Induction and detoxification of maize 1,4‐benzoxazin‐3‐ones by insect herbivores

Abstract

SUMMARYIn monocotyledonous plants, 1,4-benzoxazin-3-ones, also referred to as benzoxazinoids or hydroxamic acids, are one of the most important chemical barriers against herbivores. However, knowledge about their behavior after attack, mode of action and potential detoxification by specialized insects remains limited. We chose an innovative analytical approach to understand the role of maize 1,4-benzoxazin-3-ones in plant-insect interactions. By combining unbiased metabolomics screening and simultaneous measurements of living and digested plant tissue, we created a quantitative dynamic map of 1,4-benzoxazin-3-ones at the plant-insect interface. Hypotheses derived from this map were tested by specifically developed in vitro assays using purified 1,4-benzoxazin-3-ones and active extracts from mutant plants lacking 1,4-benzoxazin-3-ones. Our data show that maize plants possess a two-step defensive system that effectively fends off both the generalist Spodoptera littoralis and the specialist Spodoptera frugiperda. In the first step, upon insect attack, large quantities of 2-b-D-glucopyranosyloxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA-Glc) are formed. In the second step, after tissue disruption by the herbivores, highly unstable 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA) is released by plant-derived b-glucosidases. HDMBOA acts as a strong deterrent to both S. littoralis and S. frugiperda. Although constitutively produced 1,4-benzoxazin-3-ones such as 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) are detoxified via glycosylation by the insects, no conjugation of HDMBOA in the insect gut was found, which may explain why even the specialist S. frugiperda has not evolved immunity against this plant defense. Taken together, our results show the benefit of using a plant-insect interface approach to elucidate plant defensive processes and unravel a potent resistance mechanism in maize.

Influence of drought on plant performance through changes in belowground tritrophic interactions

“…In addition, to what extent the increased concentrations are the result of reduced root water contents is currently unclear. As BXDs have an important role in plant defense and protection against herbivores and pathogens (Ahmad et al., 2011; Glauser et al., 2011; Maag et al., 2016), the drought‐induced concentration increase may also alter plant interactions with other plant‐associated organisms (Erb et al., 2011; Robert et al., 2012). …”

“…BXDs were identified using synthetic standards and characteristic m/z fragments following Glauser et al. (2011). …”

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

“…Since benzoxazinoids are known to have a profound effect on maize resistance to insect herbivores (Cambier et al, 2001;Oikawa et al, 2004;Dafoe et al, 2011;Glauser et al, 2011), we measured benzoxazinoid concentration in 2-week-old seedlings of the NAM parental lines as a possible explanatory factor for the observed aphid performance differences ( Figure 2A). All of the detected benzoxazinoids showed considerable variation in the NAM parental lines (Figure 2).…”

“…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).…”

“…FW, fresh weight. Glauser et al, 2011). Thus, herbivory-induced HDMBOA-Glc accumulation creates a pool of reactive defense compounds that allows maize plants to respond more rapidly to subsequent herbivore attack.…”