Plants differ greatly in their susceptibility to insect herbivory, suggesting both local adaptation and resistance tradeoffs. We used maize (
Zea mays) recombinant inbred lines to map a quantitative trait locus (
QTL) for the maize leaf aphid (
Rhopalosiphum maidis) susceptibility to maize Chromosome 1. Phytochemical analysis revealed that the same locus was also associated with high levels of 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (
HDMBOA-Glc) and low levels of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside (DIMBOA-Glc). In vitro enzyme assays with candidate genes from the region of the
QTL identified three
O-methyltransferases (
Bx10a-c) that convert DIMBOA-Glc to
HDMBOA-Glc. Variation in
HDMBOA-Glc production was attributed to a natural CACTA family transposon insertion that inactivates
Bx10c in maize lines with low
HDMBOA-Glc accumulation. When tested with a population of 26 diverse maize inbred lines,
R. maidis produced more progeny on those with high
HDMBOA-Glc and low DIMBOA-Glc. Although
HDMBOA-Glc was more toxic to
R. maidis than DIMBOA-Glc in vitro, BX10c activity and the resulting decline of DIMBOA-Glc upon methylation to
HDMBOA-Glc were associated with reduced callose deposition as an aphid defense response in vivo. Thus, a natural transposon insertion appears to mediate an ecologically relevant trade-off between the direct toxicity and defense-inducing properties of maize benzoxazinoids.
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