Sains Malaysiana 52(12)(2023): 3357-3370

http://doi.org/10.17576/jsm-2023-5212-02

Gene Expression, Growth Performance and Body Composition of Labeo rohita Fingerlings Fed on Polyphenols Supplement

(Pengekspresan Gen, Prestasi Tumbesaran dan Komposisi Badan Anak Labeo rohita Diberi Makan Suplemen Polifenol)

SYED MAKHDOOM HUSSAIN^1,*, MUNIBA JAMIL¹, SHAFAQAT ALI^2,3, MUHAMMAD MUDASSAR SHAHZAD⁴, MAJID HUSSAIN⁵, NISAR AHMAD⁶ & DANISH RIAZ⁴

¹Fish Nutrition Lab, Department of Zoology, Government College University, Faisalabad, Punjab 38000, Pakistan

²Department of Environmental Science, College of Agriculture and Environmental Sciences, Government College University, Faisalabad, Punjab 38000, Pakistan

³Department of Biological Sciences and Technology, China Medical University, Taichung 40402, Taiwan
⁴Department of Zoology, Division Science and Technology, University of Education, Lahore, Pakistan

⁵Department of Fisheries and Aquaculture, University of Okara, Pakistan

⁶Department of Zoology, University of Jhang, Pakistan

Received: 19 December 2022/Accepted: 30 November 2023

Abstract

The aim of this research was to investigate the impacts of polyphenols-supplemented diet on growth, body composition and gene expressions of insulin-like growth factor (IGF) and growth hormone (GH) in Labeo rohita fingerlings fed canola meal-based diets. Two plant extracts; Salvadora persica and Salvadora oleoides were used to assess the efficacy of L. rohita. Twelve test diets, including control (no supplementation) and supplemented with S. persica, S. oleoidesand their mixture at the levels of 200, 400 and 800 mg/kg, were formulated. The gene expression of IGFs and GH was observed to be regulated significantly (p< 0.05) in the liver tissue of fingerlings when fed with supplemented diet. The highest expression of GH was observed at 200 mg/kg mixture diet. The results of growth performance showed that maximum weight gain% (215%) and SGR (1.63) was recorded at 200 mg/kg mixture diet. The results of carcass analysis showed that they were significantly (p< 0.05) influenced by supplemented diet when compared with control diet. As growth performance is under genetic control, the synthesis and release of IGF are stimulated by binding of GH to receptors present in the liver. Conclusively, the results showed that rohu fingerlings shown the best results of growth performance, body composition and gene expression of IGF and GH, when fed on mixture of S. persica and S. oleoides at 200 mg/kg.

Keywords: Gene expression; growth hormone; growth performance; insulin-like growth factors; polyphenols

Abstrak

Matlamat penyelidikan ini adalah untuk mengkaji kesan diet tambahan polifenol ke atas tumbesaran, komposisi badan dan pengekspresan gen faktor tumbesaran seperti insulin (IGF) dan hormon tumbesaran (GH) pada anak Labeo rohita yang diberi diet berasaskan canola. Dua ekstrak tumbuhan; Salvadora persica dan Salvadora oleoides digunakan untuk menilai keberkesanan L. rohita. Dua belas ujian diet, termasuk kawalan (tiada suplemen) dan tambahan suplemen S. persica, S. oleoides serta gabungannya pada tahap 200, 400 dan 800 mg/kg telah diformulasi. Pengekspresan gen IGF dan GH diperhatikan telah dikawal dengan ketara (p<0.05) dalam tisu hati anak apabila diberi makanan tambahan. Pengekspresan tertinggi GH diperhatikan pada diet gabungan 200 mg/kg. Keputusan prestasi tumbesaran menunjukkan peningkatan% berat badan maksimum (215%) dan SGR (1.63) direkodkan pada diet gabungan 200 mg/kg. Keputusan analisis karkas menunjukkan bahawa mereka secara signifikan (p< 0.05) dipengaruhi oleh diet tambahan jika dibandingkan dengan diet kawalan. Oleh kerana prestasi tumbesaran berada di bawah kawalan genetik, sintesis dan pembebasan IGF dirangsang oleh pengikatan GH kepada reseptor yang terdapat dalam hati. Secara konklusif, keputusan menunjukkan bahawa anak rohu menunjukkan hasil terbaik dalam prestasi tumbesaran, komposisi badan dan pengekspresan gen IGF dan GH apabila diberi makan gabungan S. persica dan S. oleoides pada 200 mg/kg.

