The role of the benzoxazinone pathway in aphid resistance in wheat

Abstract

The hydroxamic acids or benzoxazinones (BXs) are natural cereal defence compounds, biosynthesised early in development, that deter insects, pathogens and weeds. The most active are DIMBOA and DIBOA, which are stored as their inactive glucosides in the vacuole and released upon pathogen attack or wounding.

The aim of the project was to test whether BX production can be exploited to breed wheat varieties with sufficient resistance, mainly to aphids but to certain pathogens as well, to benefit UK agriculture. The wheat BX genes (TaBXs) have been sequenced, and the molecular genetic basis for BX accumulation to be analysed.

We investigated the BX content and its variation in UK wheats by screening cultivars for TaBX expression and BX accumulation in different parts of the plant (leaf, coleoptile and root). We compared these measurements with the performance of two cereal aphids, the bird cherry oat aphid, Rhopalosiphum padi, and the grain aphid, Sitobion avenae, in bioassays to test settling preference, growth rate and fecundity on the different wheat lines. Additionally, we aimed to establish whether the pathway could be induced in the plant. This would be very advantageous as inducible defence systems are less costly to the plant.

In hexaploid wheats we did not find significant variation in regulation of the pathway but TaBX gene expression was lowest and declined most dramatically in leaf tissue. We found that the enzymes that activate the glucoside were induced by aphid feeding in the leaf and that, consequently, DIMBOA levels increased. There was variation in the degree of this response but it did not correlate clearly with resistance, possibly because overall levels of DIMBOA were too low.

When we broadened our screen to include wheats with different ploidy levels we found that a B genome wheat that contains 8 times the hexaploid levels of DIMBOA was the least favoured by aphids of all the wheats that we tested. This plant showed sustained levels of TaBX expression in the leaf, suggesting that regulation of the genes in the pathway may be important. DIMBOA was accumulated to particularly high levels in the leaf extracellular spaces through which the aphid must pass its stylet during the initial stages of feeding.

However, other diploid wheats (A and B genome) that do not contain BXs in the leaves were also more resistant than the hexaploids. These findings demonstrate that ancestral wheats display aphid resistance traits, including both BX dependent and BX independent traits, that are absent from cultivated hexaploid wheat populations. Our findings can now be used for direct breeding strategies, or genetic modification, to produce wheat plants with enhanced resistance, but the former would require wide crosses, combining different traits using germplasm from wheat with different ploidy levels.