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Cited by 388Insect-Plant Interactions and ControlPlant-Microbe Interactions and ImmunityAllelopathy and phytotoxic interactions

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Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

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Ahmad, Shakoor, Veyrat, Nathalie, Gordon-Weeks, Ruth, Zhang, Yuhua, Martin, Janet, Smart, Lesley, Glauser, Gaétan, Erb, Matthias, Flors, Victor, Frey, Monika, Ton, Jurriaan·2011·Plant Physiology
DOI 10.1104/pp.111.180224PMC PMC3165881
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Abstract

Benzoxazinoids (BXs), such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. The first step in BX biosynthesis converts indole-3-glycerol phosphate into indole. In maize (Zea mays), this reaction is catalyzed by either BENZOXAZINELESS1 (BX1) or INDOLE GLYCEROL PHOSPHATE LYASE (IGL). The Bx1 gene is under developmental control and is mainly responsible for BX production, whereas the Igl gene is inducible by stress signals, such as wounding, herbivory, or jasmonates. To determine the role of BXs in defense against aphids and fungi, we compared basal resistance between Bx1 wild-type and bx1 mutant lines in the igl mutant background, thereby preventing BX production from IGL. Compared to Bx1 wild-type plants, BX-deficient bx1 mutant plants allowed better development of the cereal aphid Rhopalosiphum padi, and were affected in penetration resistance against the fungus Setosphaeria turtica. At stages preceding major tissue disruption, R. padi and S. turtica elicited increased accumulation of DIMBOA-glucoside, DIMBOA, and 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucoside (HDMBOA-glc), which was most pronounced in apoplastic leaf extracts. Treatment with the defense elicitor chitosan similarly enhanced apoplastic accumulation of DIMBOA and HDMBOA-glc, but repressed transcription of genes controlling BX biosynthesis downstream of BX1. This repression was also obtained after treatment with the BX precursor indole and DIMBOA, but not with HDMBOA-glc. Furthermore, BX-deficient bx1 mutant lines deposited less chitosan-induced callose than Bx1 wild-type lines, whereas apoplast infiltration with DIMBOA, but not HDMBOA-glc, mimicked chitosan-induced callose. Hence, DIMBOA functions as a defense regulatory signal in maize innate immunity, which acts in addition to its well-characterized activity as a biocidal defense metabolite.

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  • Benzoxazinoid-deficient bx1 maize mutants are defective in aphid- and chitosan-induced callose deposition, and callose induction is rescued by addition of DIMBOA or DIMBOA-Glc.

    “Benzoxazinoid-deficient bx1 maize (Zea mays) mutants are defective in aphid-and chitosan-induced callose deposition, and callose induction is rescued by the addition of DIMBOA or DIMBOA-Glc (Ahmad et al., 2011;Meihls et al., 2013).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Ahmad et al., 2011

    The ‘DIMBOA Regulates Callose Deposition’ section (Fig. 7) reports reduced chitosan-induced callose in BX-deficient bx1 igl maize lines. It also reports that infiltrated DIMBOA induces callose (Fig. 8), but does not show rescue of callose induction in the mutants. The paper does not report an aphid-induced callose defect or rescue by DIMBOA-Glc; the other compound tested for callose induction was HDMBOA-glc, which had no effect. (LLM, conf=0.88)

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Metadata

Authors
Ahmad, S., Veyrat, N., Gordon-Weeks, R., Zhang, Y., Martin, J., Smart, L., Glauser, G., Erb, M., Flors, V., Frey, M., & Ton, J.
Affiliations
  • Universitat Jaume I (ES)
  • Rothamsted Research, Centre for Sustainable Pest and Disease Management, Harpenden AL5 4JQ, United Kingdom (S.A., N.V., R.G.-W., Y.Z., J.M., L.S., J.T.); Laboratory for Fundamental and Applied Research in Chemical Ecology (N.V., G.G., M.E.) and Chemical Analytical Service of the Swiss Plant Science Web (G.G.), University of Neuchâtel, CH–2009 Neuchatel, Switzerland; Plant Physiology Section, Depa
Corresponding author
Ton, Jurriaan
ORCID
Venue
Plant Physiology
Publisher
Oxford University Press (OUP)
Published
2011-07-05
Volume
157
Issue
1
Pages
317-327
ISSN
  • 0032-0889 (ISSN-L)
  • 1532-2548
DOI
10.1104/pp.111.180224
PMC
PMC3165881
OpenAlex
W2136544425
Cited by
388
References
1
Citations by year
2026: 19 · 2025: 29 · 2024: 29 · 2023: 30 · 2022: 20 · 2021: 50 · 2020: 34 · 2019: 21 · 2018: 31 · 2017: 20 · 2016: 22 · 2015: 25 · 2014: 25 · 2013: 18 · 2012: 12
FWCI
20.85
Type
journal article
Language
en
Open access
Licence
Locations
  • PLANT PHYSIOLOGY (publishedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • BORIS (University Library Bern) (submittedVersion)
  • Max Planck Digital Library (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Directorate for Biological Sciences
  • Biotechnology and Biological Sciences Research Council (BB/E023959/1)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Allelopathy and phytotoxic interactions
Keywords
benzoxazinoids, DIMBOA, maize, innate immunity, aphid resistance, Rhopalosiphum padi, chitosan, callose deposition, defense signaling, plant-fungal interactions, plant-insect interactions
MeSH terms
Animals, Aphids, Zea mays, Fungi, Immunity, Innate, Transcription, Genetic, Genes, Plant, DNA, Complementary, RNA, Plant, Benzoxazines, Real-Time Polymerase Chain Reaction

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