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Journal of Integrative Agriculture  2026, Vol. 25 Issue (1): 207-226    DOI: 10.1016/j.jia.2024.03.052
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
3D genomic alterations during development of skeletal muscle in chicken

Zhongxian Xu1, 2, 3*, Tao Wang2, 3*, Wei Zhu2*, Maosen Yang2, Dong Leng2, Ziyu Li2, Jiaman Zhang2, Pengliang Liu2, Zhoulin Wu4, Mengnan He5, Yan Li5, Hua Kui2, Xue Bai2, Bo Zeng2, Yao Zhang2, Qing Zhu2, Xiaoling Zhao2, Mingzhou Li 2#, Diyan Li2, 3#

1 Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong 637009, China

2 Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China

3 Antibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, School of Pharmacy, Chengdu University, Chengdu 610106, China

4 Key Laboratory of Meat Processing of Sichuan, College of Food and Biological Engineering, Chengdu University, Chengdu 610106, China

5 Chengdu Research Base of Giant Panda Breeding, Chengdu 611081, China

 Highlights 
Multi-stage 3D genomic and epigenomic maps reveal dynamic chromatin reorganization during chicken muscle development.
A/B compartment switching and TAD remodeling are tightly linked to transcriptional transitions from myogenesis to aging.
Promoter-enhancer rewiring underlies stage-specific activation of muscle growth and senescence-associated genes.
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摘要  
骨骼肌发育过程中包含了维持肌肉形态、收缩力、细胞增殖、分化、相互作用、迁移和死亡的基因。尽管肌细胞分化过程中的动态转录调控是研究最深入热点之一,但骨骼肌发育的三维染色质结构尚未得到深入研究。本文利用RNA-seq解析了鸡肌肉12个发育时间点的基因转录表达模式;并选择4个代表性时间点用Hi-C构建了骨骼肌发育中染色质三维构象,从染色质的3种不同层级结构(染色质区室、拓扑关联结构域、染色质环)探讨了染色质拓扑结构与基因表达调控之间的关系;还利用ChIP-seq定位了组蛋白H3K27ac和H3K4me3修饰的增强子和启动子位点。结果表明大部分基因组结构变化是单向的,并与复杂的基因表达开/关相耦合:在鸡骨骼肌发育过程中,有258.30 Mb在区室层面发生变化,大量与衰老相关的基因所在区室从抑制状态向活跃状态转变;316.57 Mb的TAD内部互作强度随着法与显著变化;一些肌肉相关基因的启动子在发育过程中与活性增强子互作,受活性增强子调控的基因数目随着发育逐渐降低,部分与肌肉疾病和衰老相关的基因在老年阶段被激活。研究结果可望从三维基因组视角解析几骨骼肌发育的分析机制,为分子遗传育种的实现提供理论指导,并将为日后筛选和鉴定农业动物重要数量性状的调控元件开辟新思路。


Abstract  

The development of skeletal muscle are complicated processes involving genes responsible for proper muscle morphology, contractility, cell proliferation, differentiation, interactions, migration, and death.  The three-dimensional chromatin architecture of skeletal muscle development has not been studied intensively although dynamic transcriptional regulation during differentiation of muscle cells is one of the most deeply studied processes.  The RNA-seq was used to analyze the transcriptome pattern during chicken muscle development across 12 stages.  Hi-C was used to build chromatin architectures during four representative stages.  ChIP-seq was conducted to identify enhancers and promoters in these four stages, which are occupied by histone H3K27ac and H3K4me3 peaks.  Results show that large-scale genome architecture changes are mostly unidirectional, and coupled by complex on/off dynamic patterns of gene expression.  Specifically, we observed 258.30 Mb of the genome undergoing A/B compartment switching.  Notable alterations (316.57 Mb) of interaction frequencies within TADs were observed.  Substantial aging-associated genes exhibited ascending connectivity with the compartment transition from repressive to active status during muscle development.  Some muscle-related gene promoters that interacted with active enhancers during development, and some myopathy/aging-associated genes that were activated in aging muscle were founded.  These results provide key insights into skeletal muscle development in vivo, and offer a valuable resource that allows in-depth functional characterization of candidate genes.