Kata kunci: Faktor tumbesaran seperti insulin; hormon tumbesaran; pengekspresan gen; polifenol; prestasi tumbesaran

REFERENCES

Abdel-Tawwab, M. & Monier, M.N. 2018. Stimulatory effect of dietary taurine on growth performance, digestive enzymes activity, antioxidant capacity, and tolerance of common carp, Cyprinus carpio L., fry to salinity stress. Fish Physiology and Biochemistry 44(2): 639-649. https://doi.org/10.1007/s10695-017-0459-8

Adeshina, I., Jenyo‐Oni, A., Emikpe, B.O., Ajani, E.K. & Abdel‐Tawwab, M. 2019. Stimulatory effect of dietary clove, Eugenia caryophyllata, bud extract on growth performance, nutrient utilization, antioxidant capacity, and tolerance of African catfish, Clarias gariepinus (B.), to Aeromonas hydrophila infection. Journal of the World Aquaculture Society 50(2): 390-405. https://doi.org/10.1111/jwas.12565

Alhazzaa, R., Nichols, P.D. & Carter, C.G. 2019. Sustainable alternatives to dietary fish oil in tropical fish aquaculture. Reviews in Aquaculture 11(4): 1195-1218. https://doi.org/10.1111/raq.12287

Amin, A., El Asely, A., Abd El-Naby, A.S., Samir, F., El-Ashram, A., Sudhakaran, R. & Dawood, M.A. 2019. Growth performance, intestinal histomorphology and growth-related gene expression in response to dietary Ziziphus mauritiana in Nile tilapia (Oreochromis niloticus). Aquaculture 512: 734301. https://doi.org/10.1016/j.aquaculture.2019.734301

Association of Official Analytical Chemists (AOAC). 2005. Official Methods of Analysis. 15th ed. Washington: Association of Official Analytical Chemists. p. 1094.

Béné, C., Arthur, R., Norbury, H., Allison, E.H., Beveridge, M., Bush, S., Campling, L., Leschen, W., Little, D., Squires, D. & Thilsted, S.H. 2016. Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence. World Development 79: 177-196. https://doi.org/10.1016/j.worlddev.2015.11.007 

Blom, J.H., Dabrowski, K. & Ebeling, J. 2000. Vitamin C requirements of the Angelfish Pterophylum scalare. Journal of the World Aquaculture Society 31(1): 115-118. https:// doi.org/2F10.1111/2Fj.1749-7345.2000.tb00705.x

Burel, C. & Kaushik, S.J. 2008. Use of rapeseed/canola in diets of aquaculture species. In Alternative Protein Sources in Aquaculture Diets, edited by Lim, C., Webster, C.D. & Lee, C-S. New York and London: Haworth Press. pp. 343-408. doi: 10.3923/jfas.2011.22.36

Cheng, C.H., Guo, Z.X., Ye, C.X. & Wang, A.L. 2018. Effect of dietary astaxanthin on the growth performance, non-specific immunity, and antioxidant capacity of pufferfish (Takifugu obscurus) under high temperature stress. Fish Physiology and Biochemistry 44(1): 209-218. https://doi.org/10.1016/j.aquaculture.2019.734341

Deng, J., An, Q., Bi, B., Wang, Q., Kong, L., Tao, L. & Zhang, X. 2011. Effect of ethanolic extract of propolis on growth performance and plasma biochemical parameters of rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemitry 37(4): 959-967. https://doi.org/10.1007/s10695-011-9493-0

El-Bakary, N.E.R. & El-Gammal, H.L. 2010. Comparative histological, histochemical and ultrastructural studies on the liver of flathead grey mullet (Mugil cephalus) and sea bream (Sparus auratus). Global Veterinaria 4(6): 548-553.

Geetha, K., Manavalan, R. & Venkappayya, D. 2010. Control of urinary risk factors of stone formation by Salvadora persica in experimental hyperoxaluria. Methods and Findings in Experimental and Clinical Pharmacology 32(9): 623-629. https://doi.org/10.1358/mf.2010.32.9.1549114

Glencross, B. 2016. Understanding the nutritional and biological constraints of ingredients to optimize their application in aquaculture feeds. In Aquafeed Formulation, edited by Nates, S.F. Academic Press: New York. pp. 32-73. https://doi.org/10.1016/b978-0-12-800873-7.00003-8 

