Please wait a minute...
Journal of Integrative Agriculture  2025, Vol. 24 Issue (2): 697-711    DOI: 10.1016/j.jia.2023.05.026
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken
Yuanmei Wang*, Jingwei Yuan*, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen#

State Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China

 Highlights 
The non-additivity was the major expression pattern of ovarian circRNA in crossbred chicken.
Non-additive circRNAs, which were mainly exons-derived, contributed to the formation of sexual maturation heterosis through involving in oocyte development related process in chicken.
Non-additive circRNAs gal-FGFR2_0005 and gal-MAPKAP1_0004 could contribute to sexual maturation heterosis through modulating CNOT6, COL8A1, and FHL2 by interactions with gga-miR-1612 and gga-miR-12235-5p.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

性成熟杂种优势已在动物杂交育种中广泛使用,但鸡性成熟杂种优势分子机理尚未揭示清楚。本研究以白来航鸡和北京油鸡为亲本构建完全双列杂交群体测定纯繁WWYY和正反交WYYW组合四个群体性成熟相关性状。通过分析纯繁和正反交组合卵巢circRNA表达谱解析性成熟杂种优势潜在的分子机理。研究发现正反交组合耻骨间距、输卵管长度和见蛋日龄均表现为杂种优势。我们在四个组合卵巢中共鉴定到3,649circRNA,其中包括3,025个已知circRNAs624个新circRNAs,这些circRNA主要为外显子类型。WYYW组合中特异性表达circRNAs分别为141178通过对鉴定circRNAs进行差异分析和表达模式分析,发现WYYW组合中非加性表达circRNAs分别占其总鉴定circRNA52.38%64.63%GOKEGG功能富集分析结果显示非加性效应circRNAs来源基因主要参与TGF-beta信号通路,卵母细胞生长发育,ATP酶激活活性,卵母细胞有丝分裂,孕酮调控卵母细胞成熟和GnRH信号通路。通过加权共表达网络分析共鉴定到四个模块与输卵管长度和耻骨间距显著相关。这四个模块中的非加性表达circRNAs主要参与MAPK信号通路和Wnt信号通路。我们进一步对非加性circRNA进行竞争性RNAceRNA网络分析鉴定到gall-FGFR2_0005gal-MAPKAP1_0004可与miRNA gga-miR-1612gga-miR-12235-5p竞争性结合进而调控基因CNOT6COL8A1FHL2非加性表达,参与卵巢的发育过程。以上结果表明非加性效应circRNAs通过调控繁殖和发育过程相关基因促进性成熟杂种优势的形成。该研究首次从circRNA水平揭示了鸡性成熟杂种优势形成的潜在分子机理,丰富畜禽杂种优势分子机理探究及杂种优势科学应用提供理论基础



Abstract  
Sexual maturation heterosis has been widely exploited in animal crossbreeding.  However, the underlying mechanism has been rarely explored in chicken.  In the present study, we performed the reciprocal crossing between White Leghorn and Beijing You chicken to evaluate the phenotypes related to sexual maturation, and profiled the ovary circRNAs of purebreds (WW, YY) and crossbreds (WY, YW) to elucidate the molecular mechanism underlying heterosis for sexual maturation.  Pubic space and oviduct length exhibited positive heterosis, and age at first egg (AFE) exhibited negative heterosis in the crossbreds.  We identified 3,025 known circRNAs and 624 putative circRNAs, which were mainly derived from the exons.  Among these circRNAs, 141 and 178 circRNAs were specially expressed in WY and YW, respectively.  There were 52.38 and 64.63% of total circRNAs in WY and YW exhibited non-additive expression pattern, respectively.  GO enrichment and KEGG pathway analysis showed that the host genes of non-additive circRNAs were mainly involved in TGF-beta signaling pathway, oocyte development, ATPase activator activity, oocyte meiosis, progesterone-mediated oocyte maturation and GnRH signaling pathway.  Weighted gene co-expression network analysis identified that 4 modules were significantly (P<0.05) correlated with oviduct length and pubic space.  The host genes of non-additive circRNAs harbored in the 4 modules were associated with MAPK signaling pathway and Wnt signaling pathway.  Furthermore, competing endogenous RNAs (ceRNA) network analysis characterized non-additive circRNAs gal-FGFR2_0005 and gal-MAPKAP1_0004 could interact with gga-miR-1612 and gga-miR-12235-5p to regulate CNOT6, COL8A1, and FHL2, which were essential for ovary development, indicating that the non-additive circRNAs involved in the formation of sexual maturation heterosis through regulating genes related to the reproductive and developmental process.  The findings would provide a deeper understanding of the molecular mechanism underlying sexual maturation heterosis from a novel perspective.


