Please wait a minute...
Journal of Integrative Agriculture  2016, Vol. 15 Issue (06): 1355-1363    DOI: 10.1016/S2095-3119(15)61281-3
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Effect of feeding transgenic cry1Ab/cry1Ac rice on indices of immune function in broilers
LIU Ran-ran1, 2, ZHAO Gui-ping1, 2, ZHENG Mai-qing1, 2, LIU Jie1, ZHANG Jing-jing1, LI Peng1, LI Qing-he1, FENG Jing-hai1, 2, ZHANG Min-hong1, 2, WEN Jie1, 2
1 Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2 State Key Laboratory of Animal Nutrition, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract    The safety of feeding transgenic cry1Ab/cry1Ac rice (a genetically modified (GM) rice variety) to broilers was examined from an immunological perspective. Hatchling Arbor Acres chickens (240) were assigned to two dietary treatments (diets containing GM or non-GM rice) with 12 replicates per group and 10 birds per replicate. Traits were measured on one randomly selected bird from each replicate at d 21 and 42. The 42-d feeding trial revealed that cry1Ab/cry1Ac rice had no significant effect relative to non-GM rice on body weight and the immune organ indices. No significant pathological lesion in the spleen and bursa of Fabricius was found in the GM rice group. There were no significant differences in serum concentrations of immunoglobulin Y (IgY), IgM, interleukin 4 (IL-4) and IL-6 between the two groups at d 21 or 42, except for IL-6 being higher (P<0.05) in the GM-fed chickens at d 42. There were no differences in the T and B lymphocyte transformation rate and CD4+/CD8+ ratio between the two groups at d 42. Additionally, there was no significant difference between the two diets in expression of relevant genes viz. the major histocompatibility complex class II beta chain (BLB2), interferon beta 1 (IFNβ), tumour necrosis factor alpha-like (TNFα) and toll-like receptor 4 (TLR4) in the spleen and bursa of Fabricius. All the data demonstrated that transgenic cry1Ab/cry1Ac rice had no adverse effect on these aspects of immune function of broilers during 42-d feeding trial. Transgenic rice was therefore indistinguishable from non-GM rice in terms of short-term feeding in chickens.  
Keywords:  transgenic        cry1Ab/cry1Ac gene        rice        broiler        immune trait        gene expression  
Received: 09 March 2015   Accepted:

The research was supported by the grants from the National Science and Technology Major Project of the Ministry of Science and Technology of China (2012ZX08011001-005), the Agricultural Science and Technology Innovation Program, China (ASTIP-IAS04) and the Earmarked Fund for Modern Agro-Industry Technology Research System, China (CARS-42).

Corresponding Authors:  WEN Jie, Tel: +86-10-62815856, Fax: +86-10-62816018, E-mail:   

Cite this article: 

LIU Ran-ran, ZHAO Gui-ping, ZHENG Mai-qing, LIU Jie, ZHANG Jing-jing, LI Peng, LI Qing-he, FENG Jing-hai, ZHANG Min-hong, WEN Jie. 2016. Effect of feeding transgenic cry1Ab/cry1Ac rice on indices of immune function in broilers. Journal of Integrative Agriculture, 15(06): 1355-1363.

Bednarek D, Dudek K, Kwiatek K, Swi?tkiewicz M, Swi?tkiewicz S, Strzetelski J. 2013. Effect of a diet composed of genetically modified feed components on the selected immune parameters in pigs, cattle, and poultry. Bulletin of the Veterinary Institute in Pulawy, 57, 209–217.

Borish L, Rosenbaum R, Albury L, Clark S. 1989. Activation of neutrophils by recombinant interleukin 6. Cellular Immunology, 121, 280–289.

Cao S, He X, Xu W, Luo Y, Ran W, Liang L, Dai Y, Huang K. 2012. Potential allergenicity research of Cry1C protein from genetically modified rice. Regulatory Toxicology and Pharmacology, 63, 181–187.

Chen M, Shelton A, Ye G. 2011. Insect-resistant genetically modified rice in China: From research to commercialization. Annual Review of Entomology, 56, 81–101.