Gómez-Requeni, P., Mingarro, M., Calduch-Giner, J.A., Médale, F., Martin, S.A.M., Houlihan, D.F., Kaushik, S.  & Pérez-Sánchez, J. 2004. Protein growth performance, amino acid utilization and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232(1-4): 493-510. https://doi.org/10.1016/S0044-8486(03)00532-5

Halliwell, B. 2007. Dietary polyphenols: good, bad, or indifferent for your health? Cardiovascular Research 73(2): 341-347. https://doi.org/10.1016/j.cardiores.2006.10.004 

Hoseinifar, S.H., Dadar, M., Khalili, M., Cerezuela, R. & Esteban, M.Á. 2017. Effect of dietary supplementation of palm fruit extracts on the transcriptomes of growth, antioxidant enzyme and immune‐related genes in common carp (Cyprinus carpio) fingerlings. Aquaculture Research 48(7): 3684-3692. doi:10.1111/are.13192

Hussain, S.M., Nisar, A., Farhat, J., Arshad, J., Nosheen, A., Majid, H., Shahtaj, A., Arsalan, M.Z.H., Danish, R. & Shahzad, M.M. 2015. Effects of citric acid and phytase supplementation on nutrient digestibility and growth performance of Cirrhinus mrigala fingerlings fed on corn gluten (30%) meal based diets. International Journal of Biosciences 6(7): 82-91. http://www.innspub.net/wp-content/upl

Irm, M., Taj, S., Jin, M., Luo, J., Andriamialinirina, H.J.T. & Zhou, Q. 2020. Effects of replacement of fish meal by poultry by-product meal on growth performance and gene expression involved in protein metabolism for juvenile black sea bream (Acanthoparus schlegelii). Aquaculture 528: 735544. https://doi.org/10.1016/j.aquaculture.2020.735544

Jahazi, M.A., Hoseinifar, S.H., Jafari, V., Hajimoradloo, A., Van Doan, H. & Paolucci, M. 2020. Dietary supplementation of polyphenols positively affects the innate immune response, oxidative status, and growth performance of common carp, Cyprinus carpio L. Aquaculture 517: 734709. doi: https://doi.org/10.1016/j.aquaculture.2019.734709

Kayama, K., Kanno, M., Chisaki, N., Tanaka, M., Yao, R., Hanazono, K. & Endoh, D. 2021. Prediction of PCR amplification from primer and template sequences using recurrent neural network. Scientific Reports 11(1): 7493. https://doi.org/10.1038/s41598-021-86357-1

Kumar, S., Sándor, Z.J., Nagy, Z., Fazekas, G., Havasi, M., Sinha, A.K., De Boeck, G. & Gál, D. 2017. Potential of processed animal protein versus soybean meal to replace fish meal in practical diets for European catfish (Silurus glanis): Growth response and liver gene expression. Aquaculture Nutrition 23(5): 1179-1189. https://doi.org/10.1111/ANU.12487

Landero, J.L., Beltranena, E. & Zijlstra, R.T. 2012. The effect of feeding lentil on growth performance and diet nutrient digestibility in starter pigs. Animal Feed Science and Technology 174(1): 108-112. https://doi.org/10.1016/j.anifeedsci.2012.02.010

Lee, K.J. & Dabrowski, K. 2004. Long-term effects and interactions of dietary vitamins C and E on growth and reproduction of yellow perch, Perca flavescens. Aquaculture 230(1-4): 377-389. doi: 10.1016/S0044-8486(03)00421-6

Liang, J.J., Tian, L.X., Liu, Y.J., Yang, H.J. & Liang, G.Y. 2012. Dietary magnesium requirement and effects on growth and tissue magnesium content of juvenile grass carp (Ctenopharyngodon idella). Aquaculture Nutrition 18(1): 56-64. https://doi.org/10.1111/j.1365-2095.2011.00876.x

Livak, K.J. & Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4): 402-408. https://doi.org/10.1006/meth.2001.1262

Maqsood, S., Benjakul, S., Abushelaibi, A. & Alam, A. 2014. Phenolic compounds and plant phenolic extracts as natural antioxidants in prevention of lipid oxidation in seafood: A detailed review. Comprehensive Reviews in Food Science and Food Safety 13(6): 1125-1140. https://doi.org/10.1111/1541-4337.12106

Mathur, S. 2015. Medicinally potent and highly salt tolerant plant of arid zone Salvadora persica (Meswak): A review. Journal of Plant Sciences 3: 45-49. https://doi.org/10.11648/J.JPS.S.2015030101.17s

