Journal Article

Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels

Machado, Ricardo AR, Mateo, Pierre, Erb, Matthias, Gershenzon, Jonathan, Schirmer, Stefanie, Lori, Martina, Robert, Christelle AM, Zhang, Xi

2017

نظرة عامة

Highly adapted herbivores can phenocopy two-component systems by stabilizing, sequestering and reactivating plant toxins. However, whether these traits protect herbivores against their enemies is poorly understood. We demonstrate that the western corn rootworm Diabrotica virgifera virgifera, the most damaging maize pest on the planet, specifically accumulates the root-derived benzoxazinoid glucosides HDMBOA-Glc and MBOA-Glc. MBOA-Glc is produced by D. virgifera through stabilization of the benzoxazinoid breakdown product MBOA by N-glycosylation. The larvae can hydrolyze HDMBOA-Glc, but not MBOA-Glc, to produce toxic MBOA upon predator attack. Accumulation of benzoxazinoids renders D. virgifera highly resistant to nematodes which inject and feed on entomopathogenic symbiotic bacteria. While HDMBOA-Glc and MBOA reduce the growth and infectivity of both the nematodes and the bacteria, MBOA-Glc repels infective juvenile nematodes. Our results illustrate how herbivores combine stabilized and reactivated plant toxins to defend themselves against a deadly symbiosis between the third and the fourth trophic level enemies. The western corn rootworm is the most damaging pest of maize plants. Out of sight, the larvae of this beetle feed on maize roots, and cause billions of dollars worth of losses each year. One of the reasons why this pest remains such a problem is it can adapt and resist many crop protection strategies. Biological control refers to combating a pest using its own natural enemies – for example, its predators. Biological control of the western corn rootworm has been attempted using nematode worms. Normally, the nematodes locate and enter an insect larvae, release bacteria that kill it, and then feed and multiply within the dead larvae. Yet, the western corn rootworm seems at least partly able to resist these nematodes, and the success of biological control in the field has been variable. Several insect herbivores are known to accumulate, or sequester, plant toxins in their own body for self-defense. Previously, in 2012, researchers reported that the western corn rootworm is resistant and attracted to the major toxins in maize roots, the benzoxazinoids. The blood-like fluid of the western corn rootworm also repels many predators. Could the western corn rootworm be sequestering maize benzoxazinoids to resist the biological control of nematodes and their bacterial partners? Plants store benzoxazinoids in a non-toxic form. If herbivores damage the plant, these molecules quickly break down into compounds that are toxic to most insects. Now Robert et al. – who include two of the researchers involved in the 2012 study – show that the western corn rootworm uses a similar defense system to protect itself against biological control nematodes and their bacterial partners. First, the larvae convert a benzoxazinoid breakdown product by adding a glucose molecule. They then release large amounts of this modified molecule to repel young nematodes. Second, via an unknown mechanism, the larvae stabilize a second plant-derived benzoxazinoid, sequester its non-toxic form in their bodies, and activate it upon nematode attack. The resulting toxins can kill both nematodes and their bacterial partners. By combining different chemical strategies to stabilize and activate plant toxins, the western corn rootworm is able to resist the nematodes used for biological control. These findings can help to explain why biological control has had limited success against the western corn rootworm. In the long run, they may lead to more effective biological control programs, for instance by stopping the western corn rootworm from sequestering benzoxazinoids or by using natural enemies that are resistant to the insect’s toxins.

• الناشر: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publication,eLife Sciences Publications, Ltd
• موضوع: Agricultural pests / Bacteria / Beetles / benzoxazinoid detoxification / benzoxazinoid sequestration / Biological pest control / Corn / Diabrotica undecimpunctata / Diabrotica virgifera / Diabrotica virgifera virgifera / Ecology / Enzymes / Glucose / Glucosides / Glycosylation / Herbivores / Heterorhabditis bacteriophora / Infectivity / Insects / Legal fees / Life Sciences / Metabolites / Particle size / Photorhabdus luminescens / Plant protection / Plants (Organisms) / Roundworms / Symbiosis / tritrophic interactions / Trophic levels / Vegetal Biology / Zea mays