2004;89(12):5930–5.
pubmed: 15579739
doi: 10.1210/jc.2004-0935
Jameson JL. Of mice and men: the tale of steroidogenic factor-1. J Clin Endocrinol Metab. 2004;89(12):5927–9.
pubmed: 15579738
doi: 10.1210/jc.2004-2047
Li X, Ye J, Han X, Qiao R, Li X, Lv G, et al. Whole-genome sequencing identifies potential candidate genes for reproductive traits in pigs. Genomics. 2020;112(1):199–206.
pubmed: 30707936
doi: 10.1016/j.ygeno.2019.01.014
Divya D, Bhattacharya TK. Bone morphogenetic proteins (BMPs) and their role in poultry. Worlds Poult Sci J. 2021;77:539–64.
doi: 10.1080/00439339.2021.1959274
Yan X, Liu H, Hu J, Han X, Qi J, Ouyang Q, et al. Transcriptomic analyses of the HPG axis-related tissues reveals potential candidate genes and regulatory pathways associated with egg production in ducks. BMC Genomics. 2022;23(1):281.
pubmed: 35395713
pmcid: 8991983
doi: 10.1186/s12864-022-08483-y
Li QH, Yu ZQ, Chen Z. Effect of heat stress on mitogen-activated protein kinases in the hypothalamic-pituitary-gonadal axis of developing Wenchang chicks. Poult Sci. 2020;99(1):567–77.
pubmed: 32416843
doi: 10.3382/ps/pez499
Dunayevich P, Baltanás R, Clemente JA, Couto A, Sapochnik D, Vasen G, et al. Heat-stress triggers MAPK crosstalk to turn on the hyperosmotic response pathway. Sci Rep. 2018;8(1):15168.
pubmed: 30310096
pmcid: 6181916
doi: 10.1038/s41598-018-33203-6