Miandare, H.K., Farvardin, S., Shabani, A., Hoseinifar, S.H. & Ramezanpour, S.S. 2016. The effects of galactooligosaccharide on systemic and mucosal immune response, growth performance and appetite related gene transcript in goldfish (Carassius auratus gibelio). Fish and Shellfish Immunology 55: 479-483. https://doi.org/10.1016/j.fsi.2016.06.020

Midhun, S.J., Arun, D., Edatt, L., Sruthi, M.V., Thushara, V.V., Oommen, O.V., Sameer, Kumar, V.B. & Divya, L. 2016. Modulation of digestive enzymes, GH, IGF-1 and IGF-2 genes in the teleost, Tilapia (Oreochromis mossambicus) by dietary curcumin.   Aquaculture International 24(5): 1277-1286. https://doi.org/10.1007/s10499-016-9984-1 

Ming, J., Xie, J., Xu, P., Ge, X., Liu, W. & Ye, J. 2012. Effects of emodin and vitamin C on growth performance, biochemical parameters and two HSP70s mRNA expression of Wuchang bream (Megalobrama amblycephalaYih) under high temperature stress. Fish and Shellfish Immunology 32(5): 651-661. https://doi.org/10.1016/j.fsi.2012.01.008

Moustafa, E.M., Dawood, M.A., Assar, D.H., Omar, A.A., Elbialy, Z.I., Farrag, F.A., Shukry, M. & Zayed, M.M. 2020. Modulatory effects of fenugreek seeds powder on the histopathology, oxidative status, and immune related gene expression in Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Aquaculture 515: 734589. https://doi.org/10.1016/j.aquaculture.2019.734589

Mun, S.H., You, J.H., Oh, H.J., Lee, C.H., Baek, H.J., Lee, Y.D. & Kwon, J.Y. 2019. Expression patterns of growth related genes in juvenile red spotted grouper (Epinephelus akaara) with different growth performance after size grading. Development and Reproduction 23(1): 35. https://doi. 10.12717/DR.2019.23.1.035

Mutch, D.M., Wahli, W. & Williamson, G. 2005. Nutrigenomics and nutrigenetics: the emerging faces of nutrition. The FASEB Journal 19(12): 1602-1616. https://doi.org/10.1096/fj.05-3911rev

Nijveldt, R.J., van Nood, E.L.S., van Hoorn, D.E., Boelens, P.G., van Norren, K. & van Leeuwen, P.A. 2001. Flavonoids: A review of probable mechanisms of action and potential applications. The American Journal of Clinical Nutrition 74(4): 418-425. https://doi.org/10.1093/AJCN%2F74.4.418

Omnes, M.H., Le Goasduff, J., Le Delliou, H., Le Bayon, N., Quazuguel, P. & Robin, J.H. 2017. Effects of dietary tannin on growth, feed utilization and digestibility, and carcass composition in juvenile European seabass (Dicentrarchus labrax L.). Aquaculture Reports 6: 21-27. https://doi.org/10.1016/j.aqrep.2017.01.004

Ranjan, A., Jain, K.K., Srivastava, P.P. & Muralidhar, P.A. 2018. Dietary energy requirement of Pangasianodon hypophthalmus (Sauvage, 1878) juveniles reared at two temperatures. Turkish Journal of Fisheries and Aquatic Sciences 18(1): 101-108. https:// doi.org/2F10.4194/2F1303-2712-v18_1_11

Reverter, M., Tapissier‐Bontemps, N., Sasal, P. & Saulnier, D. 2017. Use of medicinal plants in aquaculture. In Diagnosis and Control of Diseases of Fish and Shellfish, 1st ed., edited by Austin, B. & Newaj-Fyzul, A. John Wiley & Sons Ltd. pp. 223-261. doi: 10.1002/9781119152125.ch9

Safari, R., Hoseinifar, S.H., Imanpour, M.R., Mazandarani, M., Sanchouli, H. & Paolucci, M. 2020. Effects of dietary polyphenols on mucosal and humoral immune responses, antioxidant defense and growth gene expression in beluga sturgeon (Huso huso). Aquaculture 528: 735494. https://doi.org/10.1016/j.aquaculture.2020.735494

Salehi, P. & Sh, M.D. 2006. Comparison of the antibacterial effects of persica mouthwash with chlorhexidine on streptococcus mutans in orthodontic patients. DARU Journal of Pharmaceutical Sciences 14(4): 178-182.

