Association, expression, and pathway analysis of biglycan gene with lamb quality and retail cut carcass
DOI:
https://doi.org/10.61308/GZSI2505Keywords:
biglycan, BGN, lamb quality, PCR RFLP, retail cut carcass, sheepAbstract
The quality of lamb meat and retail cut carcass traits are crucial determinants of meat quality, influencing consumer preference and high-quality lamb meat. The biglycan (BGN) gene, which regulates the formation and maintenance of connective tissues, including bone and cartilage, plays a crucial role in providing structural support strength and facilitating tissue healing and regeneration. This study examined the identification of polymorphism of the BGN gene in Indonesian sheep and its association, expression, and pathway analysis with lamb quality and retail cut carcass traits. Samples were collected from the longissimus dorsi muscle of 100 male animals (JTTS, BCS, CAS, GS, and JS), aged between 10 and 12 months, and analyzed for polymorphisms of the BGN gene using PCR-RFLP methods. The data were analyzed using the General Linear Model (GLM) test to investigate the association between genotype and phenotype characteristics. The expression levels of BGN mRNA were estimated using qRT-PCR, pathway, and network analysis using KEGG PATHWAY analysis. The BGN gene was polymorphic in different Indonesian sheep breeds. The BGN gene (g.77807325 G>C) exhibited two genotypes, GG and CC. The BGN polymorphism was significantly associated with (P<0.05) lamb quality characteristics, such as pH value and retail cut carcass traits, including leg, muscle in the leg, muscle in the rack, shank, and muscle in the shank. The GG genotype demonstrated superior values for these traits compared to the CC genotype. The analysis of the BGN gene expression showed no significant difference (P>0.05) between the GG and CC genotypes. The pathway analysis showed that the BGN gene is part of the small leucine-rich proteoglycans (SLRP) family, which plays a role in the muscle cell cytoskeleton that affects the meat quality and retail cut carcass. Sheep with the GG genotype showed improved values for several desirable traits. Thus, the G>C SNP of the BGN gene holds promise as a genetic marker for selection to improve the lamb meat quality and retail cut carcass of Indonesian sheep.
References
Alberi, C., Hisey, E., Lassaline, M., Atilano, A., Kalbfleisch, T., Stoppini, R., Hermans, H., Back, W., Mienaltowski, M. J. & Bellone, R. R. (2018). Ruling out BGN variants as simple X-linked causative mutations for bilateral corneal stromal loss in Friesian horses. Animal Genetics, 49(6), 656 - 657. DOI: https://doi.org/10.1111/age.12726
Ameye, L., Aria, D., Jepsen, K., Oldberg, Å., Xu, T. & Young, M. (2002). Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB Journal, 16(7), 673 - 680. DOI: https://doi.org/10.1096/fj.01-0848com
Amri, F., Gunawan, A. & Sumantri, C. (2023). Effect of DGAT1 gene on hot and cold carcass, neck and non-carcass traits in Indonesia sheep. Journal of Animal Production and Processing Technology, 11(1), 48 - 53. DOI: https://doi.org/10.29244/jipthp.11.1.48-53
Bianco, P., Fisher, L. W., Young, M. F., Termine, J. D. & Robey, P. G. (1990). Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. Journal of Histochemistry & Cytochemistry, 38(11), 1549 - 1563. DOI: https://doi.org/10.1177/38.11.2212616
Bowe, M. A., Mendis, D. B. & Fallon, J. R. (2000). The small leucine-rich repeat proteoglycan biglycan binds to α-dystroglycan and is upregulated in dystrophic muscle. Journal of Cell Biology, 148(4), 801 - 810. DOI: https://doi.org/10.1083/jcb.148.4.801
Griffiths, A. J. F., Wessler, S. R., Carroll, S. B. & Doebley, J. (2015). An introduction to genetic analysis (11th ed.). W. H. Freeman and Company.