Keywords:  skeletal muscle       development        gene expression        chromatin architecture  
Received: 08 October 2023   Accepted: 01 February 2024 Online: 16 March 2024  
Fund: This work was supported by the National Key R & D Program of China (2023YFD1300040 and 2022YFF1000100), the Sichuan Science and Technology Program, China (2022NSFSC0132, 2021YFYZ0009 and 2022JDJQ0054), the National Natural Science Foundation of China (32225046).
About author:  Zhongxian Xu, E-mail: xu_zhongxian@cwnu.edu.cn; Tao Wang, E-mail: wanttao@hotmail.com; Wei Zhu, E-mail: 1424518023@qq.com; #Correspondence Diyan Li, E-mail: lidiyan@cdu.edu.cn; Mingzhou Li, E-mail: mingzhou.li@sicau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Zhongxian Xu, Tao Wang, Wei Zhu, Maosen Yang, Dong Leng, Ziyu Li, Jiaman Zhang, Pengliang Liu, Zhoulin Wu, Mengnan He, Yan Li, Hua Kui, Xue Bai, Bo Zeng, Yao Zhang, Qing Zhu, Xiaoling Zhao, Mingzhou Li, Diyan Li. 2026. 3D genomic alterations during development of skeletal muscle in chicken. Journal of Integrative Agriculture, 25(1): 207-226.

Bentzinger C F, Wang Y X, Rudnicki M A. 2012. Building muscle: Molecular regulation of myogenesis. Cold Spring Harbor Perspectives in Biology4, a008342

Berti F, Nogueira J M, Wohrle S, Sobreira D R, Hawrot K, Dietrich S. 2015. Time course and side-by-side analysis of mesodermal, pre-myogenic, myogenic and differentiated cell markers in the chicken model for skeletal muscle formation. Journal of Anatomy227, 361–382.

Bryson-Richardson R J, Currie P D. 2008. The genetics of vertebrate myogenesis. Nature Review in Genetics9, 632–646.

Buckingham M, Rigby P W. 2014. Gene regulatory networks and transcriptional mechanisms that control myogenesis. Developmental Cell28, 225–238.

Cardoso-Moreira M, Halbert J, Valloton D, Velten B, Chen C, Shao Y, Liechti A, Ascencao K, Rummel C, Ovchinnikova S, Mazin P V, Xenarios I, Harshman K, Mort M, Cooper D N, Sandi C, Soares M J, Ferreira P G, Afonso S, Carneiro M, et al. 2019. Gene expression across mammalian organ development. Nature571, 505–509.

Chandra T, Ewels P A, Schoenfelder S, Furlan-Magaril M, Wingett S W, Kirschner K, Thuret J Y, Andrews S, Fraser P, Reik W. 2015. Global reorganization of the nuclear landscape in senescent cells. Cell Reports10, 471–483.

Chen G, Wang Y, Garate M, Zhou J, Li G. 2010. The tumor suppressor ING3 is degraded by SCF(Skp2)-mediated ubiquitin-proteasome system. Oncogene29, 1498–1508.

Chen L, Li J, Yuan R, Wang Y, Zhang J, Lin Y, Wang L, Zhu X, Zhu W, Bai J, Kong F, Zeng B, Lu L, Ma J, Long K, Jin L, Huang Z, Huo J, Gu Y, Wang D, Mo D, et al. 2022. Dynamic 3D genome reorganization during development and metabolic stress of the porcine liver. Cell Discovery8, 56.

Chen W, Lv Y T, Zhang H X, Ruan D, Wang S, Lin Y C. 2013. Developmental specificity in skeletal muscle of late-term avian embryos and its potential manipulation. Poultry Science92, 2754–2764.

Chin R M, Fu X, Pai M Y, Vergnes L, Hwang H, Deng G, Diep S, Lomenick B, Meli V S, Monsalve G C, Hu E, Whelan S A, Wang J X, Jung G, Solis G M, Fazlollahi F, Kaweeteerawat C, Quach A, Nili M, Krall A S, et al. 2014. The metabolite alpha-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR. Nature510, 397–401.

Chung C Y T, Lo P H Y, Lee K K H. 2020. Babam2 regulates cell cycle progression and pluripotency in mouse embryonic stem cells as revealed by induced DNA damage. Biomedicines8, 397.

Coppe J P, Desprez P Y, Krtolica A, Campisi J. 2010. The senescence-associated secretory phenotype: The dark side of tumor suppression. Annual Review of Pathology5, 99–118.

Courtois-Cox S, Jones S L, Cichowski K. 2008. Many roads lead to oncogene-induced senescence. Oncogene27, 2801–2809.

