Elsevier

Crop Protection

Volume 88, October 2016, Pages 79-87
Crop Protection

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

https://doi.org/10.1016/j.cropro.2016.06.005Get rights and content

Highlights

  • Performance of Cry1A.105-susceptible, -resistant, and –heterozygous Spodoptera frugiperda on different Bt maize was evaluated.

  • Cry1A.105-resistant populations were highly cross-resistant to Cry1F maize.

  • Cry1Ab maize was marginally effective against the susceptible population of S. frugiperda.

  • Cry1A.105-resistant populations were susceptible to maize products containing Cry2Ab2 or Vip3A.

  • Maize containing both Cry2Ab2 and Vip3A should offer a means for managing the Cry1F/Cry1A.105 resistance in S. frugiperda.

Abstract

Cry1A.105 is a Cry protein expressed in some transgenic Bacillus thuringiensis (Bt) maize products. In this study, performance of five populations of fall armyworm, Spodoptera frugiperda (J.E. Smith), were evaluated on four non-Bt and eight commercial and experimental Bt maize hybrids/lines (hereafter referred as maize products). The five insect populations included one Cry1A.105-susceptible strain, two Cry1A.105-resistant strains, and two F1 heterozygous genotypes. The eight Bt maize hybrids/lines consisted of five single-gene Bt maize products containing Cry1A.105, Cry2Ab2, Cry1F, or Cry1Ab protein, and three pyramided Bt maize products expressing Cry1A.105/Cry2Ab2, Cry1A.105/Cry2Ab2/Cry1F, or Cry1Ab/Vip3A for targeting aboveground lepidopteran maize pests. In the study, neonates of each population were tested on leaf tissues in the laboratory and whole plants in the greenhouse. Cry1A.105 and Cry1F maize killed 92.2–100% susceptible larvae in both test methods, while resistant larvae survived well on these two maize products. Performance of the two F1 populations on Cry1A.105 and Cry1F maize varied between the two test methods. In leaf tissue bioassay, Cry1Ab maize was marginally effective against the susceptible population. In contrast, few live larvae and little leaf injury from any of the five populations were observed on Cry2Ab2 and the three pyramided Bt maize products. The results of this study showed evidence of cross resistance of the Cry1A.105-resistant S. frugiperda to Cry1F and Cry1Ab maize, but not to the Bt maize products containing Cry2Ab2 or Vip3A. Data generated from this study will be useful in developing resistance management strategies for the sustainable use of Bt maize technology.

Introduction

Transgenic crops (e.g. maize, cotton, and soybean) containing Bacillus thuringiensis (Bt) genes have been widely planted for controlling some major insect pests (James, 2014). As with many other pest management tools, evolution of resistance in the pest populations is a threat to the sustainable use of Bt crop technology. Since the first Bt crops were commercialized in 1996, great efforts in implementation of resistance management plans have been made for the sustainable use of Bt crop technology (Ostlie et al., 1997, Huang et al., 2011, Matten et al., 2012, Tabashnik et al., 2013). However, due to the intensive use of Bt crops over the last 20 years, field resistance resulting in insect control problems has occurred in at least four major target species in several countries (van Rensburg, 2007, Storer et al., 2010, Dhurua and Gujar, 2011, Gassmann et al., 2011, Farias et al., 2014a, Farias et al., 2014b, Huang et al., 2014).

Fall armyworm, Spodoptera frugiperda (J.E. Smith), is a target pest of both Bt maize and Bt cotton in North and South America, as well as a target pest of Bt soybean in Brazil (Farias et al., 2014a, Yang et al., 2016). Up to now, S. frugiperda is the first and only target insect that has developed field resistance to Bt crops at multiple locations across different countries and continents (Storer et al., 2010, Farias et al., 2014a, Farias et al., 2014b, Huang et al., 2014). In Puerto Rico, Cry1F maize (event TC1507) was commercially planted to control S. frugiperda in 2003, while field control problems occurred three years later (Storer et al., 2010). Similarly, in Brazil, Cry1F maize was first commercially available in the 2009/2010 season for controlling S. frugiperda and other lepidopteran pests. Field resistance in S. frugiperda was documented in 2011, and currently the resistance has spread throughout the Western Bahia region of the country (Farias et al., 2014a, Farias et al., 2014b). In addition, field resistance of S. frugiperda to Cry1F maize has also been documented in some areas of the southern United States (Huang et al., 2014).

To slow the development of resistance, maize hybrids containing two or more pyramided Bt genes have been commercialized in the United States and several other countries (Ghimire et al., 2011, Matten et al., 2012, Buntin and Flanders, 2015). 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., 2013, Yang et al., 2015). The widespread Cry1F resistance in S. frugiperda has sparked concerns about the durability of the pyramided Bt crops (Huang et al., 2014, 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. This Bt toxin is a chimeric protein incorporating domains I and II from Cry1Ab or Cry1Ac, domain III from Cry1F, and the C-terminal domain from Cry1Ac (Biosafety Clearing-House, 2014). During 2011, two Cry1A.105-resistant strains of S. frugiperda were isolated from field populations collected in Florida (Huang et al., 2016). In this study, we evaluated the survival and plant injury of these two Cry1A.105-resistant populations, along with a susceptible population and two F1 heterozygous genotypes, on commercial and experimental Bt maize hybrids/lines containing single or pyramided Bt genes (hereafter, ‘maize products’ refers to both commercial hybrids and non-commercially experimental lines). Information generated from this study should be useful in understanding the cross-resistance among the commonly used Bt maize traits and developing effective resistant management strategies for the sustainable use of Bt maize technology.

Section snippets

Insect sources

Three populations of S. frugiperda including a known Cry1A.105-susceptible strain (SS) and two Cry1A.105-resistant (FL32 and FL67) strains were used as the original insect sources in the study. SS was collected from maize fields near Weslaco, Texas, in 2013. SS was susceptible to purified proteins of Cry1A.105, Cry2Ab2, and Cry1F, as well as to maize leaf tissues and whole plants expressing Cry1A.105, Cry2Ab2, Vip3A, and Cry1F proteins (Huang et al., 2014, Huang et al., 2016). FL32 and FL67

Larval survival of S. frugiperda on leaf tissues of non-Bt and Bt maize products containing single or pyramided genes

The effects of insect population, maize product, and their interaction on larval survivorship were all significant for both trials of the leaf tissue bioassay (Table 2). The overall performance of each of the three insect populations (SS, FL32, and FL67) that were evaluated in both trials was consistent between the two trials across all the maize products, with few exceptions. In general, larvae of the three populations survived well on leaf tissues of the non-Bt maize products with a

Discussion

A previous study demonstrated that FL32 and FL67 were resistant to the Cry1A.105 protein, allowing the larvae to survive and develop on whole Cry1A.105 maize plants (Huang et al., 2016). In the present study, these two populations also survived well on the Cry1A.105 maize product in the leaf tissue bioassay and whole-plant test. The results further validate that both FL32 and FL67 are highly resistant to Cry1A.105 maize.

Understanding the functional dominance level of resistance is important in

Acknowledgements

We thank Drs. David Kerns, Mike Stout, Julien Beuzelin, and Beibei Guo for their helpful suggestions during the study. This article is published with the approval of the Director of the Louisiana Agricultural Experiment Station as manuscript No. 2016-234-26111. This project represents work supported by Monsanto Company, the USDA regional project NC246, and Hatch funds from the USDA National Institute of Food and Agriculture.

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