Resistance to Bt maize in Mythimna unipuncta (Lepidoptera: Noctuidae) is mediated by alteration in Cry1Ab protein activation

Abstract

Bt maize cultivars based on the event MON810 (expressing Cry1Ab) have shown high efficacy for controlling corn borers. However, their efficiency for controlling some secondary lepidopteran pests such as Mythimna unipuncta has been questioned, raising concerns about potential outbreaks and its economic consequences. We have selected a resistant strain (MR) of M. unipuncta, which is capable of completing its life cycle on Bt maize and displays a similar performance when feeding on both Bt and non-Bt maize. The proteolytic activation of the protoxin and the binding of active toxin to brush border membrane vesicles were investigated in the resistant and a control strain. A reduction in the activity of proteolytic enzymes, which correlates with impaired capacity of midgut extracts to activate the Cry1Ab protoxin has been observed in the resistant strain. Moreover, resistance in larvae of the MR strain was reverted when treated with Cry1Ab toxin activated with midgut juice from the control strain. All these data indicate that resistance in the MR strain is mediated by alteration of toxin activation rather than to an increase in the proteolytic degradation of the protein. By contrast, binding assays performed with biotin labelled Cry1Ab suggest that binding to midgut receptors does not play a major role in the resistance to Bt maize. Our results emphasize the risk of development of resistance in field populations of M. unipuncta and the need to consider this secondary pest in ongoing resistance management programs to avoid the likely negative agronomic and environmental consequences.

Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in Helicoverpa zea

“…For example, the lack of a protease activating Cry1Ac protoxin is linked with resistance in Plodia interpunctella and Helicoverpa armigera . Furthermore, decreased protoxin activation is implicated in resistance to Cry1Ac in Plutella xylostella , and to Cry1Ab in Ostrinia nubilalis , Heliothis virescens and Mythimna unipuncta …”

QTL Mapping for Yield and Resistance against Mediterranean Corn Borer in Maize

“…An estimated 0.1 million hectares of Bt -corn were grown in Spain in 2014 (James, 2014). However, recent studies have reported a reduced efficacy of Bt transgenes as some important pests have developed resistance to them (Campagne et al, 2013; Gonzalez-Cabrera et al, 2013). Insect resistance is the main risk for the success of this control tool (McGaughey and Whalon, 1992).…”

Inheritance, fitness costs, incomplete resistance and feeding preferences in a laboratory-selected MON810-resistant strain of the true armywormMythimna unipuncta

“…The low efficacy of Bt maize hybrids expressing the Cry1Ab toxin against M. unipuncta has raised concerns about the consequences that Bt maize deployment could have on the assemblage of the lepidopteran community in maize fields . Larvae of M. unipuncta can feed from neonates on Cry1Ab‐expressing maize plants, and about 1–2% are capable of completing their life cycle . The high rates of toxin elimination and the rapid recovery of the midgut epithelium after Bt toxin ingestion are probably involved in the basal tolerance of this species to the Cry1Ab toxin .…”

“…This situation represents a scenario of non‐compliance with the ‘high‐dose’ strategy for this species. Although outbreaks of M. unipuncta have not been reported in Bt maize fields, the populations of this secondary pest are exposed to high selection pressure in hotspot areas (high adoption rate and repeated cultivation of Bt maize) in the Ebro Valley (north‐east Spain), where the risk of field‐evolved resistance increases . Indeed, we have demonstrated that a laboratory‐selected MON810‐resistant (MR) strain of M. unipuncta was able to develop resistance to MON810 maize after 5–12 generations of laboratory selection (22–57% of the larvae completed their life cycle on Bt maize plants), this resistance being mediated by the alteration of toxin activation by midgut proteases …”