title: Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity.
abstract: 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.
authors.affiliation: Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, USA.
authors.forename: Lisa N
authors.initials: LN
authors.lastname: Meihls
authors.forename: Vinzenz
authors.initials: V
authors.lastname: Handrick
authors.forename: Gaetan
authors.initials: G
authors.lastname: Glauser
authors.forename: Hugues
authors.initials: H
authors.lastname: Barbier
authors.forename: Harleen
authors.initials: H
authors.lastname: Kaur
authors.forename: Meena M
authors.initials: MM
authors.lastname: Haribal
authors.forename: Alexander E
authors.initials: AE
authors.lastname: Lipka
authors.forename: Jonathan
authors.initials: J
authors.lastname: Gershenzon
authors.forename: Edward S
authors.initials: ES
authors.lastname: Buckler
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.forename: Tobias G
authors.initials: TG
authors.lastname: Köllner
authors.forename: Georg
authors.initials: G
authors.lastname: Jander
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001042:Aphids / Q000502:physiology*; D048588:Benzoxazines / Q000378:metabolism*; D002874:Chromosome Mapping; D032461:Chromosomes, Plant / Q000235:genetics; D004251:DNA Transposable Elements / Q000235:genetics; D060467:Disease Resistance / Q000235:genetics; D005960:Glucosides / Q000378:metabolism; D006790:Host-Parasite Interactions; D007527:Isoenzymes / Q000145:classification / Q000235:genetics / Q000378:metabolism; D008780:Methyltransferases / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D016254:Mutagenesis, Insertional; D010802:Phylogeny; D010935:Plant Diseases / Q000235:genetics / Q000469:parasitology; D010940:Plant Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D040641:Quantitative Trait Loci / Q000235:genetics; D017386:Sequence Homology, Amino Acid; D003313:Zea mays / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology*
chemical_list: C430218:2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside; D048588:Benzoxazines; D004251:DNA Transposable Elements; D005960:Glucosides; D007527:Isoenzymes; D010940:Plant Proteins; D008780:Methyltransferases; C050733:2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one
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