Crane E, Bian Q, McCord R P, Lajoie B R, Wheeler B S, Ralston E J, Uzawa S, Dekker J, Meyer B J. 2015. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature523, 240–244.

Criscione S W, Teo Y V, Neretti N. 2016. The chromatin landscape of cellular senescence. Trends in GeneticsTIG32, 751–761.

David V, Martin A, Hedge A M, Rowe P S. 2009. Matrix extracellular phosphoglycoprotein (MEPE) is a new bone renal hormone and vascularization modulator. Endocrinology150, 4012–4023.

Deschamps J, Duboule D. 2017. Embryonic timing, axial stem cells, chromatin dynamics, and the Hox clock. Genes & Development31, 1406–1416.

Dethlefsen M M, Halling J F, Moller H D, Plomgaard P, Regenberg B, Ringholm S, Pilegaard H. 2018. Regulation of apoptosis and autophagy in mouse and human skeletal muscle with aging and lifelong exercise training. Experimental Gerontology111, 141–153.

Dittmer J. 2003. The biology of the Ets1 proto-oncogene. Molecular Cancer2, 29.

Dixon J R, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget J E, Lee A Y, Ye Z, Kim A, Rajagopal N, Xie W, Diao Y, Liang J, Zhao H, Lobanenkov V V, Ecker J R, Thomson J A, Ren B. 2015. Chromatin architecture reorganization during stem cell differentiation. Nature518, 331–336.

Dixon J R, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu J S, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature485, 376–380.

Doi T, Puri P, Bannigan J, Thompson J. 2012. Eya1 and Eya2 gene expression is down-regulated during somitic myogenesis in the cadmium-induced omphalocele chick model. Journal of Pediatric Surgery47, 1123–1127.

Durand N C, Shamim M S, Machol I, Rao S S, Huntley M H, Lander E S, Aiden E L. 2016. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems3, 95–98.

Esteves de Lima J, Bou Akar R, Mansour M, Rocancourt D, Buckingham M, Relaix F. 2021. M-Cadherin Is a PAX3 target during myotome patterning. Frontiers in Cell Developmental Biology9, 652652.

Fishman V, Battulin N, Nuriddinov M, Maslova A, Zlotina A, Strunov A, Chervyakova D, Korablev A, Serov O, Krasikova A. 2019. 3D organization of chicken genome demonstrates evolutionary conservation of topologically associated domains and highlights unique architecture of erythrocytes’ chromatin. Nucleic Acids Research47, 648–665.

Flyamer I M, Gassler J, Imakaev M, Brandão H B, Ulianov S V, Abdennur N, Razin S V, Mirny L A, Tachibana-Konwalski K. 2017. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature544, 110–114.

Ghosh S, Chan C K. 2016. Analysis of RNA-seq data using TopHat and Cufflinks. Methods in Molecular Biology1374, 339–361.

Grifone R, Demignon J, Giordani J, Niro C, Souil E, Bertin F, Laclef C, Xu P X, Maire P. 2007. Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Developmental Biology302, 602–616.

Grove B K, Cerny L, Perriard J C, Eppenberger H M. 1985. Myomesin and M-protein: Expression of two M-band proteins in pectoral muscle and heart during development. The Journal of Cell Biology101, 1413–1421.

Gupta A, Place M, Goldstein S, Sarkar D, Zhou S, Potamousis K, Kim J, Flanagan C, Li Y, Newton M A, Callander N S, Hematti P, Bresnick E H, Ma J, Asimakopoulos F, Schwartz D C. 2015. Single-molecule analysis reveals widespread structural variation in multiple myeloma. Proceedings of the National Academy of Sciences of the United States of America112, 7689–7694.

Knížetová H, Hyánek J, Hyánková L, Bělíček P. 1995. Comparative study of growth curves in poultry. Genetics Selection Evolution27, 365–375.

Hammoud S S, Low D H P, Yi C, Carrell D T, Guccione E, Cairns B R. 2014. Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell15, 239–253.

Heinz S, Benner C, Spann N, Bertolino E, Lin Y C, Laslo P, Cheng J X, Murre C, Singh H, Glass C K. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell38, 576–589.

van Hengel J, Calore M, Bauce B, Dazzo E, Mazzotti E, De Bortoli M, Lorenzon A, Li Mura I E, Beffagna G, Rigato I, Vleeschouwers M, Tyberghein K, Hulpiau P, van Hamme E, Zaglia T, Corrado D, Basso C, Thiene G, Daliento L, Nava A, et al. 2013. Mutations in the area composita protein alphaT-catenin are associated with arrhythmogenic right ventricular cardiomyopathy. European Heart Journal34, 201–210.