Keywords:  chicken        sexual maturation        heterosis        ovary        circRNA  
Received: 19 January 2023   Accepted: 17 April 2023
Fund: 

This research was funded by the National Natural Science Foundation of China (32172721), China Agriculture Research System (CARS-40), Central Public-interest Scientific Institution Basal Research Fund (2021-YWF-ZYSQ-12) and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP-IAS04).

About author:  Yuanmei Wang, E-mail: ymwang062723@163.com; Jingwei Yuan, E-mail: yuanjingwei@caas.cn; #Correspondence Jilan Chen, E-mail: Chen.jilan@163.com * These authors contribute equally to this study.

Cite this article: 

Yuanmei Wang, Jingwei Yuan, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen. 2025. Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken. Journal of Integrative Agriculture, 24(2): 697-711.

Abdelmohsen K, Panda A C, De S, Grammatikakis I, Kim J, Ding J, Noh J H, Kim K M, Mattison J A, de Cabo R, Gorospe M. 2015. Circular RNAs in monkey muscle: Age-dependent changes. Aging, 7, 903–910.

Ahmed S M, Hassan K M, El-Sabrout K, Kamel S M. 2020. Crossing effect for improving egg production traits in chickens involving local and commercial strains. Veterinary World13, 407–412.

Berisha B, Welter H, Shimizu T, Miyamoto A, Meyer H H, Schams D. 2006. Expression of fibroblast growth factor 1 (FGF1) and FGF7 in mature follicles during the periovulatory period after GnRH in the cow. The Journal of Reproduction and Development, 52, 307–313.

Bu D, Luo H, Huo P, Wang Z, Zhang S, He Z, Wu Y, Zhao L, Liu J, Guo J, Fang S, Cao W, Yi L, Zhao Y, Kong L. 2021. KOBAS-i: Intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Research, 49, W317–W325.

Budna J, Chachuła A, Kaźmierczak D, Rybska M, Ciesiółka S, Bryja A, Kranc W, Borys S, Żok A, Bukowska D, Antosik P, Bruska M, Brüssow K P, Nowicki M, Zabel M, Kempisty B. 2017. Morphogenesis-related gene-expression profile in porcine oocytes before and after in vitro maturation. Zygote, 25, 331–340.

Castilho A C, Nogueira M F, Fontes P K, Machado M F, Satrapa R A, Razza E M, Barros CM. 2014. Ovarian superstimulation using FSH combined with equine chorionic gonadotropin (eCG) upregulates mRNA-encoding proteins involved with LH receptor intracellular signaling in granulosa cells from Nelore cows. Theriogenology, 82, 1199–1205.

Chen Z J. 2013. Genomic and epigenetic insights into the molecular bases of heterosis. Nature reviews. Genetics, 14, 471–482.

Cui Y M, Wang J, Hai J Z, Feng J, Wu S G, Qi G H. 2019. Effect of photoperiod on ovarian morphology, reproductive hormone secretion, and hormone receptor mRNA expression in layer ducks during the pullet phase. Poultry Science, 98, 2439–2447.

Cui Z, Ning Z, Deng X, Du X, Amevor F K, Liu L, Kang X, Tian Y, Wang Y, Li D, Zhao X. 2022. Integrated proteomic and metabolomic analyses of chicken ovary revealed the crucial role of lipoprotein lipase on lipid metabolism and steroidogenesis during sexual maturity. Frontiers in Physiology, 13, 885030.

Dai X X, Jiang Z Y, Wu Y W, Sha Q Q, Liu Y, Ding J Y, Xi W D, Li J, Fan H Y. 2021. CNOT6/6L-mediated mRNA degradation in ovarian granulosa cells is a key mechanism of gonadotropin-triggered follicle development. Cell Reports, 37, 110007.

Dietzel E, Weiskirchen S, Floehr J, Horiguchi M, Todorovic, V, Rifkin, D B, Jahnen D W, Weiskirchen R. 2017. Latent TGF-β binding protein-1 deficiency decreases female fertility. Biochemical and Biophysical Research Communications, 482, 1387–1392.