Chen X P, Zuo Q, Piao J H. 2004. Immunotoxicologic assessment of transgenic rice. Journal of Hygiene Research,  33, 77–79. (in Chinese)

Cromwell G L, Henry B J, Scott A L, Gerngross M F, Dusek D L, Fletcher D W. 2005. Glufosinate herbicide-tolerant (LibertyLink) rice vs. conventional rice in diets for growing-finishing swine. Journal of Animal Science, 83, 1068–1074.

Ferro P J, Swaggerty C L, He H, Rothwell L, Kaiser P, Kogut M H. 2005. Recombinant chicken IL-6 does not activate heterophils isolated from day-old chickens in vitro. Developmental & Comparative Immunology, 29, 375–383.

Finamore A, Roselli M, Britti S. 2008. Intestinal and peripheral immune response to MON810 maize ingestion in weaning and old mice. Journal of Agriculture and Food Chemistry, 56, 533–539.

Gaur U, Aggarwal B. 2003. Regulation of proliferation, survival and apoptosis by members of the TNF super family. Biochemical Pharmacology, 66, 1403–1408.

High S M, Cohen M B, Shu Q Y, Altosaar I. 2004. Achieving successful deployment of Bt rice. Trends in Plant Science, 9, 286–292.

Iqbal M, Philbin V J, Smith A L. 2005. Expression patterns of chicken toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Veterinary Immunology and Immunopathology, 4, 117–127.

Isaacs A, Lindenmann J. 1957. Virus interference. I. The interferon. Proceeding of The Royal Society (B: Biological Sciences), 147, 258–267.

James C. 2014. Global Status of Commercialized Biotech/Gm Crops. ISAAA, Brief No. 49. ISAAA, Ithaca, NY.

Jones S A. 2005. Direct transition from innate to acquired immunity: Defining a role for IL-6. The Journal of Immunology, 175, 3463–3468.

Kroghsbo S, Madsen C, Poulsen M. 2008. Immunotoxicological studies of genetically modified rice expressing PHA-E lectin or Bt toxin in wistar rats. Toxicology, 245, 24–34.

König A, Cockburn A, Crevel R W, Debruyne E, Grafstroem R, Hammerling U, Kimber I, Knudsen I, Kuiper H A, Peijnenburg A A, Penninks A H, Poulsen M, Schauzu M, Wal J M. 2004. Assessment of the safety of foods derived from genetically modified (GM) crops. Food and Chemical Toxicology, 42, 1047–1088.

Kuiper H A, Kleter G A, Noteborn H P, Kok E J. 2001. Assessment of the food safety issues related to genetically modified foods. The Plant Journal, 27, 503–528.

Li B, Wei K, Yang S F, Yang Y, Zhang Y B, Zhu F J, Wang D, Zhu R L. 2015. Immunomodulatory effects of Taishan Pinus massoniana pollenpolysaccharide and propolis on immunosuppressed chickens. Microbial Pathogenesis, 78, e13.

Liu R R, Wen J. 2013. Cultivation and developments in the field of GM plants in Asia. In: Flachowsky G, ed., Animal Nutrition with Transgenic Plants. CABI Biotechnology Series. CABI, Oxfordshire, UK. pp. 193–200.

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, 402–408.

Maqbool S B, Riazuddin S, Loc N T, Gatehouse A R, Gatehouse J A, Christou P. 2001. Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Molecular Breeding, 7, 85–93.

Medzhitov R, Preston-Hurlburt P, Janeway C A. 1997. A human homologue of the drosophila toll protein signals activation of adaptive immunity. Nature, 388, 394–397.

Mosmann T R, Coffman R L. 1989. Thl and Th2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology, 7, 145–173.

NRC (National Research Council). 1994. Nutrient Requirements of Poultry. National Academy Press, Washington, D.C.

NY/T 33-2004 (Agriculture Standard of The People’s Republic of China). 2004. Feeding standard of chicken. Ministry of Agriculture of the People’s Republic of China, Beijing.

Reichert M, Kozaczynski W, Karpinska T A, Bocian L, Jasik A, Kycko A, Swi?tkiewicz M, Swi?tkiewicz S, Furgal-Dier?uk I, Arczewska-Wlosek A. 2012. Histopathological study of internal organs of experimental animals fed with genetically modified corn and soybean meal. Bulletin of Veterinary Institute in Pulawy, 56, 617–622.

