Coexistence of Bacillus thuringiensis (Bt)-transgenic and conventional rice affects insect abundance and plant fitness in fields.

BACKGROUND As genetically modified (GM) crops are cultivated worldwide, concerns are emerging about the ecological consequences of the coexistence of transgenic and non-transgenic crops in fields. We first conducted field experiments using insect-resistant transgenic rice expressing Bacillus thuringiensis (Bt-transgenic rice) and its counterpart conventional rice (Oryza sativa L.) with or without insecticide spraying in 2013 and 2014. In 2015 and 2016, Bt-transgenic and conventional rice plants were employed in pure and mixed cages, with an infestation of the target insect (Chilo suppressalis) and with insecticide spraying as the control treatment to prevent target insect infestation. RESULTS The presence of Bt-transgenic rice decreased the abundance of target insects but did not affect non-target insects and predators in fields. Compared with conventional rice, Bt-transgenic rice showed more empty seeds but comparable seed production in cages. The infestation of target insects significantly decreased the plant fitness of conventional rice in pure cages, but did not affect its fitness when conventional rice coexisted with Bt-transgenic rice. In mixed cages, the presence of Bt-transgenic rice decreased the abundance of target insects and the percentage of dead sheaths in conventional rice. CONCLUSION The presence of Bt-transgenic rice benefits the growth and reproduction of non-transgenic rice in fields because of a decreased abundance of target insects. © 2018 Society of Chemical Industry.

[1]  Dong Xu,et al.  Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm , 2017, Proceedings of the National Academy of Sciences.

[2]  Yongbo Liu,et al.  Effects of Bt-transgenic rice cultivation on planktonic communities in paddy fields and adjacent ditches. , 2016, The Science of the total environment.

[3]  G. Yè,et al.  Effects of Transgenic Bt Rice on Nontarget Rhopalosiphum maidis (Homoptera: Aphididae) , 2016, Environmental Entomology.

[4]  Yongbo Liu,et al.  The presence of Bt-transgenic oilseed rape in wild mustard populations affects plant growth , 2015, Transgenic Research.

[5]  G. Yè,et al.  Transgenic cry1C or cry2A rice has no adverse impacts on the life-table parameters and population dynamics of the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). , 2015, Pest management science.

[6]  Yongbo Liu,et al.  Characterization of competitive interactions in the coexistence of Bt-transgenic and conventional rice , 2015, BMC Biotechnology.

[7]  B. Tabashnik,et al.  Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops , 2014, Nature Biotechnology.

[8]  C. N. Stewart,et al.  The effect of Bt-transgene introgression on plant growth and reproduction in wild Brassicajuncea , 2015, Transgenic Research.

[9]  B. Bonning,et al.  Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests , 2013, Proceedings of the National Academy of Sciences.

[10]  Keping Ma,et al.  Spread of introgressed insect-resistance genes in wild populations of Brassica juncea: a simulated in-vivo approach , 2012, Transgenic Research.

[11]  B. Halkier,et al.  Engineering of benzylglucosinolate in tobacco provides proof-of-concept for dead-end trap crops genetically modified to attract Plutella xylostella (diamondback moth). , 2012, Plant biotechnology journal.

[12]  Wei Wang,et al.  Transgenes for insect resistance reduce herbivory and enhance fecundity in advanced generations of crop–weed hybrids of rice , 2011, Evolutionary applications.

[13]  A. Gatehouse,et al.  Insect-resistant biotech crops and their impacts on beneficial arthropods , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Wei Wang,et al.  Enhanced yield performance of Bt rice under target-insect attacks: implications for field insect management , 2011, Transgenic Research.

[15]  P. Raven.  Does the use of transgenic plants diminish or promote biodiversity? , 2010, New Biotechnology.

[16]  Rosalind J Wright,et al.  Areawide Suppression of European Corn Borer with Bt Maize Reaps Savings to Non-Bt Maize Growers , 2010, Science.

[17]  G. Yè,et al.  Laboratory and Field Assessments of Prey-Mediated Effects of Transgenic Bt Rice on Ummeliata insecticeps (Araneida: Linyphiidae) , 2010, Environmental entomology.

[18]  Yanhui Lu,et al.  Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China , 2010, Science.

[19]  M. Jongsma,et al.  Insect oviposition behavior affects the evolution of adaptation to Bt crops: consequences for refuge policies , 2010, Evolutionary Ecology.

[20]  Kongming Wu,et al.  Suppression of Cotton Bollworm in Multiple Crops in China in Areas with Bt Toxin–Containing Cotton , 2008, Science.

[21]  Matty Demont,et al.  Regulating coexistence of GM and non-GM crops without jeopardizing economic incentives. , 2008, Trends in biotechnology.

[22]  A. Shelton,et al.  Suppression of diamondback moth using Bt-transgenic plants as a trap crop , 2008 .

[23]  A. Shelton,et al.  Sequential transformation to pyramid two Bt genes in vegetable Indian mustard (Brassica juncea L.) and its potential for control of diamondback moth larvae , 2008, Plant Cell Reports.

[24]  Elin Boalt,et al.  Tolerance to apical and foliar damage: costs and mechanisms in Raphanus raphanistrum , 2007 .

[25]  B. Jank,et al.  Co-existence of agricultural production systems. , 2006, Trends in biotechnology.

[26]  A. Snow,et al.  Effects of insect-resistance transgenes on fecundity in rice (Oryza sativa, Poaceae): a test for underlying costs , 2006 .

[27]  A. Shelton,et al.  Development of transgenic collards (Brassica oleracea L., var. acephala) expressing a cry1Ac or cry1C Bt gene for control of the diamondback moth , 2005 .

[28]  A. Shelton,et al.  Dead-end trap cropping: a technique to improve management of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) , 2004 .

[29]  F. Bigler,et al.  Uptake of Bt‐toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea , 2002 .

[30]  J. Losey,et al.  Transgenic Insecticidal Corn: Beyond Insecticidal Toxicity to Ecological Complexity , 2001 .

[31]  N. Ellstrand,et al.  When transgenes wander, should we worry? , 2001, Plant physiology.

[32]  I. Altosaar,et al.  Field Evaluation of Resistance of Transgenic Rice Containing a Synthetic cry1Ab Gene from Bacillus thuringiensis Berliner to Two Stem Borers , 2001, Journal of economic entomology.

[33]  R. Kfir,et al.  The possibility of using Indian mustard, Brassica juncea, as a trap crop for the diamondback moth, Plutella xylostella, in South Africa. , 2000 .

[34]  G. Hu,et al.  Management of Diamondback Moth (Lepidoptera: Plutellidae) in Cabbage Using Collard as a Trap Crop , 2000 .

[35]  J. Ingram,et al.  The separation distances required to ensure cross-pollination is below specified limits in non-seed crops of sugar beet, maize and oilseed rape. , 2000 .

[36]  J. Losey,et al.  Transgenic pollen harms monarch larvae , 1999, Nature.

[37]  A. Hilbeck,et al.  Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla cornea (Neuroptera: Chrysopidae) , 1998 .

[38]  C. Palm,et al.  Costs of resistance: a test using transgenic Arabidopsis thaliana , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  William F. Morris,et al.  Do Barren Zones and Pollen Traps Reduce Gene Escape From Transgenic Crops , 1994 .