Drews F, Knöbel S, Moser M, Muhlack K G, Mohren S, Stoll C, Bosio A, Gressner A M, Weiskirchen R. 2008. Disruption of the latent transforming growth factor-beta binding protein-1 gene causes alteration in facial structure and influences TGF-beta bioavailability. Biochimica et Biophysica Acta, 1783, 34–48.

Elling R, Chan J, Fitzgerald K A. 2016. Emerging role of long noncoding RNAs as regulators of innate immune cell development and inflammatory gene expression. European Journal of Immunology, 46, 504–512.

Farghly M F A, Mahrose K M, Rehman Z U, Yu, S, Abdelfattah M G, El-Garhy O H. 2019. Intermittent lighting regime as a tool to enhance egg production and eggshell thickness in Rhode Island Red laying hens. Poultry Science, 98, 2459–2465.

Feibelmann T C, Silva A P, Resende D C, Resende E A, Scatena L M, Borges Mde F. 2015. Puberty in a sample of Brazilian schoolgirls: Timing and anthropometric characteristics. Archives of Endocrinology and Metabolism, 59, 105–111.

Fischer J W, Leung A K. 2017. CircRNAs: A regulator of cellular stress. Critical Reviews in Biochemistry and Molecular Biology, 52, 220–233.

França M M, Mendonca B B. 2022. Genetics of ovarian insufficiency and defects of folliculogenesis. Best Practice & Research Clinical Endocrinology & Metabolism, 36, 101594.

Gao Y, Li S, Lai Z, Zhou Z, Wu F, Huang Y, Lan X, Lei C, Chen H, Dang R. 2019. Analysis of long non-coding RNA and mRNA expression profiling in immature and mature bovine (Bos taurus) testes. Frontiers in Genetics, 10, 646.

Gao Y, Wang J, Zhao F. 2015. CIRI: An efficient and unbiased algorithm for de novo circular RNA identification. Genome Biology, 16, 4.

Gao Y, Wu M, Fan Y, Li S, Lai Z, Huang Y, Lan X, Lei C, Chen H, Dang R. 2018. Identification and characterization of circular RNAs in Qinchuan cattle testis. Royal Society Open Science, 5, 180413.

Geach T. 2016. Neuroendocrinology: MicroRNAs regulate puberty timing. Nature Reviews Endocrinology, 12, 372.

Gu J, Su C, Huang F, Zhao Y, Li J. 2022. Past, present and future: The relationship between circular RNA and immunity. Frontiers in Immunology13, 894707.

Haberfeld A, Dunnington E A, Siegel P B, Hillel J. 1996. Heterosis and DNA fingerprinting in chickens. Poultry Science, 75, 951–953.

Hansen T B, Jensen T I, Clausen B H, Bramsen J B, Finsen B, Damgaard C K, Kjems J. 2013. Natural RNA circles function as efficient microRNA sponges. Nature495, 384–389.

Huang C, Ge F, Ma X, Dai R, Dingkao R, Zhaxi Z, Burenchao, G, Bao P, Wu X, Guo X, Chu M, Yan P, Liang C. 2021. Comprehensive analysis of mRNA, lncRNA, circRNA, and miRNA expression profiles and their ceRNA networks in the longissimus dorsi muscle of cattle-yak and yak. Frontiers in Genetics, 12, 772557.

Isa A M, Sun Y, Li Y, Wang Y, Ni A, Yuan J, Ma H, Shi L, Tesfay H H, Fan J, Wang P, Chen J. 2022. MicroRNAs with non-additive expression in the ovary of hybrid hens target genes enriched in key reproductive pathways that may influence heterosis for egg laying traits. Frontiers in Genetics, 13, 974619.

Isa A M, Sun Y, Shi L, Jiang L, Li Y, Fan J, Wang P, Ni A, Huang Z, Ma H, Li D, Chen J. 2020. Hybrids generated by crossing elite laying chickens exhibited heterosis for clutch and egg quality traits. Poultry Science, 99, 6332–6340.

Jeck W R, Sharpless N E. 2014. Detecting and characterizing circular RNAs. Nature Biotechnology, 32, 453–461.

Kezele P, Nilsson E E, Skinner M K. 2005. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biology of Reproduction, 73, 967–973.

Kristensen L S, Andersen M S, Stagsted L V W, Ebbesen K K, Hansen T B, Kjems J. 2019. The biogenesis, biology and characterization of circular RNAs. Nature reviews. Genetics, 20, 675–691.

Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.

Li J, Shi B, Wang C, Shao C, Liu X, Zhang D. 2021. Comprehensive circRNA profiling and selection of key circRNAs reveal the potential regulatory roles of circRNAs throughout ovarian development and maturation in cynoglossus semilaevis. Biology, 10, 830.

Li M, Liu Y, Zhang X, Liu J, Wang P. 2018. Transcriptomic analysis of high-throughput sequencing about circRNA, lncRNA and mRNA in bladder cancer. Gene, 677, 189–197.

Li Q. 2015. Inhibitory SMADs: Potential regulators of ovarian function. Biology of Reproduction, 92, 50.

Li Q, Pan X, Li N, Gong W, Chen Y, Yuan X. 2021. Identification of circular RNAs in hypothalamus of gilts during the onset of puberty. Genes, 12, 84.

Liu W, Zhang Y, He H, He G, Deng X W. 2022. From hybrid genomes to heterotic trait output: Challenges and opportunities. Current Opinion in Plant Biology, 66, 102193.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Luo Z, Qian J, Chen S, Li L. 2020. Dynamic patterns of circular and linear RNAs in maize hybrid and parental lines. TAG. Theoretical and applied genetics. Theoretical and Applied Genetics, 133, 593–604.

Mai C, Wen C, Xu Z, Xu G, Chen S, Zheng J, Sun C, Yang N. 2021. Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis. Journal of Animal Science and Biotechnology, 12, 52.

Matulis C K, Mayo K E. 2012. The LIM domain protein FHL2 interacts with the NR5A family of nuclear receptors and CREB to activate the inhibin-α subunit gene in ovarian granulosa cells. Molecular and Cellular Endocrinology26, 1278–1290.

Melo T P, Fortes M R S, Fernandes Junior G A, Albuquerque L G, Carvalheiro R. 2019. RAPID COMMUNICATION: Multi-breed validation study unraveled genomic regions associated with puberty traits segregating across tropically adapted breeds. Journal of Animal Science, 97, 3027–3033.

Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak S D, Gregersen L H, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N. 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 495, 333–338.

Meng S, Zhou H, Feng Z, Xu Z, Tang Y, Li P, Wu M. 2017. CircRNA: Functions and properties of a novel potential biomarker for cancer. Molecular Cancer, 16, 94.

Pan X, Gong W, He Y, Li N, Zhang H, Zhang Z, Li J, Yuan X. 2021. Ovary-derived circular RNAs profile analysis during the onset of puberty in gilts. BMC Genomics, 22, 445.

Pan X Y, Zhang Z H, Wu L X, Wang Z C. 2015. Effect of HIF-1a/VEGF signaling pathway on plasma progesterone and ovarian prostaglandin F2a secretion during luteal development of pseudopregnant rats. Genetics and Molecular Research14, 8796–8809.

Pan Z, Zhang J, Li Q, Li Y, Shi F, Xie Z, Liu H. 2012. Current advances in epigenetic modification and alteration during mammalian ovarian folliculogenesis. Journal of Genetics and Genomics39, 111–123.

Perkel J M. 2021. Ten computer codes that transformed science. Nature, 589, 344–348.

Prevot V, Lomniczi A, Corfas G, Ojeda S R. 2005. erbB-1 and erbB-4 receptors act in concert to facilitate female sexual development and mature reproductive function. Endocrinology, 146, 1465–1472.

Ro S, Song R, Park C, Zheng H, Sanders K M, Yan W. 2007. Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA, 13, 2366–2380.

Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, Herzog M, Schreyer L, Papavasileiou P, Ivanov A, Öhman M, Refojo D, Kadener S, Rajewsky N. 2015. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Molecular Cell, 58, 870–885.

Sauvegarde C, Paul D, Bridoux L, Jouneau A, Degrelle S, Hue I, Rezsohazy R, Donnay I. 2016. Dynamic pattern of HOXB9 protein localization during oocyte maturation and early embryonic development in mammals. PLoS ONE, 11, e0165898.

Schütz L F, Hemple A M, Morrell B C, Schreiber N B, Gilliam J N, Cortinovis C, Totty M L, Caloni F, Aad P Y, Spicer L J. 2022. Changes in fibroblast growth factor receptors-1c, -2c, -3c, and -4 mRNA in granulosa and theca cells during ovarian follicular growth in dairy cattle. Domestic Animal Endocrinology, 80, 106712.

