High Susceptibility to Cry1Ac and Low Resistance Allele Frequency Reduce the Risk of Resistance of Helicoverpa armigers to Bt Soybean in Brazil.

Patrick M Dourado,Samuel Martinelli,Fabiana B Bacalhau,Douglas Amado,Renato A Carvalho,Graham P Head,Celso Omoto,Nicolas Desneux

doi:10.1371/journal.pone.0161388

Patrick M Dourado, Samuel Martinelli + Show 6 more

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https://doi.org/10.1371/journal.pone.0161388

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Abstract

The Old World bollworm, Helicoverpa armigera (Hübner), was recently introduced into Brazil, where it has caused extensive damage to cotton and soybean crops. MON 87701 × MON 89788 soybean, which expresses the Bt protein Cry1Ac, was recently deployed in Brazil, providing high levels of control against H. armigera. To assess the risk of resistance to the Cry1Ac protein expressed by MON 87701 × MON 89788 soybean in Brazil, we conducted studies to evaluate the baseline susceptibility of H. armigera to Cry1Ac, in planta efficacy including the assessment of the high-dose criterion, and the initial resistance allele frequency based on an F2 screen. The mean Cry1Ac lethal concentration (LC50) ranged from 0.11 to 1.82 μg·mL−1 of diet among all H. armigera field populations collected from crop seasons 2013/14 to 2014/15, which indicated about 16.5-fold variation. MON 87701 × MON 89788 soybean exhibited a high level of efficacy against H. armigera and most likely met the high dose criterion against this target species in leaf tissue dilution bioassays up to 50 times. A total of 212 F2 family lines of H. armigera were established from field collections sampled from seven locations across Brazil and were screened for the presence of MON 87701 × MON 89788 soybean resistance alleles. None of the 212 families survived on MON 87701 × MON 89788 soybean leaf tissue (estimated allele frequency = 0.0011). The responses of H. armigera to Cry1Ac protein, high susceptibility to MON 87701 × MON 89788 soybean, and low frequency of resistance alleles across the main soybean-producing regions support the assumptions of a high-dose/refuge strategy. However, maintenance of reasonable compliance with the refuge recommendation will be essential to delay the evolution of resistance in H. armigera to MON 87701 × MON 89788 soybean in Brazil.

Highlights

Helicoverpa armigera (Hübner) is considered to be one of the most important agricultural pests in the world [1]
In the Old World and in Australia, where H. armigera is a major pest of cotton, this species is the primary target of genetically modified cotton containing insecticidal proteins from Bacillus thuringiensis (Bt), which has been widely adopted by growers to overcome insecticide resistance issues [6,7,8]
The baseline susceptibility of H. armigera documented using a diet-incorporated bioassay for insects sampled in crop seasons 2013/14 and 2014/15 indicated neonate larvae were highly susceptible to Cry1Ac with LC50 values ranging from 0.11 to 1.82 μg Cry1Ac mL−1 diet (Table 1) and EC50 values ranging from 0.0029 to 0.0165 μg Cry1Ac mL−1 diet (Table 2)

Summary

Introduction

Helicoverpa armigera (Hübner) is considered to be one of the most important agricultural pests in the world [1]. In the Old World and in Australia, where H. armigera is a major pest of cotton, this species is the primary target of genetically modified cotton containing insecticidal proteins from Bacillus thuringiensis (Bt), which has been widely adopted by growers to overcome insecticide resistance issues [6,7,8]. This species was identified in South America, especially in Brazil [9, 10]. Soybean and cotton represent the largest areas in Brazil, totaling 30 million and 1 million hectares per year, respectively [1]

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