Dively Galen P, Venugopal P Dilip, Finkenbinder Chad
Department of Entomology, University of Maryland, College Park, Maryland, United States of America.
American Association for the Advancement of Science - Science and Technology Policy Fellowship Program, Transportation and Climate Division, Office of Transportation & Air Quality, United States Environmental Protection Agency, District of Columbia, United States of America.
PLoS One. 2016 Dec 30;11(12):e0169115. doi: 10.1371/journal.pone.0169115. eCollection 2016.
Transgenic corn engineered with genes expressing insecticidal toxins from the bacterium Bacillus thuringiensis (Berliner) (Bt) are now a major tool in insect pest management. With its widespread use, insect resistance is a major threat to the sustainability of the Bt transgenic technology. For all Bt corn expressing Cry toxins, the high dose requirement for resistance management is not achieved for corn earworm, Helicoverpa zea (Boddie), which is more tolerant to the Bt toxins.
METHODOLOGY/MAJOR FINDINGS: We present field monitoring data using Cry1Ab (1996-2016) and Cry1A.105+Cry2Ab2 (2010-2016) expressing sweet corn hybrids as in-field screens to measure changes in field efficacy and Cry toxin susceptibility to H. zea. Larvae successfully damaged an increasing proportion of ears, consumed more kernel area, and reached later developmental stages (4th - 6th instars) in both types of Bt hybrids (Cry1Ab-event Bt11, and Cry1A.105+Cry2Ab2-event MON89034) since their commercial introduction. Yearly patterns of H. zea population abundance were unrelated to reductions in control efficacy. There was no evidence of field efficacy or tissue toxicity differences among different Cry1Ab hybrids that could contribute to the decline in control efficacy. Supportive data from laboratory bioassays demonstrate significant differences in weight gain and fitness characteristics between the Maryland H. zea strain and a susceptible strain. In bioassays with Cry1Ab expressing green leaf tissue, Maryland H. zea strain gained more weight than the susceptible strain at all concentrations tested. Fitness of the Maryland H. zea strain was significantly lower than that of the susceptible strain as indicated by lower hatch rate, longer time to adult eclosion, lower pupal weight, and reduced survival to adulthood.
CONCLUSIONS/SIGNIFICANCE: After ruling out possible contributing factors, the rapid change in field efficacy in recent years and decreased susceptibility of H. zea to Bt sweet corn provide strong evidence of field-evolved resistance in H. zea populations to multiple Cry toxins. The high adoption rate of Bt field corn and cotton, along with the moderate dose expression of Cry1Ab and related Cry toxins in these crops, and decreasing refuge compliance probably contributed to the evolution of resistance. Our results have important implications for resistance monitoring, refuge requirements and other regulatory policies, cross-resistance issues, and the sustainability of the pyramided Bt technology.
转导了来自苏云金芽孢杆菌(Berliner)(Bt)的表达杀虫毒素基因的转基因玉米,如今已成为害虫治理的一项主要手段。随着其广泛应用,昆虫抗性成为Bt转基因技术可持续性的一大主要威胁。对于所有表达Cry毒素的Bt玉米而言,针对棉铃虫(Helicoverpa zea (Boddie)),尚未达到抗性治理所需的高剂量要求,棉铃虫对Bt毒素的耐受性更强。
方法/主要发现:我们展示了利用表达Cry1Ab(1996 - 2016年)和Cry1A.105 + Cry2Ab2(2010 - 2016年)的甜玉米杂交种作为田间筛选手段的田间监测数据,以测定田间防治效果的变化以及棉铃虫对Cry毒素的敏感性。自这两种Bt杂交种(Cry1Ab事件Bt11和Cry1A.105 + Cry2Ab2事件MON89034)商业化推广以来,幼虫成功损害的玉米穗比例不断增加,消耗的籽粒面积更多,且在这两种Bt杂交种中均发育到了后期阶段(4龄至6龄)。棉铃虫种群数量的年度变化模式与防治效果的降低并无关联。没有证据表明不同Cry1Ab杂交种之间在田间防治效果或组织毒性方面存在差异,而这种差异可能导致了防治效果的下降。来自实验室生物测定的支持性数据表明,马里兰棉铃虫品系与一个敏感品系在体重增加和适合度特征方面存在显著差异。在对表达Cry1Ab的绿叶组织进行的生物测定中,马里兰棉铃虫品系在所有测试浓度下的体重增加均超过敏感品系。马里兰棉铃虫品系的适合度显著低于敏感品系,表现为孵化率更低、成虫羽化所需时间更长、蛹重更低以及成虫存活率降低。
结论/意义:在排除了可能的影响因素之后,近年来田间防治效果的迅速变化以及棉铃虫对Bt甜玉米敏感性的降低,有力地证明了棉铃虫种群对多种Cry毒素产生了田间进化抗性。Bt田间玉米和棉花的高采用率,以及这些作物中Cry1Ab和相关Cry毒素的中等剂量表达,再加上避难所合规性的降低,可能促成了抗性的进化。我们的研究结果对于抗性监测、避难所要求及其他监管政策、交叉抗性问题以及复合Bt技术的可持续性具有重要意义。