Salin, K.R., Arun, V.V., Mohanakumaran Nair, C. & Tidwell, J.H. 2018. Sustainable aquafeed. In Sustainable Aquaculture, edited by Hai, F., Visvanathan, C. & Boopathy, R. Springer, Cham. pp. 123-151. https://doi.org/10.1007/978-3-319-73257-2_4

Singh, P.K., Gaur, S.R. & Chari, M.S. 2006. Effect of varying protein levels on the growth of Indian Major Carp Rohu, Labeo rohita (Hamilton). International Journal of Zoological Research 2: 186-191. https://dx.doi.org/10.3923/ijzr.2006.186.191

Snedecor, G.W. & Cochran, W.G. 1991. Statistical Methods. 8th ed.  Iowa State University Press. p. 503.

Steel, R.G.D., Torrie, J.H. & Dickey, D.A. 1996. Principles and Procedures of Statistics. 3rd ed. New York: McGraw Hill International Book Co. pp. 336-352.

Tan, X., Sun, Z., Huang, Z., Zhou, C., Lin, H., Tan, L., Xun, P. & Huang, Q. 2017. Effects of dietary hawthorn extract on growth performance, immune responses, growth-and immune-related genes expression of juvenile golden pompano (Trachinotus ovatus) and its susceptibility to Vibrio harveyi infection. Fish and Shellfish Immunology 70: 656-664. https://doi.org/10.1016/j.fsi.2017.09.041

Tatar, M., Bartke, A. & Antebi, A. 2003. The endocrine regulation of aging by insulin-like signals. Science 299(5611): 1346-1351. https://doi.org/10.1126/science.1081447

Turan, F. & Akyurt, I. 2005. Effects of red clover extract on growth performance and body composition of African catfish Clarias gariepinus. Fisheries Science 71(3): 618-620. https://doi.org/2F10.1111/2Fj.1444-2906.2005.01006.x

Verma, R., Purohit, S., Bhandari, A., Kumar, B. & Priyanka, P. 2009. Salvadora persica L (tooth brush tree): A review. Journal of Pharmacy Research 2(12): 1809-1812.

Wahab, M.A., Rahman, M.M. & Milstein, A. 2002. The effect of common carp, Cyprinus carpio (L.) and mrigal, Cirrhinus mrigala (Hamilton) as bottom feeders in major Indian carp polycultures. Aquaculture Research 33(8): 547-556. https://doi.org/10.1046/j.1365-2109.2002.00654.x

Wang, X., Kim, K.W., Bai, S.C., Huh, M.D. & Cho, BY. 2003. Effects of the different levels of dietary vitamin C on growth and tissue ascorbic acid changes in parrot fish (Oplegnathus fasciatus). Aquaculture 215(1-4): 203-211. http://dx.doi.org/10.5713/ajas.14.0532

Xu, Z., Li, X., Yang, H., Liang, G., Gao, B. & Leng, X. 2019. Dietary quercetin improved the growth, antioxidation, and flesh quality of grass carp (Ctenopharyngodon idella). Journal of the World Aquaculture Society 50(6): 1182-1195. https://doi.org/10.1111/jwas.12663 

Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S. & Madden, T. L. 2012. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13: 1-11. https://doi.org/10.1186/1471-2105-13-134

Yigit, N.O. & Olmez, M. 2009. Canola meal as an alternative protein source in diets for fry of tilapia (Oreochromis niloticus). Israeli Journal of Aquaculture – Bamidgeh 61: 35-41. https://doi.org/10.46989/001c.20535 

Zhang, C. & Wen, A. 2012. Different of chlorogenic acid doses on growth performance, non-specific immunity and antioxidant functions of Cyprinus carpio var. Journal of Sichuan Agricultural University 30: 92-97. https://doi.org/10.1111/ANU.12500

Zhong, H., Zhou, Y., Liu, S., Tao, M., Long, Y., Liu, Z. & Liu, Y. 2012. Elevated expressions of GH/IGF axis genes in triploid Crucian carp. General and Comparative Endocrinology 178(2): 291-300. https://doi.org/10.1016/j.ygcen.2012.06.006

Zhong, L., Hu, Y., Hu, Y., Li, J., Tian, Y., Chen, J., Ai, Q, & Xiao, T. 2020. Effects of dietary tea polyphenols on growth, immunity and lipid metabolism of juvenile black carp Mylopharyngodon piceus. Aquaculture Research 51(2): 569-576. https://doi.org/10.1111/are.14403

*Corresponding author; email: drmakhdoomhussain@gcuf.edu.pk