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Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals


Li, B; Förster, C; Robert, C A M; Züst, T; Hu, L; Machado, R A R; Berset, J-D; Handrick, V; Knauer, T; Hensel, G; Chen, W; Kumlehn, J; Yang, P; Keller, B; Gershenzon, J; Jander, G; Köllner, T G; Erb, M (2018). Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals. Science Advances, 4(12):eaat6797.

Abstract

Tailoring defense responses to different attackers is important for plant performance. Plants can use secondary metabolites with dual functions in resistance and defense signaling to mount herbivore-specific responses. To date, the specificity and evolution of this mechanism are unclear. Here, we studied the functional architecture, specificity, and genetic basis of defense regulation by benzoxazinoids in cereals. We document that DIMBOA-Glc induces callose as an aphid resistance factor in wheat. O-methylation of DIMBOA-Glc to HDMBOA-Glc increases plant resistance to caterpillars but reduces callose inducibility and resistance to aphids. DIMBOA-Glc induces callose in wheat and maize, but not in Arabidopsis, while the glucosinolate 4MO-I3M does the opposite. We identify a wheat O-methyltransferase (TaBX10) that is induced by caterpillar feeding and converts DIMBOA-Glc to HDMBOA-Glc in vitro. While the core pathway of benzoxazinoid biosynthesis is conserved between wheat and maize, the wheat genome does not contain close homologs of the maize DIMBOA-Glc O-methyltransferase genes, and TaBx10 is only distantly related. Thus, the functional architecture of herbivore-specific defense regulation is similar in maize and wheat, but the regulating biosynthetic genes likely evolved separately. This study shows how two different cereal species independently achieved herbivore-specific defense activation by regulating secondary metabolite production.

Abstract

Tailoring defense responses to different attackers is important for plant performance. Plants can use secondary metabolites with dual functions in resistance and defense signaling to mount herbivore-specific responses. To date, the specificity and evolution of this mechanism are unclear. Here, we studied the functional architecture, specificity, and genetic basis of defense regulation by benzoxazinoids in cereals. We document that DIMBOA-Glc induces callose as an aphid resistance factor in wheat. O-methylation of DIMBOA-Glc to HDMBOA-Glc increases plant resistance to caterpillars but reduces callose inducibility and resistance to aphids. DIMBOA-Glc induces callose in wheat and maize, but not in Arabidopsis, while the glucosinolate 4MO-I3M does the opposite. We identify a wheat O-methyltransferase (TaBX10) that is induced by caterpillar feeding and converts DIMBOA-Glc to HDMBOA-Glc in vitro. While the core pathway of benzoxazinoid biosynthesis is conserved between wheat and maize, the wheat genome does not contain close homologs of the maize DIMBOA-Glc O-methyltransferase genes, and TaBx10 is only distantly related. Thus, the functional architecture of herbivore-specific defense regulation is similar in maize and wheat, but the regulating biosynthetic genes likely evolved separately. This study shows how two different cereal species independently achieved herbivore-specific defense activation by regulating secondary metabolite production.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
Dewey Decimal Classification:580 Plants (Botany)
Language:English
Date:1 December 2018
Deposited On:10 Jan 2019 09:55
Last Modified:17 Sep 2019 19:51
Publisher:American Association for the Advancement of Science
ISSN:2375-2548
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1126/sciadv.aat6797
Project Information:
  • : FunderSNSF
  • : Grant ID316030_157884
  • : Project TitleSupercritical fluid chromatography tandem mass spectrometry as a new analytical tool for plant sciences
  • : FunderSNSF
  • : Grant IDPMPDP3_164480
  • : Project TitleO-methylation of DIMBOA-Glc as a key regulator of herbivore resistance in maize and wheat
  • : FunderSNSF
  • : Grant IDCRSII3_160786
  • : Project TitleSugar wars: Glucose-mediated activation, neutralization and re-activation of defensive metabolites in a soil tritrophic system

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