Hernandez S F, Vahidi N A, Park S, Weitzel R P, Tisdale J, Rueda B R, Wolff E F. 2015. Characterization of extracellular DDX4- or Ddx4-positive ovarian cells. Nature Medcine21, 1114–1116.

Huang Q, Li F, Liu X, Li W, Shi W, Liu F F, O’Sullivan B, He Z, Peng Y, Tan A C, Zhou L, Shen J, Han G, Wang X J, Thorburn J, Thorburn A, Jimeno A, Raben D, Bedford J S, Li C Y. 2011. Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nature Medcine17, 860–866.

Hug C B, Vaquerizas J M. 2018. The birth of the 3D genome during early embryonic development. Trends in Genetics34, 903–914.

Imakaev M, Fudenberg G, McCord R P, Naumova N, Goloborodko A, Lajoie B R, Dekker J, Mirny L A. 2012. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nature Methods9, 999–1003.

Ishihara T, Ikeda K, Sato S, Yajima H, Kawakami K. 2008. Differential expression of Eya1 and Eya2 during chick early embryonic development. Gene Expression Patterns8, 357–367.

Janssens B, Mohapatra B, Vatta M, Goossens S, Vanpoucke G, Kools P, Montoye T, van Hengel J, Bowles N E, van Roy F, Towbin J A. 2003. Assessment of the CTNNA3 gene encoding human alpha T-catenin regarding its involvement in dilated cardiomyopathy. Human Genetics112, 227–236.

Jejurikar S S, Henkelman E A, Cederna P S, Marcelo C L, Urbanchek M G, Kuzon Jr W M. 2006. Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Experimental Gerontology41, 828–836.

Jin L, Wang D, Zhang J, Liu P, Wang Y, Lin Y, Liu C, Han Z, Long K, Li D, Jiang Y, Li G, Zhang Y, Bai J, Li X, Li J, Lu L, Kong F, Wang X, Li H, et al. 2023. Dynamic chromatin architecture of the porcine adipose tissues with weight gain and loss. Nature Communications14, 3457.

Kalmes A, Daum G, Clowes A W. 2001. EGFR transactivation in the regulation of SMC function. Annals of the New York Academy of Sciences947, 42–54.

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S L. 2013. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology14, R36.

Knight P A, Ruiz D. 2012. A fast algorithm for matrix balancing. IMA Journal of Numerical Analysis33, 1029–1047.

Kocamis H, McFarland D C, Killefer J. 2001. Temporal expression of growth factor genes during myogenesis of satellite cells derived from the biceps femoris and pectoralis major muscles of the chicken. Journal of Cellular Physiology186, 146–152.

Kong S, Zhang Y. 2019. Deciphering Hi-C: From 3D genome to function. Cell Biology and Toxicology35, 15–32.

Kragesteen B K, Spielmann M, Paliou C, Heinrich V, Schopflin R, Esposito A, Annunziatella C, Bianco S, Chiariello A M, Jerkovic I, Harabula I, Guckelberger P, Pechstein M, Wittler L, Chan W L, Franke M, Lupianez D G, Kraft K, Timmermann B, Vingron M, et al. 2018. Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis. Nature Genetics50, 1463–1473.

Krijger P H, Di Stefano B, de Wit E, Limone F, van Oevelen C, de Laat W, Graf T. 2016. Cell-of-origin-specific 3D genome structure acquired during somatic cell reprogramming. Cell Stem Cell18, 597–610.

Lamber E P, Guicheney P, Pinotsis N. 2022. The role of the M-band myomesin proteins in muscle integrity and cardiac disease. Journal of Biomedical Science29, 18.

Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods9, 357–359.

Li C, Liu F, Liu S, Pan H, Du H, Huang J, Xie Y, Li Y, Zhao R, Wei Y. 2020. Elevated myocardial SORBS2 and the underlying implications in left ventricular noncompaction cardiomyopathy. eBioMedicine53, 102695.

Li D, He M, Tang Q, Tian S, Zhang J, Li Y, Wang D, Jin L, Ning C, Zhu W, Hu S, Long K, Ma J, Liu J, Zhang Z, Li M. 2022a. Comparative 3D genome architecture in vertebrates. BMC Biology20, 99.