Shu QvY, Ye G G, Cui H R, Cheng X Y, Xiang Y B, Wu D X, Gao M W, Xia Y W, Hu C, Sardana R, Altosaar I. 2000. Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran rice pest species. Molecular Breeding, 6, 433–439.

Song Y, Liang C, Wang W, Fang J, Sun N, Jia X, Li N. 2014. Immunotoxicological evaluation of corn genetically modified with Bacillus thuringiensis Cry1Ah gene by a 30-day feeding study in BALB/c mice. PLOS ONE, 9, e78566.

Swiatkiewicz S, Koreleski J, Arczewska-Wlosek A, Swiatkiewicz M, Twardowska M, Markowski J, Mazur M, Sieradzki Z, Kwiatek K. 2011. Detection of transgenic DNA from Bt maize and herbicide tolerant soybean meal in tissues, eggs and digestive tract content of laying hens fed diets containing genetically modified plants. Annals of Animal Science, 11, 413–424.

Swiatkiewicz S, Swiatkiewicz M, Arczewska-Wlosek A, Jozefiak D. 2014. Genetically modified feeds and their effect on the metabolic parameters of food-producing animals: A review of recent studies. Animal Feed Science and Technology, 198, 1–19.

Swiatkiewicz S, Swiatkiewicz M, Koreleski J, Kwiatek K. 2010a. Nutritional efficiency of genetically-modified insect resistant corn (MON 810) and glyphosate-tolerant soybean meal (Roundup Ready) for broilers. Bulletin of Veterinary Institute in Pulawy, 54, 43–48.

Swiatkiewicz S, Twardowska M, Markowski J, Mazur M, Sieradzki Z, Kwiatek K. 2010b. Fate of transgenic dna from Bt corn and roundup ready soybean meal in broilers fed gmo feed. Bulletin of Veterinary Institute in Pulawy, 54, 237–242.

Tarek M, El-Achkar, Huang X P. 2006. Sepsis induces changes in the expression and distribution of toll-like receptor 4 in the rat kidney. American Journal of Physiology-Renal Physiology, 290, 1034–1043.

Trabalza-Marinucci M, Brandi G, Rondini C, Avellini L, Giammarini C, Costarelli S, Acuti G, Orlandi C, Filippini G, Chiaradia E, Malatesta M, Crotti S, Antonini C, Amagliani G, Manuali E, Mastrogiacomo A R, Moscati L, Haouet M N, Gaiti A, Magnani M. 2008. A three-year longitudinal study on the effects of a diet containing genetically modified Bt176 maize on the health status and performance of sheep. Livestock Science, 113, 178–190.

Wang Y, Wei B, Tian Y, Wang Z, Tian Y, Tan S, Dong S, Song Q. 2013. Evaluation of the potential effect of transgenic rice expressing Cry1Ab on the hematology and enzyme activity in organs of female swiss rats. PLOS ONE, 8, e80424.

Xu W, Cao S, He X, Luo Y, Guo X, Yuan Y, Huang K. 2009. Safety assessment of Cry1Ab/Ac fusion protein. Food and Chemical Toxicology, 47, 1459–1465.

