Bt性状对转基因水稻的生长特性和杂草竞争力的影响

doi:10.1016/j.jia.2023.01.001

摘要/Abstract

摘要：

转基因逃逸可能会导致外源基因基因漂移逃逸到非转基因作物及其野生近缘种，形成野生转基因群体，进而与杂草竞争生存空间，引起生态风险。目前，尚不清楚苏云金芽孢杆菌(Bacillus thuringiensis, Bt)基因在转基因水稻中的表达是否会改变转基因水稻与杂草之间的关系并导致不良的环境后果。通过田间试验，研究了转基因Bt水稻在无除草剂和控制鳞翅目害虫的环境下的杂草竞争力，并评估了Bt水稻的生态风险。结果表明，与移栽水稻相比，杂草-水稻的竞争在直播水稻中出现更早、更严重，导致直播水稻的生物量和产量显著下降。然而，在常规品种中，相同栽培方式下的Bt水稻与非Bt水稻的产量差异不显著。在生长前期和成熟期，常规品种的Bt水稻的杂草数量、杂草覆盖率和杂草多样性指数显著高于非Bt水稻，特别是在直播水稻小区中，说明Bt性状不会增加转基因水稻的杂草竞争力，也没有对杂草多样性产生不利影响。在杂交品种中，虽然不同杂交稻品系之间的籽粒产量和杂草发生数量存在差异，但是这些指标在Bt和非Bt杂交水稻之间差异不显著。杂交稻小区中昆虫的数量随着杂草数量的增加而增加，但是Bt和非Bt杂交水稻的昆虫数量和多样性无显著差异。因此，转基因Bt水稻的生态风险与非Bt水稻相当。

Abstract: Transgene escape could lead to genetically modified rice establishing wild populations in the natural environment and competing for survival space with weeds. However, whether the expression of the Bacillus thuringiensis (Bt) gene in rice will alter the relationship between transgene plants and weeds and induce undesirable environmental consequences are poorly understood. Thus, field experiments were conducted to investigate the weed competitiveness and assess the ecological risk of transgenic Bt rice under herbicide-free and lepidopterous pest-controlled environments. Results showed that weed–rice competition in the direct-sowing (DS) field was earlier and more severe than that in the transplanting (TP) field, which resulted in a significant decrease in biomass and yield in DS. However, conventional Bt and non-Bt rice yield was not significantly different. The weed number, weed coverage ratio, and weed diversity of conventional Bt rice were significantly higher than those of non-Bt rice at the early growth and mature stages, especially in DS plots, suggesting that Bt traits did not increase the weed competitiveness of transgenic rice and had no negative effect on weed diversity. Grain yield and weed number varied between different hybrid rice lines, but those differences were insignificant between Bt and non-Bt rice. The number of insects increased with the increase of weeds in hybrid rice plots, whereas the insect number and diversity did not display a significant difference between Bt and non-Bt rice. Therefore, the ecological risk of transgenic Bt rice is comparable to non-Bt rice.

Key words: biosafety , field evaluationg , enetically modified crops , Oryza sativa , weed competitiveness

WANG Kang-xu, ZHANG Ke-rou, CAO Cou-gui, JIANG Yang. Bt性状对转基因水稻的生长特性和杂草竞争力的影响[J]. Journal of Integrative Agriculture, 2023, 22(8): 2346-2358.

WANG Kang-xu , ZHANG Ke-rou, CAO Cou-gui, JIANG Yang. Effect of Bt traits on transgenic rice’s growth and weed competitiveness[J]. Journal of Integrative Agriculture, 2023, 22(8): 2346-2358.

参考文献

Arpaia S, Birch A N E, Kiss J, van Loon J J A, Messéan A, Nuti M, Perry J N, Sweet J B, Tebbe C C. 2017. Assessing environmental impacts of genetically modified plants on non-target organisms: The relevance of in planta studies. Science of the Total Environment, 583, 123–132.

Benaragama D, Shirtliffe S J, Johnson E N, Duddu H S N, Syrovy L D. 2016. Does yield loss due to weed competition differ between organic and conventional cropping systems? Weed Research, 56, 274–283.

Cao Q J, Xia H, Yang X, Lu B R. 2009. Performance of hybrids between weedy rice and insect-resistant transgenic rice under field experiments: Implication for environmental biosafety assessment. Journal of Integrative Plant Biology, 51, 1138–1148.

Carriere Y, Ellers-Kirk C, Hartfield K, Larocque G, Degain B, Dutilleul P, Dennehy T J, Marsh S E, Crowder D W, Li X, Ellsworth P C, Naranjo S E, Palumbo J C, Fournier A, Antilla L, Tabashnik B E. 2012. Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America, 109, 775–780.

Chen H, Tang W, Xu C, Li X, Lin Y, Zhang Q. 2005. Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theoretical and Applied Genetics, 111, 1330–1337.

Chen M, Liu Z, Ye G, Shen Z, Hu C, Peng Y, Altosaar I, Shelton A M. 2007. Impacts of transgenic cry1Ab rice on non-target planthoppers and their main predator Cyrtorhinus lividipennis (Hemiptera: Miridae) - A case study of the compatibility of Bt rice with biological control. Biological Control, 42, 242–250.