Li D, Li Y, Li M, Che T, Tian S, Chen B, Zhou X, Zhang G, Gaur U, Luo M, Tian K, He M, He S, Xu Z, Jin L, Tang Q, Dai Y, Xu H, Hu Y, Zhao X, et al. 2019. Population genomics identifies patterns of genetic diversity and selection in chicken. BMC Genomics20, 263.

Li D, Ning C, Zhang J, Wang Y, Tang Q, Kui H, Wang T, He M, Jin L, Li J, Lin Y, Zeng B, Yin H, Zhao X, Zhang Y, Xu H, Zhu Q, Li M. 2022b. Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis. Nature Communications13, 131.

Li H, Cybulsky M I, Gimbrone Jr M A, Libby P. 1993. Inducible expression of vascular cell adhesion molecule-1 by vascular smooth muscle cells in vitro and within rabbit atheroma. The American Journal of Pathology143, 1551–1559.

Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics26, 589–595.

Liang F, Wang B, Geng J, You G, Fa J, Zhang M, Sun H, Chen H, Fu Q, Zhang X, Zhang Z. 2021. SORBS2 is a genetic factor contributing to cardiac malformation of 4q deletion syndrome patients. eLife10, e67481.

Lieberman-Aiden E, van Berkum N L, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie B R, Sabo P J, Dorschner M O, Sandstrom R, Bernstein B, Bender M A, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny L A, Lander E S, Dekker J. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science326, 289–293.

Liesenfeld M, Mosig S, Funke H, Jansen L, Runnebaum I B, Durst M, Backsch C. 2013. SORBS2 and TLR3 induce premature senescence in primary human fibroblasts and keratinocytes. BMC Cancer13, 507.

Lindsly S, Chen C, Liu S, Ronquist S, Dilworth S, Perlman M, Rajapakse I. 2021. 4DNvestigator: Time series genomic data analysis toolbox. Nucleus12, 58–64.

Ljt K, Rh V D W, Ketting R F, De W E. 2018. Systemic loss and gain of chromatin architecture throughout zebrafish development. Cell Reports24, 1–10.

Lombardo S D, Mazzon E, Basile M S, Campo G, Corsico F, Presti M, Bramanti P, Mangano K, Petralia M C, Nicoletti F, Fagone P. 2019. Modulation of tetraspanin 32 (TSPAN32) expression in T cell-mediated immune responses and in multiple sclerosis. International Journal of Molecular Sciences20, 4323.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology15, 550.

Lu H, Ju D D, Yang G D, Zhu L Y, Yang X M, Li J, Song W W, Wang J H, Zhang C C, Zhang Z G, Zhang R. 2019. Targeting cancer stem cell signature gene SMOC-2 overcomes chemoresistance and inhibits cell proliferation of endometrial carcinoma. eBioMedicine40, 276–289.

Luo W, Lin Z, Chen J, Chen G, Zhang S, Liu M, Li H, He D, Liang S, Luo Q, Zhang D, Nie Q, Zhang X. 2021. TMEM182 interacts with integrin beta 1 and regulates myoblast differentiation and muscle regeneration. Journal of CachexiaSarcopenia and Muscle12, 1704–1723.

Lupianez D G, Kraft K, Heinrich V, Krawitz P, Brancati F, Klopocki E, Horn D, Kayserili H, Opitz J M, Laxova R, Santos-Simarro F, Gilbert-Dussardier B, Wittler L, Borschiwer M, Haas S A, Osterwalder M, Franke M, Timmermann B, Hecht J, Spielmann M, et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell161, 1012–1025.

MacPhillamy C, Pitchford W S, Alinejad-Rokny H, Low W Y. 2021. Opportunity to improve livestock traits using 3D genomics. Animal Genetics52, 785–798.

Magli A, Baik J, Pota P, Cordero C O, Kwak I Y, Garry D J, Love P E, Dynlacht B D, Perlingeiro R C R. 2019. Pax3 cooperates with Ldb1 to direct local chromosome architecture during myogenic lineage specification. Nature Communications10, 2316.

Maharjan P, Beitia A, Weil J, Suesuttajit N, Hilton K, Caldas J, Umberson C, Martinez D, Kong B, Owens C M, Coon C. 2021. Woody breast myopathy broiler show age-dependent adaptive differential gene expression in pectoralis major and altered in-vivo triglyceride kinetics in adipogenic tissues. Poultry Science100, 101092.