Christensen, R. (2016). Analysis of variance, design, and regression: Linear modeling for unbalanced data (2nd ed., 636 pp.). Chapman and Hall/CRC. https://doi.org/10.1201/9781315370095. DOI: https://doi.org/10.1201/9781315370095
Chuan-hao, L., Wei, C., Jia-qing, H., Yan-dong, W., Shou-dong, W., Yong-qing, Z. & Hui, W. (2016). miRNA-29a targets COL3A1 to regulate the level of type III collagen in pig. Gene, 592(1), 140 - 147. DOI: https://doi.org/10.1016/j.gene.2016.07.068
Ernawati, D. & Rosida, D. F. (2022). The physicochemical properties of flavor enhancer made from different types of snail protein hydrolysates. International Journal of Food, Agriculture, and Natural Resources, 3(1), 1 - 7. DOI: https://doi.org/10.46676/ij-fanres.v3i1.54
Esenbuğa, N., Macit, M., Karaoğlu, M. M., Aksakal, V., Aksu, M. I., Yörük, M. & Gül, M. (2009). Effect of breed on fattening performance, slaughter and meat quality characteristics of Awassi and Morkaraman lambs. Livestock Science, 123(2-3), 255 - 260. DOI: https://doi.org/10.1016/j.livsci.2008.11.014
Febriana, A., Sutopo, S., Kurnianto, E. & Widiyanto, W. (2022). A novel SNPs of the kiss1 gene strongly associated with litter size in Indonesian goat breeds. Tropical Animal Science Journal, 45(3), 255 - 269. DOI: https://doi.org/10.5398/tasj.2022.45.3.255
Fuller, E., Little, C. B. & Melrose, J. (2016). Interleukin-1α induces focal degradation of biglycan and tissue degeneration in an in-vitro ovine meniscal model. Experimental and Molecular Pathology, 101(2), 214 – 220. DOI: https://doi.org/10.1016/j.yexmp.2016.09.001
Furqon, A., Gunawan, A., Ulupi, N., Suryati, T. & Sumantri, C. (2017). Expression and association of SCD gene polymorphisms and fatty acid compositions in chicken cross. Media Peternakan, 40(3), 151 - 157. DOI: https://doi.org/10.5398/medpet.2017.40.3.151
Han, F., Li, J., Liu, N., Zhao, R., Liu, L., Li, L. & He, J. (2020). Identification and co-expression analysis of long noncoding RNAs and mRNAs involved in the deposition of intramuscular fat in Aohan fine-wool sheep. BMC Genomics, 22(98), 20 - 26. DOI: https://doi.org/10.1186/s12864-021-07385-9
Harahap, R. S., Noor, R. R. & Gunawan, A. (2021). The polymorphism and expression of CYP2E1 gene and its relation to carcass and meat quality of Indonesian lamb. Tropical Animal Science Journal, 44(4), 377 - 385. DOI: https://doi.org/10.5398/tasj.2021.44.4.377
Hasan, N., Choudhary, S., Naaz, N., Sharma, N. & Laskar, R. A. (2021). Recent advancements in molecular marker-assisted selection and applications in plant breeding programmes. Journal of Genetic Engineering & Biotechnology, 19, 128. DOI: https://doi.org/10.1186/s43141-021-00231-1
Heegaard, A., Corsi, A., Danielsen, C. C., Nielsen, K., Jørgensen, H., Riminucci, M. & Bianco, P. (2007). Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation, 115(21), 2731 - 2738. DOI: https://doi.org/10.1161/CIRCULATIONAHA.106.653980
Heezen, L., Abdelaal, T., Putten, M., Aartsma‐Rus, A., Mahfouz, A. & Spitali, P. (2022). Spatial transcriptomics reveal markers of histopathological changes in Duchenne muscular dystrophy mouse models. BioRxiv, 484699, 1 - 25. DOI: https://doi.org/10.1101/2022.03.17.484699
Hernández-Castellano, L. E., Morales-delaNuez, A., Moreno-Indias, I., Torres, A., Sánchez-Macías, D., Capote, J., Castro, N. & Argüello, A. (2013). Carcass and meat quality determination as a tool to promote local meat consumption in outermost regions of Europe. Journal of Applied Animal Research, 41(3), 269 - 276. DOI: https://doi.org/10.1080/09712119.2012.742849
Hsieh, L. T., Nastase, M. V., Zeng-Brouwers, J., Iozzo, R. V. & Schaefer, L. (2014). Soluble biglycan as a biomarker of inflammatory renal diseases. International Journal of Biochemistry & Cell Biology, 54, 223 - 235. DOI: https://doi.org/10.1016/j.biocel.2014.07.020
Hunt, M. C., Honikel, K., Puolanne, E., Kapper, C., Klont, R., Young, J. F. & Algers, A. (2011). Fundamentals in water holding capacity (WHC) of meat. Q-Pork Chains, Learning Resource 6. https://pure.au.dk/portal/en/publications/fundamentals-in-water-holding-capacity-whc-of-meat/.