Dang C, Lu Z, Wang L, Chang X, Wang F, Yao H, Peng Y, Stanley D, Ye G. 2017. Does Bt rice pose risks to non-target arthropods? Results of a meta-analysis in China. Plant Biotechnology Journal, 15, 1047–1053.

Dass A, Shekhawat K, Choudhary A K, Sepat S, Rathore S S, Mahajan G, Chauhan B S. 2017. Weed management in rice using crop competition - A review. Crop Protection, Role of Crop Competition in Weed Management, 95, 45–52.

Fu J, Song X, Liu B, Shi Y, Shen W, Fang Z, Zhang L. 2018. Fitness cost of transgenic cry1Ab/c rice under saline-alkaline soil condition. Frontiers in Plant Science, 9, 1552.

García-Ruiz E, Cobos G, Sánchez-Ramos I, Pascual S, Chueca M C, Escorial M C, Santín-Montanyá I, Loureiro Í, González-Núñez M. 2020. Dynamics of canopy-dwelling arthropods under different weed management options, including glyphosate, in conventional and genetically modified insect-resistant maize. Insect Science, 28, 1121–1138.

Griffiths B S, Heckmann L H, Caul S, Thompson J, Scrimgeour C, Krogh P H. 2007. Varietal effects of eight paired lines of transgenic Bt maize and near-isogenic non-Bt maize on soil microbial and nematode community structure. Plant Biotechnology Journal, 5, 60–68.

Han Y, Xu X, Ma W, Yuan B, Wang H, Liu F, Wang M, Wu G, Hua H. 2011. The influence of transgenic cry1Ab/cry1Ac, cry1C and cry2A rice on non-target planthoppers and their main predators under field conditions. Agricultural Sciences in China, 10, 1739–1747.

Huang Y, Li J, Qiang S, Dai W, Song X. 2016. Transgenic restorer rice line T1c-19 with stacked cry1C*/bar genes has low weediness potential without selection pressure. Journal of Integrative Agriculture, 15, 1046–1058.

Huang Y, Wang Y, Qiang S, Song X, Dai W. 2019. Fitness of F1 hybrids between stacked transgenic rice T1c-19 with cry1C*/bar genes and weedy rice. Journal of Integrative Agriculture, 18, 2793–2805.

International Service for the Acquisition of Agri-biotech Applications (ISAAA). 2018. Global Status of Commercialized Biotech/GM Crops in 2018: Biotech Crops Continue to Help Meet the Challenges of Increased Population and Climate Change (International Service for the Acquisition of Agri-biotech Applications Brief No. 54). International Service for the Acquisition of Agri-biotech Applications, Ithaca, New York.

Jia S, Yuan Q, Pei X, Wang F, Hu N, Yao K, Wang Z. 2014. Rice transgene flow: Its patterns, model and risk management. Plant Biotechnology Journal, 12, 1259–1270.

Jian Z, Wang F, Li Z, Chen Y, Ma X, Nie L, Cui K, Peng S, Lin Y, Song H, Li Y, Huang J. 2014. Grain yield and nitrogen use efficiency responses to N application in Bt (Cry1Ab/Ac) transgenic two-line hybrid rice. Field Crops Research, 155, 184–191.

Jiang Y, Ling L, Zhang L, Domingo A, Cai M, Li C, Zhan M, Wang J, Cao C. 2017. Different response of an elite Bt restorer line of hybrid rice (Oryza sativa L.) in adaptation to nitrogen deficiency. Acta Physiologiae Plantarum, 39, 89.

Jiang Y, Ling L, Zhang L, Wang K, Cai M, Zhan M, Li C, Wang J, Chen X, Lin Y, Cao C. 2016. Transgenic Bt (Cry1Ab/Ac) rice lines with different genetic backgrounds exhibit superior field performance under pesticide-free environment. Field Crops Research, 193, 117–122.

Jiang Y, Ling L, Zhang L, Wang K, Li X, Cai M, Zhan M, Li C, Wang J, Cao C. 2018. Comparison of transgenic Bt rice and their non-Bt counterpart in yield and physiological response to drought stress. Field Crops Research, 217, 45–52.

Jiang Y, Meng J, Zhang L, Cai M, Li C, Zhan M, Wang J, Wang B, Mohamed I, Cao C. 2014. Non-target effects of Bt transgenes on grain yield and related traits of an elite restorer rice line in response to nitrogen and potassium applications. Field Crops Research, 169, 39–48.

Kaur T, Bhullar M S, Kaur S. 2019. Weed control in Bt (Bacillus thuringiensis) cotton with pre mix of pyrithiobac sodium plus quizalofop ethyl in north-west India. Crop Protection, 119, 69–75.

Kaya-Altop E, Şahin M, Jabran K, Phillippo C J, Zandstra B H, Mennan H. 2019. Effect of different water management strategies on competitive ability of semi-dwarf rice cultivars with Echinochloa Oryzoides. Crop Protection, 116, 33–42.