Malik L, Patro R. 2019. Rich chromatin structure prediction from Hi-C data. IEEE/ACM Transactions on Computational Biology and Bioinformatics16, 1448–1458.

Martone J, Mariani D, Desideri F, Ballarino M. 2019. Non-coding RNAs shaping muscle. Frontiers in Cell and Developmental Biology7, 394.

Matharu N, Ahituv N. 2015. Minor loops in major folds: Enhancer-promoter looping, chromatin restructuring, and their association with transcriptional regulation and disease. PLoS Genetics11, e1005640.

Mele M, Ferreira P G, Reverter F, DeLuca D S, Monlong J, Sammeth M, Young T R, Goldmann J M, Pervouchine D D, Sullivan T J, Johnson R, Segre A V, Djebali S, Niarchou A, Consortium G T, Wright F A, Lappalainen T, Calvo M, Getz G, Dermitzakis E T, et al. 2015. Human genomics. The human transcriptome across tissues and individuals. Science348, 660–665.

Molina-Privado I, Jimenez P R, Montes-Moreno S, Chiodo Y, Rodriguez-Martinez M, Sanchez-Verde L, Iglesias T, Piris M A, Campanero M R. 2012. E2F4 plays a key role in Burkitt lymphoma tumorigenesis. Leukemia26, 2277–2285.

Neems D S, Garza-Gongora A G, Smith E D, Kosak S T. 2016. Topologically associated domains enriched for lineage-specific genes reveal expression-dependent nuclear topologies during myogenesis. Proceedings of the National Academy of Sciences of the United States of America113, E1691–E1700.

Newman A B, Kupelian V, Visser M, Simonsick E M, Goodpaster B H, Kritchevsky S B, Tylavsky F A, Rubin S M, Harris T B, Ofhealth, Behalf O. 2006. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. The Journals of Gerontology Series (Biological Sciences and Medical Sciences), 61, 72–77.

Nkabyo Y S, Go Y M, Ziegler T R, Jones D P. 2005. Extracellular cysteine/cystine redox regulates the p44/p42 MAPK pathway by metalloproteinase-dependent epidermal growth factor receptor signaling. American Journal of Physiology Gastrointestinal and Liver Physiology289, G70–G78.

Noordermeer D, Leleu M, Schorderet P, Joye E, Chabaud F, Duboule D. 2014. Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. eLife3, e02557.

Nora E P, Lajoie B R, Schulz E G, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum N L, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature485, 381–385.

Nueda M J, Tarazona S, Conesa A. 2014. Next maSigPro: Updating maSigPro bioconductor package for RNA-seq time series. Bioinformatics30, 2598–2602.

Paliou C, Guckelberger P, Schopflin R, Heinrich V, Esposito A, Chiariello A M, Bianco S, Annunziatella C, Helmuth J, Haas S, Jerkovic I, Brieske N, Wittler L, Timmermann B, Nicodemi M, Vingron M, Mundlos S, Andrey G. 2019. Preformed chromatin topology assists transcriptional robustness of Shh during limb development. Proceedings of the National Academy of Sciences of the United States of America116, 12390–12399.

Pan W, Zhang N, Liu W, Liu J, Zhou L, Liu Y, Yang M. 2018. The long noncoding RNA GAS8-AS1 suppresses hepatocarcinogenesis by epigenetically activating the tumor suppressor GAS8. The Journal of Biological Chemistry293, 17154–17165.

Parker M H, Seale P, Rudnicki M A. 2003. Looking back to the embryo: Defining transcriptional networks in adult myogenesis. Nature Reviews Genetics4, 497–507.

Paulsen J, Liyakat Ali T M, Nekrasov M, Delbarre E, Baudement M O, Kurscheid S, Tremethick D, Collas P. 2019. Long-range interactions between topologically associating domains shape the four-dimensional genome during differentiation. Nature Genetics51, 835–843.

Pertea M, Pertea G M, Antonescu C M, Chang T C, Mendell J T, Salzberg S L. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology33, 290–295.

Prenzel N, Fischer O M, Streit S, Hart S, Ullrich A. 2001. The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocrine Related Cancer8, 11–31.

