Evidence of Field-Evolved Resistance of Spodoptera frugiperda to Bt Corn Expressing Cry1F in Brazil That Is Still Sensitive to Modified Bt Toxins

Abstract

Brazil ranked second only to the United States in hectares planted to genetically modified crops in 2013. Recently corn producers in the Cerrado region reported that the control of Spodoptera frugiperda with Bt corn expressing Cry1Fa has decreased, forcing them to use chemicals to reduce the damage caused by this insect pest. A colony of S. frugiperda was established from individuals collected in 2013 from Cry1Fa corn plants (SfBt) in Brazil and shown to have at least more than ten-fold higher resistance levels compared with a susceptible colony (Sflab). Laboratory assays on corn leaves showed that in contrast to SfLab population, the SfBt larvae were able to survive by feeding on Cry1Fa corn leaves. The SfBt population was maintained without selection for eight generations and shown to maintain high levels of resistance to Cry1Fa toxin. SfBt showed higher cross-resistance to Cry1Aa than to Cry1Ab or Cry1Ac toxins. As previously reported, Cry1A toxins competed the binding of Cry1Fa to brush border membrane vesicles (BBMV) from SfLab insects, explaining cross-resistance to Cry1A toxins. In contrast Cry2A toxins did not compete Cry1Fa binding to SfLab-BBMV and no cross-resistance to Cry2A was observed, although Cry2A toxins show low toxicity to S. frugiperda. Bioassays with Cry1AbMod and Cry1AcMod show that they are highly active against both the SfLab and the SfBt populations. The bioassay data reported here show that insects collected from Cry1Fa corn in the Cerrado region were resistant to Cry1Fa suggesting that resistance contributed to field failures of Cry1Fa corn to control S. frugiperda.

Field-Evolved Mode 1 Resistance of the Fall Armyworm to Transgenic Cry1Fa-Expressing Corn Associated with Reduced Cry1Fa Toxin Binding and Midgut Alkaline Phosphatase Expression

“…Strains of S. frugiperda from Brazil with field-evolved resistance have been reported to display reduced Cry1Fa toxin binding using semiquantitative methods (6), although the receptors involved were not documented. Moreover, while Cry1Aa and Cry1Ab binding was also reduced in resistant compared to susceptible S. frugiperda, Cry1Ac binding was not affected.…”

“…These high levels of Bt crop adoption represent increased selection pressure for the evolution of insect resistance, which is currently considered the major threat to the sustainability of this technology. Almost 2 decades since the commercialization of Bt crops targeting lepidopteran pests, field control failures due to the evolution of insect resistance in lepidopteran pests have been documented for populations of Busseola fusca (maize stalk borer) in Cry1Ab corn in South Africa (3), Pectinophora gossypiella (pink bollworm) in Cry1Ac cotton in India (4), and Spodoptera frugiperda (fall armyworm) in Cry1Fa corn in Puerto Rico (5) and Brazil (6). More specifically, high levels of S. frugiperda resistance to Bt corn event TC1507 in Puerto Rico represented the first case in a U.S. territory of practical resistance (7) in a lepidopteran pest resulting in withdrawal of the Bt crop event from the local market (5).…”

“…Commonly accepted steps in the Cry intoxication model in lepidopteran larvae include solubilization and proteolysis in the gut digestive fluids of the target insect to yield an activated Cry toxin core, which then binds to receptors on the brush border membrane of the midgut epithelium and inserts into the cell membrane to form a pore responsible for osmotic cell lysis (14). Recent qualitative studies suggest an association between reduced binding and field-evolved resistance to TC1507 corn in S. frugiperda from Brazil (6). Reduced levels of diverse putative Cry1Fa toxin receptors were detected in strains of S. frugiperda from Puerto Rico with field-evolved resistance to TC1507 corn compared to the levels in susceptible insects (15,16), yet the mechanistic relevance of these differences to resistance was not addressed.…”

Toxicidad sobre Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) de la proteína Bt expresada en hojas de diferentes eventos de maíz transgénico iberados en Paraguay

“…La eficacia del maíz Bt para controlar a S. frugiperda se evaluó en diferentes países, y existen reportes de éxitos y fracasos (Williams et al, 1997;Waquil et al, 2002;Zenner et al, 2009;Giaveno et al, 2010;Flores & Balbi, 2014;Grandis de Lima & Assmann 2015;Monnerat et al, 2015). Por otro lado, en Puerto Rico, Brasil y el sur de Estados Unidos se detectó resistencia de S. frugiperda a maíces Bt que expresan las proteínas Cry1F o Cry1Ab (Storer et al, 2010;Farias et al, 2014;Huang et al, 2014;Omoto et al, 2016).…”

Resistance to Bt Crops; Influence, mechanisms and management strategies

“…Diabrotica virgifera virgifera showed resistance to Cry3Bb1 in Bt maize (Gassmann et al, 2011). S. frugiperda evolved resistance to Cry1Fa toxin in Bt corn (Farias et al, 2015;Jakka et al, 2015;Monnerat et al, 2015).…”