Edible Safety Assessment of Genetically Modified Rice T1C-1 for Sprague Dawley Rats through Horizontal Gene Transfer, Allergenicity and Intestinal Microbiota

Kai Zhao; Fangfang Ren; Fangting Han; Qiwen Liu; Guogan Wu; Yan Xu; Jian Zhang; Xiao Wu; Jinbin Wang; Peng Li; Wei Shi; Hong Zhu; Jianjun Lv; Xiao Zhao; Xueming Tang

doi:10.1371/journal.pone.0163352

Edible Safety Assessment of Genetically Modified Rice T1C-1 for Sprague Dawley Rats through Horizontal Gene Transfer, Allergenicity and Intestinal Microbiota

PLoS One. 2016 Oct 5;11(10):e0163352. doi: 10.1371/journal.pone.0163352. eCollection 2016.

Authors

Kai Zhao^{1

2}, Fangfang Ren³, Fangting Han³, Qiwen Liu³, Guogan Wu^{1

2}, Yan Xu³, Jian Zhang⁴, Xiao Wu^{1

2}, Jinbin Wang^{1

2}, Peng Li^{1

2}, Wei Shi³, Hong Zhu¹, Jianjun Lv⁵, Xiao Zhao⁶, Xueming Tang^{1

2}

Affiliations

¹ Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, People's Republic of China.
² Key Laboratory of Agricultural Genetics and Breeding, Shanghai Academy of Agricultural Sciences, Shanghai, People's Republic of China.
³ College of Life and Environment Sciences, Shanghai Normal University, Shanghai, People's Republic of China.
⁴ Alberta Innovates-Technology Futures, Vegreville, Alberta, Canada.
⁵ National Center for Safety Evaluation of Drugs, Beijing Economic-Technological Development Area, Beijing, People's Republic of China.
⁶ Life Science College, Ningxia University, Yinchuan, Ningxia, People's Republic of China.

Abstract

In this study, assessment of the safety of transgenic rice T1C-1 expressing Cry1C was carried out by: (1) studying horizontal gene transfer (HGT) in Sprague Dawley rats fed transgenic rice for 90 d; (2) examining the effect of Cry1C protein in vitro on digestibility and allergenicity; and (3) studying the changes of intestinal microbiota in rats fed with transgenic rice T1C-1 in acute and subchronic toxicity tests. Sprague Dawley rats were fed a diet containing either 60% GM Bacillus thuringiensis (Bt) rice T1C-1 expressing Cry1C protein, the parental rice Minghui 63, or a basic diet for 90 d. The GM Bt rice T1C-1 showed no evidence of HGT between rats and transgenic rice. Sequence searching of the Cry1C protein showed no homology with known allergens or toxins. Cry1C protein was rapidly degraded in vitro with simulated gastric and intestinal fluids. The expressed Cry1C protein did not induce high levels of specific IgG and IgE antibodies in rats. The intestinal microbiota of rats fed T1C-1 was also analyzed in acute and subchronic toxicity tests by DGGE. Cluster analysis of DGGE profiles revealed significant individual differences in the rats' intestinal microbiota.

MeSH terms

Allergens / immunology*
Animals
Bacillus thuringiensis / genetics
Bacillus thuringiensis / metabolism
Bacteria / classification
Bacteria / genetics
Bacteria / isolation & purification
Bacterial Proteins / genetics*
Bacterial Proteins / immunology
Bacterial Proteins / metabolism
Cluster Analysis
Feces / microbiology
Female
Food, Genetically Modified / toxicity
Gene Transfer, Horizontal / physiology*
Genetic Variation
Immunoglobulin G / blood
Immunoglobulin G / immunology
Immunoglobulin M / blood
Immunoglobulin M / immunology
Insect Proteins
Intestinal Mucosa / metabolism
Intestines / microbiology*
Male
Microbiota
Muscles / metabolism
Oryza / genetics*
Oryza / metabolism
Phylogeny
Plants, Genetically Modified / genetics
RNA, Ribosomal, 16S / genetics
RNA, Ribosomal, 16S / metabolism
Rats
Rats, Sprague-Dawley
Receptors, Cell Surface / genetics*
Receptors, Cell Surface / immunology
Receptors, Cell Surface / metabolism
Toxicity Tests, Acute

Substances

Allergens
Bacterial Proteins
Cry toxin receptors
Immunoglobulin G
Immunoglobulin M
Insect Proteins
RNA, Ribosomal, 16S
Receptors, Cell Surface

Grants and funding

This work was supported by Shanghai Agricultural Science Committee foundation of China, grant no.6-4 (2009),http://e-nw.shac.gov.cn/index.html. Shanghai Agricultural Science Key Research Foundation grant no.1-8 (2011), http://e-nw.shac.gov.cn/index.html. The Public Research Platform Foundation of Shanghai Science and Technology Committee, grant no. 13DZ2290700, http://www.stcsm.gov.cn/. The Science and Technology Development Programme of Shanghai Acedemy of Agricultural Sciences,2013(14), http://www.saas.sh.cn/. The Science and Technology Development Programme of Shanghai Acedemy of Agricultural Sciences,2012(8), http://www.saas.sh.cn/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.