Quiat D, Voelker K A, Pei J, Grishin N V, Grange R W, Bassel-Duby R, Olson E N. 2011. Concerted regulation of myofiber-specific gene expression and muscle performance by the transcriptional repressor Sox6. Proceedings of the National Academy of Sciences of the United States of America108, 10196–10201.

Rao S S, Huntley M H, Durand N C, Stamenova E K, Bochkov I D, Robinson J T, Sanborn A L, Machol I, Omer A D, Lander E S, Aiden E L. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell159, 1665–1680.

Rieber L, Mahony S. 2017. miniMDS: 3D structural inference from high-resolution Hi-C data. Bioinformatics33, i261-i266.

Robin J D, Jacome Burbano M S, Peng H, Croce O, Thomas J L, Laberthonniere C, Renault V, Lototska L, Pousse M, Tessier F, Bauwens S, Leong W, Sacconi S, Schaeffer L, Magdinier F, Ye J, Gilson E. 2020. Mitochondrial function in skeletal myofibers is controlled by a TRF2-SIRT3 axis over lifetime. Aging Cell19, e13097.

Rosa-Garrido M, Chapski D J, Schmitt A D, Kimball T H, Karbassi E, Monte E, Balderas E, Pellegrini M, Shih T T, Soehalim E, Liem D, Ping P, Galjart N J, Ren S, Wang Y, Ren B, Vondriska T M. 2017. High-resolution mapping of chromatin conformation in cardiac myocytes reveals structural remodeling of the epigenome in heart failure. Circulation136, 1613–1625.

Rowley M J, Nichols M H, Lyu X, Ando-Kuri M, Rivera I S M, Hermetz K, Wang P, Ruan Y, Corces V G. 2017. Evolutionarily conserved principlespredict 3D chromatin organization. Molecular Cell67, 837–852.e7.

Ruis P, Van Ly D, Borel V, Kafer G R, McCarthy A, Howell S, Blassberg R, Snijders A P, Briscoe J, Niakan K K, Marzec P, Cesare A J, Boulton S J. 2021. TRF2-independent chromosome end protection during pluripotency. Nature589, 103–109.

Salama R, Sadaie M, Hoare M, Narita M. 2014. Cellular senescence and its effector programs. Genes & Development28, 99–114.

Sanders S J, Campbell A J, Cottrell J R, Moller R S, Wagner F F, Auldridge A L, Bernier R A, Catterall W A, Chung W K, Empfield J R, George Jr A L, Hipp J F, Khwaja O, Kiskinis E, Lal D, Malhotra D, Millichap J J, Otis T S, Petrou S, Pitt G, et al. 2018. Progress in understanding and treating SCN2A-mediated disorders. Trends in Neuroscience41, 442–456.

Sati S, Bonev B, Szabo Q, Jost D, Bensadoun P, Serra F, Loubiere V, Papadopoulos G L, Rivera-Mulia J C, Fritsch L, Bouret P, Castillo D, Gelpi J L, Orozco M, Vaillant C, Pellestor F, Bantignies F, Marti-Renom M A, Gilbert D M, Lemaitre J M, et al. 2020. 4D Genome rewiring during oncogene-induced and replicative senescence. Molecular Cell78, 522–538. e9.

Schrauwen I, Valgaeren H, Tomas-Roca L, Sommen M, Altunoglu U, Wesdorp M, Beyens M, Fransen E, Nasir A, Vandeweyer G, Schepers A, Rahmoun M, van Beusekom E, Huentelman M J, Offeciers E, Dhooghe I, Huber A, Van de Heyning P, Zanetti D, De Leenheer E M R, et al. 2019. Variants affecting diverse domains of MEPE are associated with two distinct bone disorders, a craniofacial bone defect and otosclerosis. Genetics in Medcine21, 1199–1208.

Sousa-Victor P, Garcia-Prat L, Munoz-Canoves P. 2022. Control of satellite cell function in muscle regeneration and its disruption in ageing. Nature ReviewsMolecular Cell Biology23, 204–226.

Stanic B, Katsuyama M, Miller Jr F J. 2010. An oxidized extracellular oxidation-reduction state increases Nox1 expression and proliferation in vascular smooth muscle cells via epidermal growth factor receptor activation. ArteriosclerosisThrombosisand Vascular Biology30, 2234–2241.

Su Y, Wang T, Wu N, Li D, Fan X, Xu Z, Mishra S K, Yang M. 2019. Alpha-ketoglutarate extends Drosophila lifespan by inhibiting mTOR and activating AMPK. Aging11, 4183–4197.

