Rapidly Induced Chemical Defenses in Maize Stems and Their Effects on Short-term Growth of Ostrinia nubilalis

Abstract

Plants damaged by insect herbivory often respond by inducing a suite of defenses that can negatively affect an insect's growth and fecundity. Ostrinia nubilalis (European corn borer, ECB) is one of the most devastating insect pests of maize, and in the current study, we examined the early biochemical changes that occur in maize stems in response to ECB herbivory and how these rapidly induced defenses influence the growth of ECB. We measured the quantities of known maize defense compounds, benzoxazinoids and the kauralexin class of diterpenoid phytoalexins. ECB herbivory resulted in decreased levels of the benzoxazinoid, 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one)-β-D-glucopyranose (DIMBOA-Glc), and a corresponding increase in 2-(2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one)-β-D-glucopyranose (HDMBOA-Glc). Total quantities of benzoxazinoids and kauralexins were increased as early as 24 h after the initiation of ECB feeding. The plant hormones, jasmonic acid (JA) and ethylene (ET), and the transcripts encoding their key biosynthetic enzymes also accumulated in response to ECB herbivory, consistent with a role in defense regulation. The combined pharmacological application of JA and the ET precursor, 1-aminocyclopropane-1-carboxylic acid to stem internode tissue likewise resulted in changes in benzoxazinoids similar to that observed with ECB damage. Despite the fact that maize actively mounts a defense response to ECB stem feeding, no differences in percent weight gain were observed between ECB larvae that fed upon non-wounded control tissues compared to tissues obtained from plants previously subjected to 24 h ECB stem herbivory. These rapid defense responses in maize stems do not appear to negatively impact ECB growth, thus suggesting that ECB have adapted to these induced biochemical changes.

Natural Variation in Maize Aphid Resistance Is Associated with 2,4-Dihydroxy-7-Methoxy-1,4-Benzoxazin-3-One Glucoside Methyltransferase Activity

“…The nonenzymatic breakdown of the major aglucone DIMBOA results in the formation of 6-methoxybenzoxalin-3-one, which is insect deterrent (Grambow et al, 1986). Insect feeding also induces enzymatic conversion of DIMBOA-Glc to HDMBOA-Glc (Oikawa et al, 2004;Dafoe et al, 2011;Glauser et al, 2011). While HDMBOA-Glc is also activated by glucosidases during tissue maceration, further nonenzymatic breakdown is faster for HDMBOA than DIMBOA (Maresh et al, 2006).…”

“…While HDMBOA-Glc is also activated by glucosidases during tissue maceration, further nonenzymatic breakdown is faster for HDMBOA than DIMBOA (Maresh et al, 2006). The conversion of DIMBOA-Glc to HDMBOAGlc has been associated with increased resistance to both pathogens and herbivores (Oikawa et al, 2004;Dafoe et al, 2011; (A) The number of R. maidis progeny produced per adult aphid over 7 d is shown (mean 6 SE; n = 8; n = 18 for B73). Asterisks indicate significant differences relative to B73 (*P < 0.05, Dunnett's test).…”

Signals that stop the rot: Regulation of secondary metabolite defences in cereals

“…Parallel studies in which maize stems were infected with either R. microsporus [27] or Fusarium graminearum [28] resulted in substantial levels of JA and Et, which preceded kauralexin and zealexin accumulation, respectively. Key enzymes of the biosynthetic pathway of both phytohormones were upregulated after attack by Ostrinia nubilalis, followed by increased accumulation of phytohormones and kauralexins [92].…”

“…JA regulates DIMBOA accumulation in maize leaves as well as both the roots and above ground parts of wheat (Table 1) [93,112]. DIMBOA furthermore accumulates after Ostrinia nubilalis herbivory in conjunction with build-up of JA and Et [92]. Treatment of maize leaves with exogenous JA and E resulted in a marked increase in DIMBOA, suggesting that JA/Et synergy plays a positive role in signal transduction leading to DIMBOA accumulation [92].…”

“…DIMBOA furthermore accumulates after Ostrinia nubilalis herbivory in conjunction with build-up of JA and Et [92]. Treatment of maize leaves with exogenous JA and E resulted in a marked increase in DIMBOA, suggesting that JA/Et synergy plays a positive role in signal transduction leading to DIMBOA accumulation [92]. Additionally it has been shown that systemic ABA induces the production of DIMBOA in maize leaves after root herbivory [91].…”