Multi-Toxin Resistance Enables Pink Bollworm Survival on Pyramided Bt Cotton

Abstract

Transgenic crops producing Bacillus thuringiensis (Bt) proteins kill key insect pests, providing economic and environmental benefits. However, the evolution of pest resistance threatens the continued success of such Bt crops. To delay or counter resistance, transgenic plant “pyramids” producing two or more Bt proteins that kill the same pest have been adopted extensively. Field populations of the pink bollworm (Pectinophora gossypiella) in the United States have remained susceptible to Bt toxins Cry1Ac and Cry2Ab, but field-evolved practical resistance to Bt cotton producing Cry1Ac has occurred widely in India. Here we used two rounds of laboratory selection to achieve 18,000- to 150,000-fold resistance to Cry2Ab in pink bollworm. Inheritance of resistance to Cry2Ab was recessive, autosomal, conferred primarily by one locus, and independent of Cry1Ac resistance. We created a strain with high resistance to both toxins by crossing the Cry2Ab-resistant strain with a Cry1Ac-resistant strain, followed by one selection with Cry2Ab. This multi-toxin resistant strain survived on field-collected Bt cotton bolls producing both toxins. The results here demonstrate the risk of evolution of resistance to pyramided Bt plants, particularly when toxins are deployed sequentially and refuges are scarce, as seen with Bt cotton and pink bollworm in India.

Field‐evolved resistance of pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), to transgenic Bacillus thuringiensis (Bt) cotton expressing crystal 1Ac (Cry1Ac) and Cry2Ab in India

“…In the USA, PBW pestilence and resistance development have been effectively managed by pheromone‐based monitoring, implementation of integrated pest management (IPM) programs, including release of male sterile moths, planting of refuges and cultivation of stacked‐gene transgenic cotton . These strategies have ensured that the pest is still under control and resistance development has been delayed . In China, a small but statistically significant increase in PBW resistance to Cry1Ac was reported in the Yangtze River Valley from 2005 to 2010, but resistance did not increase until 2015 .…”

“…To counter potential problems with resistance, second‐generation transgenic cotton that produces the Bt toxin Cry2Ab in combination with Cry1Ac was developed and introduced into India in 2006. The second‐generation Bt ‐II technology was effective in controlling Cry1Ac‐resistant and Cry2Ab‐susceptible PBW, primarily because Cry2Ab and Cry1Ac bind to different receptors in PBW and also because of the negligible cross‐resistance in PBW to the two toxins . Redundant killing occurs when insects resistant to one Bt toxin are killed by another toxin in a pyramid such as Bt ‐II.…”

“…The Government of India stipulated a minimum of five border rows of conventional (n Bt ) cotton hybrid of the corresponding Bt hybrid to be planted as a ‘refuge’ around the Bt cotton field or 20% n Bt cotton of the total Bt crop area for a given acre, whichever is greater . Compliance with the requirement for refuge planting has been poor in India …”

Concepts and Strategies of Organic Plant Breeding in Light of Novel Breeding Techniques

“…The widespread use of herbicide resistant genotypes eased the workload of conventional farmers, however, it also resulted in increased herbicide residues in feed and human food [38] and within short time their benefits are overcome by resistant weeds. Similar for Bt cotton, after wide spread use, severe yield losses were caused in India in 2016 due to resistant pink bollworm attack [39]. Giving high priority to holistic approaches, the organic sector has a different risk perception and therefore different interpretation of outcomes of risk analyses.…”

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.…”