Surakka I, Fritsche L G, Zhou W, Backman J, Kosmicki J A, Lu H, Brumpton B, Nielsen J B, Gabrielsen M E, Skogholt A H, Wolford B, Graham S E, Chen Y E, Lee S, Kang H M, Langhammer A, Forsmo S, Asvold B O, Styrkarsdottir U, Holm H, Gudbjartsson D, et al. 2020. MEPE loss-of-function variant associates with decreased bone mineral density and increased fracture risk. Nature Communications11, 4093.

Syafruddin S E, Mohtar M A, Wan Mohamad Nazarie W F, Low T Y. 2020. Two sides of the same coin: The roles of KLF6 in physiology and pathophysiology. Biomolecules10, 1378.

Symmons O, Pan L, Remeseiro S, Aktas T, Klein F, Huber W, Spitz F. 2016. The Shh topological domain facilitates the action of remote enhancers by reducing the effects of genomic distances. Developmental Cell39, 529–543.

Taglietti V, Maroli G, Cermenati S, Monteverde S, Ferrante A, Rossi G, Cossu G, Beltrame M, Messina G. 2016. Nfix induces a switch in Sox6 transcriptional activity to regulate MyHC-I expression in fetal muscle. Cell Reports17, 2354–2366.

Tiscia G L, Margaglione M. 2018. Human fibrinogen: Molecular and genetic aspects of congenital disorders. International Journal of Molecular Sciences19, 1597.

Whyte W A, Orlando D A, Hnisz D, Abraham B J, Lin C Y, Kagey M H, Rahl P B, Lee T I, Young R A. 2013. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell153, 307–319.

Williams T M, Lisanti M P. 2004. The caveolin proteins. Genome Biology5, 214.

Xu P X, Cheng J, Epstein J A, Maas R L. 1997. Mouse Eya genes are expressed during limb tendon development and encode a transcriptional activation function. Proceedings of the National Academy of Sciences of the United States of America94, 11974–11979.

Xu Z, Che T, Li F, Tian K, Zhu Q, Mishra S K, Dai Y, Li M, Li D. 2018. The temporal expression patterns of brain transcriptome during chicken development and ageing. BMC Genomics19, 917.

Yang T, Zhang F, Yardimci G G, Song F, Hardison R C, Noble W S, Yue F, Li Q. 2017. HiCRep: Assessing the reproducibility of Hi-C data using a stratum-adjusted correlation coefficient. Genome Research27, 1939–1949.

Yau M S, Kuipers A L, Price R, Nicolas A, Tajuddin S M, Handelman S K, Arbeeva L, Chesi A, Hsu Y H, Liu C T, Karasik D, Zemel B S, Grant S F, Jordan J M, Jackson R D, Evans M K, Harris T B, Zmuda J M, Kiel D P. 2021. A meta-analysis of the transferability of bone mineral density genetic loci associations from European to African ancestry populations. Journal of Bone and Mineral Research36, 469–479.

Yuan R, Zhang J, Wang Y, Zhu X, Hu S, Zeng J, Liang F, Tang Q, Chen Y, Chen L, Zhu W, Li M, Mo D. 2021. Reorganization of chromatin architecture during prenatal development of porcine skeletal muscle. DNA Research28, 1–11.

Zhan Y, Mariani L, Barozzi I, Schulz E G, Bluthgen N, Stadler M, Tiana G, Giorgetti L. 2017. Reciprocal insulation analysis of Hi-C data shows that TADs represent a functionally but not structurally privileged scale in the hierarchical folding of chromosomes. Genome Research27, 479–490.

Zhang Y, Liu T, Meyer C A, Eeckhoute J, Johnson D S, Bernstein B E, Nusbaum C, Myers R M, Brown M, Li W, Liu X S. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biology9, R137.

Zheng H, Xie W. 2019. The role of 3D genome organization in development and cell differentiation. Nature ReviewsMolecular Cell Biology20, 53tt50.

Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi A H, Tanaseichuk O, Benner C, Chanda S K. 2019. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nature Communications10, 1523.

Zhu B, Rippe C, Holmberg J, Zeng S, Perisic L, Albinsson S, Hedin U, Uvelius B, Swärd K. 2018. Nexilin/NEXN controls actin polymerization in smooth muscle and is regulated by myocardin family coactivators and YAP. Scientific Reports8, 13025.

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