Sekulovski N, Whorton A E, Shi M, Hayashi K, MacLean J A. 2020. Periovulatory insulin signaling is essential for ovulation, granulosa cell differentiation, and female fertility. FASEB Journal34, 2376–2391.

Seymour D K, Chae E, Grimm D G, Martín P C, Habring-Müller A, Vasseur F, Rakitsch B, Borgwardt K M, Koenig D, Weigel D. 2016. Genetic architecture of nonadditive inheritance in Arabidopsis thaliana hybrids. Proceedings of the National Academy of Sciences of the United States of America, 113, e7317–e7326.

Sha Q Q, Yu J L, Guo J X, Dai X X, Jiang J C, Zhang Y L, Yu C, Ji S Y, Jiang Y, Zhang S Y, Shen L, Ou X H, Fan H Y. 2018. CNOT6L couples the selective degradation of maternal transcripts to meiotic cell cycle progression in mouse oocyte. The EMBO Journal37, e99333.

Shen M, Li T, Zhang G, Wu P, Chen F, Lou Q, Chen L, Yin X, Zhang T, Wang J. 2019. Dynamic expression and functional analysis of circRNA in granulosa cells during follicular development in chicken. BMC Genomics, 20, 96.

Shen M, Wu P, Li T, Wu P, Chen F, Chen L, Xie K, Wang J, Zhang G. 2020. Transcriptome analysis of circRNA and mRNA in theca cells during follicular development in chickens. Genes, 11, 489.

Shu H Y, Zhou H, Mu H L, Wu S H, Jiang Y L, Yang Z, Hao Y Y, Zhu J, Bao W L, Cheng S H, Zhu G P, Wang Z W. 2021. Integrated analysis of mRNA and non-coding RNA transcriptome in pepper (Capsicum chinense) hybrid at seedling and flowering stages. Frontiers in Genetics, 12, 685788.

Swanson-Wagner R A, Jia Y, DeCook R, Borsuk L A, Nettleton D, Schnable P S. 2006. All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proceedings of the National Academy of Sciences of the United States of America, 103, 6805–6810.

Tian W, Zhang B, Zhong H, Nie R, Ling Y, Zhang H, Wu C. 2021. Dynamic expression and regulatory network of circular RNA for abdominal preadipocytes differentiation in chicken (Gallus gallus). Frontiers in Cell and Developmental Biology, 9, 761638.

Di Timoteo, G, Rossi F, Bozzoni I. 2020. Circular RNAs in cell differentiation and development. Development (Cambridge, England), 147, dev182725.

Vromman M, Vandesompele J, Volders P J. 2021. Closing the circle: Current state and perspectives of circular RNA databases. Briefings in Bioinformatics, 22, 288–297.

Wang H, Zhang Y, Sun D Y Y. 2005. Relationship between differential gene expression patterns in chicken ovary and heterosis of egg number in a chicken diallel cross. Chinese Journal of Animal Veterinary Science, 36, 111–115.

Wang J, Ren Q, Hua L, Chen J, Zhang J, Bai H, Li H, Xu B, Shi Z, Cao H, Xing B, Bai X. 2019. Comprehensive analysis of differentially expressed mrna, lncrna and circrna and their ceRNA networks in the longissimus dorsi muscle of two different pig breeds. International Journal of Molecular Sciences, 20, 1107.

Wang J, Zhuo Z, Ma X, Liu Y, Xu J, He C, Fu Y, Wang F, Ji P, Zhang L, Liu G. 2021. Melatonin alleviates the suppressive effect of hypoxanthine on oocyte nuclear maturation and restores meiosis via the melatonin receptor 1 (MT1)-mediated pathway. Frontiers in Cell and Developmental Biology, 9, 648148.

Wang X, Qin T, Peng Z, Zhang Y, Yang Q, Geng X, Salih H, Sun J, He S, Wang Q J I C. 2021. Genome-wide profiling of circular RNAs in the hybridization of two elite inbred lines of Gossypium hirsutumIndustrial Crops and Products170, 113754.

Wang Y, Yuan J, Sun Y, Li Y, Wang P, Shi L, Ni A, Zong Y, Zhao J, Bian S, Ma H, Chen J. 2022. Genetic basis of sexual maturation heterosis: Insights from ovary lncRNA and mRNA repertoire in chicken. Frontiers in Endocrinology, 13, 951534.