Jager, N., Hudson, N., Reverter, A., Barnard, R., Café, L., Greenwood, P. & Dalrymple, B. (2013). Gene expression phenotypes for lipid metabolism and intramuscular fat in skeletal muscle of cattle. Journal of Animal Science, 91(3), 1112 - 1128. DOI: https://doi.org/10.2527/jas.2012-5409
Jeong, J. Y., Ibrahim, M., Kim, M. J., So, K., Jeong, Y. D., Park, S., Kim, M. & Lee, H. J. (2017). Comparisons of extracellular matrix-related gene expression levels in different adipose tissues from Korean cattle. Livestock Science, 198, 138 - 146. DOI: https://doi.org/10.1016/j.livsci.2017.02.020
Jørgensen, L., Jepsen, P., Boysen, A., Dalgaard, L., Hvid, L., Ørtenblad, N. & Schrøder, H. (2017). Sparc interacts with actin in skeletal muscle in vitro and in vivo. American Journal of Pathology, 187(2), 457 - 474. DOI: https://doi.org/10.1016/j.ajpath.2016.10.013
Kayan, A., Uddin, M. J., Kocamis, H., Tesfaye, D., Looft, C., Tholen, E., Schellander, K. & Cinar, M. U. (2013). Association and expression analysis of porcine HNF1A gene related to meat and carcass quality traits. Meat Science, 94(4), 474 - 479. DOI: https://doi.org/10.1016/j.meatsci.2013.04.015
Kram, V., Shainer, R., Jani, P., Meester, J. A. N., Loeys, B. & Young, M. F. (2020). Biglycan in the skeleton. Journal of Histochemistry & Cytochemistry, 68(11), 747 - 762. DOI: https://doi.org/10.1369/0022155420937371
Lee, P. Y., Costumbrado, J., Hsu, C. Y. & Kim, Y. H. (2012). Agarose gel electrophoresis for the separation of DNA fragments. Journal of Visualized Experiments, 62, 3923. DOI: https://doi.org/10.3791/3923-v
Leiphart, R. J., Pham, H., Harvey, T., Komori, T., Kilts, T. M., Shetye, S. S., Weiss, S. N., Adams, S. M., Birk, D. E., Soslowsky, L. J. & Young, M. F. (2021). Coordinate roles for collagen VI and biglycan in regulating tendon collagen fibril structure and function. Matrix Biology Plus, 13, 100099. DOI: https://doi.org/10.1016/j.mbplus.2021.100099
Listyarini, K., Sumantri, C., Rahayu, S., Islam, A., Akter, S. H., Uddin, M. J. & Gunawan, A. (2023). Hepatic transcriptome analysis reveals genes, polymorphisms, and molecules related to lamb tenderness. Animals, 13(4), 674. DOI: https://doi.org/10.3390/ani13040674
Nallanthighal, S., Heiserman, J. P. & Cheon, D. J. (2019). The role of the extracellular matrix in cancer stemness. Frontiers in Developmental Biology, 86(7), 1 - 14. DOI: https://doi.org/10.3389/fcell.2019.00086
Nastase, M. V., Young, M. F. & Schaefer, L. (2012). Biglycan: A multivalent proteoglycan providing structure and signals. Journal of Histochemistry & Cytochemistry, 60(12), 963 - 975. DOI: https://doi.org/10.1369/0022155412456380
Nei, M. & Kumar, S. (2000). Molecular evolution and phylogenetics. Oxford University Press, USA. DOI: https://doi.org/10.1093/oso/9780195135848.001.0001
Neufeld, E. B., Zadrozny, L. M., Phillips, D., Aponte, A., Yu, Z. X. & Balaban, R. S. (2014). Decorin and biglycan retain LDL in disease-prone valvular and aortic subendothelial intimal matrix. Atherosclerosis, 233(1), 113 - 121. DOI: https://doi.org/10.1016/j.atherosclerosis.2013.12.038
Oswalt, H., Smith, S., Williams, B., Ferdous, F., Burns, M., Bridges, W., Scott, T. & Dunn, H. W. (2021). Methodology to identify candidate genes from beef carcass traits at weaning: A pilot study. Animal Genetics, 20, 1 - 8. DOI: https://doi.org/10.1016/j.angen.2021.200113
Petersen, G. V. (1984). Cross-sectional studies of ultimate pH in lambs. New Zealand Journal of Agricultural Research, 32, 51 - 57. DOI: https://doi.org/10.1080/00480169.1984.11728698
Robinson, K. A., Sun, M., Barnum, C. E., Weiss, S. N., Huegel, J., Shetye, S. S. & Birk, D. E. (2017). Decorin and biglycan are necessary for maintaining collagen fibril structure, fiber realignment, and mechanical properties of mature tendons. Matrix Biology, 64, 81 - 93. DOI: https://doi.org/10.1016/j.matbio.2017.08.004
Salimi, H., Suzuki, A., Habibi, H., Orita, K., Hori, Y., Yabu, A. & Nakamura, H. (2021). Biglycan expression and its function in human ligamentum flavum. Scientific Reports, 11(1), 4867. DOI: https://doi.org/10.1038/s41598-021-84363-x
Saputra, F., Jakaria, J., Anggraeni, A. & Sumantri, C. (2020). Genetic diversity of Indonesian swamp buffalo based on microsatellite markers. Tropical Animal Science Journal, 43(3), 191 - 196. DOI: https://doi.org/10.5398/tasj.2020.43.3.191
Schiaffino, S. & Mammucari, C. (2011). Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: Insights from genetic models. Skeletal Muscle, 1(1), 1 - 14. DOI: https://doi.org/10.1186/2044-5040-1-4
Schönherr, E., Witsch-Prehm, P., Harrach, B., Robenek, H., Rauterberg, J. & Kresse, H. (1995). Interaction of biglycan with type I collagen. Journal of Biological Chemistry, 270, 2776 - 2783. DOI: https://doi.org/10.1074/jbc.270.6.2776
Sevane, N., Armstrong, E., Cortés, O., Wiener, P., Wong, R. & Dunner, S. (2013). Association of bovine meat quality traits with genes included in the PPARG and PPARGC1A networks. Meat Science, 94(3), 328 - 335. DOI: https://doi.org/10.1016/j.meatsci.2013.02.014
Silver, N., Best, S., Jiang, J. & Thein, S. L. (2006). Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Molecular Biology, 7, 33. DOI: https://doi.org/10.1186/1471-2199-7-33
Stromer, M. (1998). The cytoskeleton in skeletal, cardiac, and smooth muscle cells. Histology & Histopathology, 13(1), 283 - 291.
