Comparative efficacy of gypsy moth (Lepidoptera: Erebidae) entomopathogens on transgenic blight‐tolerant and wild‐type American, Chinese, and hybrid chestnuts (Fagales: Fagaceae)

Abstract

American chestnut (Castanea dentata [Marsh.] Borkh.) was once the dominant hardwood species in Eastern North America before an exotic fungal pathogen, Cryphonectria parasitica (Murrill) Barr, functionally eliminated it across its range. One promising approach toward restoring American chestnut to natural forests is development of blight‐tolerant trees using genetic transformation. However, transformation and related processes can result in unexpected and unintended phenotypic changes, potentially altering ecological interactions. To assess unintended tritrophic impacts of transgenic American chestnut on plant–herbivore interactions, gypsy moth (Lymantria dispar L.) caterpillars were fed leaf disks excised from two transgenic events, Darling 54 and Darling 58, and four control American chestnut lines. Leaf disks were previously treated with an LD50 dose of either the species‐specific Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) or the generalist pathogen Bacillus thuringiensis subsp. kurstaki (Btk). Mortality was quantified and compared to water blank controls. Tree genotype had a strong effect on the efficacies of both pathogens. Larval mortality from Btk‐treated foliage from only one transgenic event, Darling 54, differed from its isogenic progenitor, Ellis 1, but was similar to an unrelated wild‐type American chestnut control. LdMNPV efficacy was unaffected by genetic transformation. Results suggest that although genetic modification of trees may affect interactions with other nontarget organisms, this may be due to insertion effects, and variation among different genotypes (whether transgenic or wild‐type) imparts a greater change in response than transgene presence.

Intentional introgression of a blight tolerance transgene to rescue the remnant population of American chestnut

“…It is worth noting that many of the rules or expectations from regulatory agencies overlap with our own goals in creating a safe and effective restoration tree. While we understand that reintroducing an ecologically important tree would likely have numerous effects on many aspects of the ecosystem, we would not want to release a tree if the transgene product might be detrimental to neighboring native plants, animals, or beneficial soil fungi (Brown, Newhouse, Powell, & Parry, 2020; Goldspiel, Newhouse, Gibbs, & Powell, 2019; Newhouse et al, 2018). Legal mandates of the regulatory agencies address some of the same types of questions, such as protecting the environment from novel pests and ensuring safety of human food & animal feed (McHughen & Smyth, 2012).…”

Pathogen‐induced expression of a blight tolerance transgene in American chestnut

“…The expression levels of OxO in resistant transgenic lines were determined and a theoretical threshold level of expression necessary for enhanced blight tolerance was established (Zhang et al, 2013). These blight‐tolerant transgenic lines have been intensively studied for potential environmental interactions (Brown et al, 2019; D'Amico et al, 2015; Goldspiel et al, 2018; Newhouse et al, 2018; Steiner et al, 2017) and at the time of publication for this study are undergoing US regulatory review for release and potential use in restoration.…”

Bumble bee (Bombus impatiens) survival, pollen usage, and reproduction are not affected by oxalate oxidase at realistic concentrations in American chestnut (Castanea dentata) pollen

“…Several environmental interactions have already been observed or tested experimentally with transgenic chestnuts, including mycorrhizal interactions with chestnut roots (Tourtellot 2013 ; D’Amico et al 2015 ), native seed germination through chestnut leaf litter (Newhouse et al 2018 ), insect herbivory on chestnut leaves (Brown et al 2020 ), chestnut leaf decomposition rates (Gray 2015 ), aquatic insect survival and growth on chestnut leaves (Newhouse et al 2020 ), and tadpole feeding on aquatic leaf litter (Goldspiel et al 2019 ). The overwhelming consensus from these studies is that differences between transgenic chestnuts and non-transgenic controls are either insignificant or smaller than changes resulting from traditional hybrid breeding.…”