Zhu H J, Chen Y, Li Y H, Wang J M, Ding J T, Chen X P, Peng Y F. 2015. A 90 day safety assessment of genetically modified rice expressing Cry1Ab/1Ac protein using an aquatic animal model. Journal of Agricultural and Food Chemistry, 63, 3627–3633.
[1] GAO Peng, ZHANG Tuo, LEI Xing-yu, CUI Xin-wei, LU Yao-xiong, FAN Peng-fei, LONG Shi-ping, HUANG Jing, GAO Ju-sheng, ZHANG Zhen-hua, ZHANG Hui-min. Improvement of soil fertility and rice yield after long-term application of cow manure combined with inorganic fertilizers[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2221-2232.
[2] Zaid CHACHAR, Siffat Ullah KHAN, ZHANG Xue-huan, LENG Peng-fei, ZONG Na, ZHAO Jun. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development[J]. >Journal of Integrative Agriculture, 2023, 22(2): 389-399.
[3] Jelli VENKATESH, Sung Jin KIM, Muhammad Irfan SIDDIQUE, Ju Hyeon KIM, Si Hyeock LEE, Byoung-Cheorl KANG. CopE and TLR6 RNAi-mediated tomato resistance to western flower thrips[J]. >Journal of Integrative Agriculture, 2023, 22(2): 471-480.
[4] ZHANG Yan-mei, AO De, LEI Kai-wen, XI Lin, Jerry W SPEARS, SHI Hai-tao, HUANG Yan-ling, YANG Fa-long. Dietary copper supplementation modulates performance and lipid metabolism in meat goat kids[J]. >Journal of Integrative Agriculture, 2023, 22(1): 214-221.
[5] LONG Ke-ren, LI Xiao-kai, ZHANG Ruo-wei, GU Yi-ren, DU Min-jie, XING Xiang-yang, DU Jia-xiang, MAI Miao-miao, WANG Jing, JIN Long, TANG Qian-zi, HU Si-lu, MA Ji-deng, WANG Xun, PAN Deng-ke, LI Ming-zhou. Transcriptomic analysis elucidates the enhanced skeletal muscle mass, reduced fat accumulation, and metabolically benign liver in human follistatin-344 transgenic pigs[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2675-2690.
[6] JIANG Yong, MA Xin-yan, XIE Ming, ZHOU Zheng-kui, TANG Jing, CHANG Guo-bin, CHEN Guo-hong, HOU Shui-sheng. Dietary threonine deficiency affects expression of genes involved in lipid metabolism in adipose tissues of Pekin ducks in a genotype-dependent manner[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2691-2699.
[7] RONG Hao, YANG Wen-jing, XIE Tao, WANG Yue, WANG Xia-qin, JIANG Jin-jin, WANG You-ping. Transcriptional profiling between yellow- and black-seeded Brassica napus reveals molecular modulations on flavonoid and fatty acid content[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2211-2226.
[8] GAO Zhi-ping, XU Min-li, ZHANG Hai-zi, LÜ Chuan-gen, CHEN Guo-xiang. Photosynthetic properties of the mid-vein and leaf lamina of field-grown, high-yield hybrid rice during senescence[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1913-1926.
[9] TIAN Chang, SUN Ming-xue, ZHOU Xuan, LI Juan, XIE Gui-xian, YANG Xiang-dong, PENG Jian-wei. Increase in yield and nitrogen use efficiency of double rice with long-term application of controlled-release urea[J]. >Journal of Integrative Agriculture, 2022, 21(7): 2106-2118.
[10] ZHOU Tian-yang, LI Zhi-kang, LI En-peng, WANG Wei-lu, YUAN Li-min, ZHANG Hao, LIU Li-jun, WANG Zhi-qin, GU Jun-fei, YANG Jian-chang. Optimization of nitrogen fertilization improves rice quality by affecting the structure and physicochemical properties of starch at high yield levels[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1576-1592.
[11] ZHAO Man, LI Yun-he, NIU Lin-lin, CHEN Lin, LIANG Ge-mei . Assessment of the potential toxicity of insecticidal compounds to Peristenus spretus, a parasitoid of mirid bugs[J]. >Journal of Integrative Agriculture, 2022, 21(5): 1424-1435.
[12] LIU Cong, LI De-xiong, HUANG Xian-biao, Zhang Fu-qiong, Xie Zong-zhou, Zhang Hong-yan, Liu Ji-hong. Manual thinning increases fruit size and sugar content of Citrus reticulata Blanco and affects hormone synthesis and sugar transporter activity[J]. >Journal of Integrative Agriculture, 2022, 21(3): 725-735.
[13] Christian Adler PHARES, Selorm AKABA. Co-application of compost or inorganic NPK fertilizer with biochar influenced soil quality, grain yield and net income of rice[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3600-3610.
[14] CHEN Yan-hui, XIE Bin, AN Xiu-hong, MA Ren-peng, ZHAO De-ying, CHENG Cun-gang, LI En-mao, ZHOU Jiang-tao, KANG Guo-dong, ZHANG Yan-zhen. Overexpression of the apple expansin-like gene MdEXLB1 accelerates the softening of fruit texture in tomato[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3578-3588.
[15] Muhammad Amjad BASHIR, ZHAI Li-mei, WANG Hong-yuan, LIU Jian, Qurat-Ul-Ain RAZA, GENG Yu-cong, Abdur REHIM, LIU Hong-bin. Apparent variations in nitrogen runoff and its uptake in paddy rice under straw incorporation[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3356-3367.
No Suggested Reading articles found!