Cross-Resistance between Cry1 Proteins in Fall Armyworm (Spodoptera frugiperda) May Affect the Durability of Current Pyramided Bt Maize Hybrids in Brazil

Abstract

Genetically modified plants expressing insecticidal proteins from Bacillus thuringiensis (Bt) offer valuable options for managing insect pests with considerable environmental and economic benefits. Despite the benefits provided by Bt crops, the continuous expression of these insecticidal proteins imposes strong selection for resistance in target pest populations. Bt maize (Zea mays) hybrids have been successful in controlling fall armyworm (Spodoptera frugiperda), the main maize pest in Brazil since 2008; however, field-evolved resistance to the protein Cry1F has recently been reported. Therefore it is important to assess the possibility of cross-resistance between Cry1F and other Cry proteins expressed in Bt maize hybrids. In this study, an F2 screen followed by subsequent selection on MON 89034 maize was used to select an S. frugiperda strain (RR) able to survive on the Bt maize event MON 89034, which expresses the Cry1A.105 and Cry2Ab2 proteins. Field-collected insects from maize expressing the Cry1F protein (event TC1507) represented most of the positive (resistance allele-containing) (iso)families found. The RR strain showed high levels of resistance to Cry1F, which apparently also conferred high levels of cross resistance to Cry1A.105 and Cry1Ab, but had only low-level (10-fold) resistance to Cry2Ab2. Life history studies to investigate fitness costs associated with the resistance in RR strain revealed only small reductions in reproductive rate when compared to susceptible and heterozygous strains, but the RR strain produced 32.2% and 28.4% fewer females from each female relative to the SS and RS (pooled) strains, respectively. Consistent with the lack of significant resistance to Cry2Ab2, MON 89034 maize in combination with appropriate management practices continues to provide effective control of S. frugiperda in Brazil. Nevertheless, the occurrence of Cry1F resistance in S. frugiperda across Brazil, and the cross-resistance to Cry1Ab and Cry1A.105, indicates that current Cry1-based maize hybrids face a challenge in managing S. frugiperda in Brazil and highlights the importance of effective insect resistance management for these technologies.

Performance of Cry1A.105-selected fall armyworm (Lepidoptera: Noctuidae) on transgenic maize plants containing single or pyramided Bt genes

“…The nonrecessive resistance could be one of the reasons that led to the rapid development of resistance to the Cry1F maize in some field populations of S. frugiperda. Cross-resistance of Cry1F-resistant S. frugiperda to Cry1A.105 protein or Cry1A.105 maize has also been reported in two previous studies Bernardi et al, 2015); Cry1F and Cry1A.105 have similar structures and thus selection for resistance to one is expected to confer resistance to the other. A previous study also showed that Cry1A.105 resistance alleles in the field populations of S. frugiperda collected in 2011 from Florida, U.S. was relatively abundant, reached 0.056 with a 95% credibility interval of 0.032e0.087 .…”

“…Relative to the single-gene Bt maize, these pyramided Bt maize products are usually more effective against some target pests, especially Noctuidae species such as the corn earworm (Helicoverpa zea [Boddie]) and S. frugiperda (Burkness et al, 2010;Niu et al, 2014;Yang et al, 2013Yang et al, , 2015. The widespread Cry1F resistance in S. frugiperda has sparked concerns about the durability of the pyramided Bt crops Bernardi et al, 2015;Santos-Amaya et al, 2015;Yang et al, 2016). One of the Bt proteins expressed in some pyramided Bt maize is Cry1A.105.…”

Resistance to Bt Crops; Influence, mechanisms and management strategies

“…While, a few cases of study in laboratory and field populations showed that the insect could evolve resistance to pyramid crops (Bernardi et al, 2015;Brévault et al, 2013;Fabrick et al, 2015;Wei et al, 2015;Welch et al, 2015). However, study by who reported that the resistance to pyramids is due to similarity of amino acid sequence between Bt toxins, which affect the cross-resistance when the resistance is associated with mutations, that reduce binding to midgut receptor.…”

Análise de risco para a evolução da resistência de <i>Helicoverpa armigera</i> (Lepidoptera: Noctuidae) à proteína Cry1Ac expressa pelo evento de soja MON 87701 × MON 89788 no Brasil

“…Ocupando 45,7 milhões de hectares, mais de 90% da área total do país de soja, milho e algodão é semeada com culturas transgênicas que se tornaram a principal ferramenta para o manejo de insetos pragas e plantas daninhas (CELERES, 2016). No entanto, o plantio contínuo e sucessivo de extensas áreas com culturas que expressam genes de Bacillus thuringiensis Berliner tem acarretado em intenso processo de seleção e evolução de populações de pragas resistentes (FARIAS et al, 2013;BERNARDI et al, 2015;OMOTO et al, 2016). No Brasil, trinta e três eventos que expressam proteínas Bt para o controle de insetos são autorizados para o plantio comercial (CTNBIO, 2016).…”

“…Entretanto, diversos autores têm demonstrado que estas mudanças temporais e espaciais na paisagem têm contribuído para o aumento populacional de pragas polífagas (MATSON et al, 1997;BIANCHI et al, 2003BIANCHI et al, , 2006MARTINELLI et al, 2006MARTINELLI et al, , 2007FARIAS et al, 2014;BERNARDI et al, 2015). A habilidade de H. armigera em colonizar diversos hospedeiros simultaneamente em diferentes regiões ao longo do ano é reconhecida como o principal fator que define o tamanho e a manutenção populacional (PASHLEY, 1988;FITT, 1989;NAGOSHI;MEAGHER, 2008).…”