Sujarwanta, R. O., Afidah, U., Suryanto, E., Rusman, Triyannanto, E. & Hoffman, L. C. (2024). Goat and sheep meat production in Indonesia. Sustainability, 16(11), 4448. DOI: https://doi.org/10.3390/su16114448
Tang, T., Thompson, J., Wilson, P., Nelson, C., Williams, K. & Tannock, L. (2012). Decreased body fat, elevated plasma transforming growth factor-β levels, and impaired BMP4-like signaling in biglycan-deficient mice. Connective Tissue Research, 54(1), 5 - 13. DOI: https://doi.org/10.3109/03008207.2012.715700
Tripathi, A. K., Koringa, P. G., Jakhesara, S. J., Ahir, V. B., Ramani, U. V., Bhatt, V. D., Sajnani, M. R., Patel, D. A., Joshi, A. J., Shanmuga, S. J., Rank, D. N. & Joshi, C. G. (2012). A preliminary sketch of horn cancer transcriptome in Indian zebu cattle. Gene, 493, 124 - 131. DOI: https://doi.org/10.1016/j.gene.2011.11.007
Wahyuni, D., Priyanto, R. & Nuraini, H. (2018). Meat physical and sensoric quality of Brahman cross cattle fed pineapple waste as fiber source. Jurnal Pertanian, 09(2), 1481. DOI: https://doi.org/10.30997/jp.v9i2.1481
Wang, Z. (2023). Identifying crucial biomarkers in osteoporosis and ulcerative colitis through bioinformatics analysis of co-expressed genes. Cureus, 15(9), 1 - 16. DOI: https://doi.org/10.7759/cureus.45063
Ward, M. G. & Ajuwon, K. M. (2012). Biglycan deletion alters adiponectin expression in murine adipose tissue and 3T3-L1 adipocytes. PLoS One, 7(11), e50554. DOI: https://doi.org/10.1371/journal.pone.0050554
Wigginton, J. E., Cutler, D. J. & Abecasis, G. R. (2005). A note on exact tests of Hardy-Weinberg equilibrium. American Journal of Human Genetics, 76(5), 887 - 893. DOI: https://doi.org/10.1086/429864
Zhang, X., Liao, H., Yanxia, Q., Wang, Y., Pang, Y., Zhang, Z. & Liu, P. (2016). The relationships of collagen and ADAMTS2 expression levels with meat quality traits in cattle. Indian Journal of Animal Research, 52, 167 - 172. DOI: https://doi.org/10.18805/ijar.v0iOF.4557
Zhao, X., Chen, J., Sun, H., Zhang, Y. & Zou, D. (2022). New insights into fibrosis from the ECM degradation perspective: the macrophage-MMP-ECM. Cell & Bioscience, 12(1), 1 - 10. DOI: https://doi.org/10.1186/s13578-022-00856-w
Zhao, L., Liang, J., Zhong, W., Han, C., Liu, D. & Chen, X. (2022). Expression and prognostic analysis of BGN in head and neck squamous cell carcinoma. Gene, 827, 146461. DOI: https://doi.org/10.1016/j.gene.2022.146461
Zhou, Z., Xu, M.-J. & Gao, B. (2016). Hepatocytes: A key cell type for innate immunity. Cell & Molecular Immunology, 13(3), 301 - 315. DOI: https://doi.org/10.1038/cmi.2015.97
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Bulgarian Journal of Agricultural Science

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