Li F F, Ye G Y, Wu Q, Peng Y F, Chen X X. 2007. Arthropod abundance and diversity in Bt and non-Bt rice fields. Environmental Entomology, 36, 646–654.

Li Z, Li L K, Liu B, Wang L, Parajulee M N, Chen F J. 2019. Effects of seed mixture sowing with transgenic Bt rice and its parental line on the population dynamics of target stemborers and leafrollers, and non-target planthoppers. Insect Science, 26, 777–794.

Ling L, Li X, Wang K, Cai M, Jiang Y, Cao C. 2019. Carbon and nitrogen partitioning of transgenic rice T2A-1 (Cry2A*) with different nitrogen treatments. Scientific Reports, 9, 5351.

Liu L, Guo R, Qin Q, Fu J, Liu B. 2020. Expression of Bt protein in transgenic Bt cotton plants and ecological fitness of these plants in different habitats. Frontiers in Plant Science, 11, 1209.

Liu Y, Ge F, Liang Y, Wu G, Li J. 2015. Characterization of competitive interactions in the coexistence of Bt-transgenic and conventional rice. BMC Biotechnology, 15, 27.

Lu Z B, Tian J C, Han N S, Hu C, Peng Y F, Stanley D, Ye G Y. 2014. No direct effects of two transgenic Bt rice lines, T1C-19 and T2A-1, on the arthropod communities. Environmental Entomology, 43, 1453–1463.

Luo Y, Fu H, Traore S. 2014. Biodiversity conservation in rice paddies in China: Toward ecological sustainability. Sustainability, 6, 6107–6124.

Maqbool S B, Husnain T, Riazuddin S, Masson L, Christou P. 1998. Effective control of yellow stem borer and rice leaf folder in transgenic rice indica varieties Basmati 370 and M 7 using the novel δ-endotoxin cry2A Bacillus thuringiensis gene. Molecular Breeding, 4, 501–507.

Marvier M, McCreedy C, Regetz J, Kareiva P. 2007. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science, 316, 1475–1477.

Saito K. 2010. Weed pressure level and the correlation between weed competitiveness and rice yield without weed competition: An analysis of empirical data. Field Crops Research, 117, 1–8.

Shimada N, Sugiura S. 2020. Indirect effects of weeds on rice plants via shared heteropteran herbivores. Journal of Applied Entomology, 145, 117–124.

Tang W, Chen H, Xu C, Li X, Lin Y, Zhang Q. 2006. Development of insect-resistant transgenic indica rice with a synthetic cry1C* gene. Molecular Breeding, 18, 1–10.

Wang F, Ye C, Zhu L, Nie L, Cui K, Peng S, Lin Y, Huang J. 2012. Yield differences between Bt transgenic rice lines and their non-Bt counterparts, and its possible mechanism. Field Crops Research, 126, 8–15.

Wang F, Yuan Q H, Shi L, Qian Q, Liu W G, Kuang B G, Zeng D L, Liao Y L, Cao B, Jia S R. 2006. A large-scale field study of transgene flow from cultivated rice (Oryza sativa) to common wild rice (O. rufipogon) and barnyard grass (Echinochloa crusgalli). Plant Biotechnology Journal, 4, 667–676.

Wang X, Liu Q, Meissle M, Peng Y, Wu K, Romeis J, Li Y. 2018. Bt rice could provide ecological resistance against nontarget planthoppers. Plant Biotechnology Journal, 16, 1748–1755.

Wang Y, Zhang G, Du J, Liu B, Wang M. 2010. Influence of transgenic hybrid rice expressing a fused gene derived from cry1Ab and cry1Ac on primary insect pests and rice yield. Crop Protection, 29, 128–133.

Wolfenbarger L L, Naranjo S E, Lundgren J G, Bitzer R J, Watrud L S. 2008. Bt crop effects on functional guilds of non-target arthropods: A meta-analysis. PLoS ONE, 3, e2118.

Xia H, Chen L, Wang F, Lu B R. 2010. Yield benefit and underlying cost of insect-resistance transgenic rice: Implication in breeding and deploying transgenic crops. Field Crops Research, 118, 215–220.

Xia H, Lu B R, Xu K, Wang W, Yang X, Yang C, Luo J, Lai F, Ye W, Fu Q. 2011. Enhanced yield performance of Bt rice under target-insect attacks: implications for field insect management. Transgenic Research, 20, 655–664.

Yang X, Xia H, Wang W, Wang F, Su J, Snow A A, Lu B R. 2011. Transgenes for insect resistance reduce herbivory and enhance fecundity in advanced generations of crop–weed hybrids of rice. Evolutionary Applications, 4, 672–684.

Yang Y, Liu K, Han H, Xu H, Zhang F, Zheng X, Tian J, Wang G, Chen G, Lu Z. 2016. Impacts of nitrogen fertilizer on major insect pests and their predators in transgenic Bt rice lines T2A-1 and T1C-19. Entomologia Experimentalis et Applicata, 160, 281–291.

Yang Z, Chen H, Tang W, Hua H, Lin Y. 2011. Development and characterisation of transgenic rice expressing two Bacillus thuringiensis genes. Pest Management Science, 67, 414–422.