Wu W, Ji P, Zhao F. 2020 CircAtlas: An integrated resource of one million highly accurate circular RNAs from 1070 vertebrate transcriptomes. Genome Biology21, 101.

Wu X, Li R, Li Q, Bao H, Wu C. 2016. Comparative transcriptome analysis among parental inbred and crosses reveals the role of dominance gene expression in heterosis in Drosophila melanogasterScientific Reports, 6, 21124.

Wu Z, Zhang W. 1983. Heterosis and statistical tests. Heredity (Beijing), 5, 24–26. (in Chiense)

Xu C, Shah M A, Mipam T, Wu S, Yi C, Luo H, Yuan M, Chai Z, Zhao W, Cai X. 2020. Bovid microRNAs involved in the process of spermatogonia differentiation into spermatocytes. International Journal of Biological Sciences, 16, 239–250.

Yang L, Mo C, Adetula A A, Elokil A, Li S. 2020. Bilateral apex pubis distance: A novel index for follicular development and egg laying status in domestic hens (Gallus gallus domesticus). British Poultry Science61, 195–199.

Zhang H, Klausen C, Zhu H, Chang H M, Leung P C. 2015. BMP4 and BMP7 suppress StAR and progesterone production via ALK3 and SMAD1/5/8-SMAD4 in human granulosa-lutein cells. Endocrinology, 156, 4269–4280.

Zhang J, Chen S, Yang J, Zhao F. 2020. Accurate quantification of circular RNAs identifies extensive circular isoform switching events. Nature Communications11, 90.

Zhao X Y, Wu Y P, Li H Y, Cao Y, Mei Z Y, Li J H. 2022. Differential expression and functional analysis of circRNA in the ovaries of Yili geese at different egg-laying stages. Genes & Genomics, 44, 1171–1180.

Zheng L, Liu L, Lin L, Tang H, Fan X, Lin H, Li X. 2019. Cecal circRNAs are associated with the response to salmonella enterica serovar enteritidis inoculation in the chicken. Frontiers in Immunology, 10, 1186.

Zhu Y, Wang H, Wang J, Han S S, Zhang Y, Ma M G, Zhu Q, Zhang K Y, Yin H D. 2021. Zearalenone induces apoptosis and cytoprotective autophagy in chicken granulosa cells by PI3K-AKT-mTOR and MAPK signaling pathways. Toxins (Basel), 13, 199.

[1] Wenya Li, Haoxiang Ma, Yanxing Wang, Yushi Zhang, Yang Liu, Ruili Han, Hong Li, Hanfang Cai, Xiaojun Liu, Xiangtao Kang, Ruirui Jiang, Zhuanjian Li. The VGLL2 gene participates in muscle development in Gushi chickens[J]. >Journal of Integrative Agriculture, 2025, 24(1): 246-260.
[2] Lei Shi, Yanyan Sun, Yunlei Li, Hao Bai, Jingwei Yuan, Hui Ma, Yuanmei Wang, Panlin Wang, Aixin Ni, Linlin Jiang, Pingzhuang Ge, Shixiong Bian, Yunhe Zong, Jinmeng Zhao, Adamu M. Isa, Hailai H. Tesfay, Jilan Chen. Asymmetric expression of CA2 and CA13 linked to calcification in the bilateral mandibular condyles cause crossed beaks in chickens[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2379-2390.
[3] ZHAO Wen-juan, YUAN Xiao-ya, XIANG Hai, MA Zheng, CUI Huan-xian, LI Hua, ZHAO Gui-ping. Transcriptome-based analysis of key genes and pathways affecting the linoleic acid content in chickens[J]. >Journal of Integrative Agriculture, 2023, 22(12): 3744-3754.
[4] SUN Yu-hang, ZHAI Gui-ying, PANG Yong-jia, LI Rui, LI Yu-mao, CAO Zhi-ping, WANG Ning, LI Hui, WANG Yu-xiang. PPAR gamma2: The main isoform of PPARγ that positively regulates the expression of the chicken Plin1 gene[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2357-2371.
[5] LI Mei-zhen, XIAO Hua-mei, HE Kang, LI Fei. Progress and prospects of noncoding RNAs in insects[J]. >Journal of Integrative Agriculture, 2019, 18(4): 729-747.
No Suggested Reading articles found!