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, 68 (16), 4709-4723

Rapid Defense Responses in Maize Leaves Induced by Spodoptera Exigua Caterpillar Feeding

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Rapid Defense Responses in Maize Leaves Induced by Spodoptera Exigua Caterpillar Feeding

Vered Tzin et al. J Exp Bot.

Abstract

Insects such as the beet armyworm (Spodoptera exigua) cause extensive damage to maize (Zea mays). Maize plants respond by triggering defense signaling, changes in gene expression, and biosynthesis of specialized metabolites. Leaves of maize inbred line B73, which has an available genome sequence, were infested with S. exigua for 1 to 24 h, followed by comparisons of the transcript and metabolite profiles with those of uninfested controls. The most extensive gene expression responses occurred rapidly, within 4-6 h after caterpillar infestation. However, both gene expression and metabolite profiles were altered within 1 h and continued to change during the entire 24 h experiment. The defensive functions of three caterpillar-induced genes were examined using available Dissociation transposon insertions in maize inbred line W22. Whereas mutations in the benzoxazinoid biosynthesis pathway (Bx1 and Bx2) significantly improved caterpillar growth, the knockout of a 13-lipoxygenase (Lox8) involved in jasmonic acid biosynthesis did not. Interestingly, 9-lipoxygenases, which lead to the production of maize death acids, were more strongly induced by caterpillar feeding than 13-lipoxygenases, suggesting an as yet unknown function in maize defense against herbivory. Together, these results provide a comprehensive view of the dynamic transcriptomic and metabolomic responses of maize leaves to caterpillar feeding.

Keywords: Benzoxazinoid; RNAseq; Spodoptera exigua; Zea mays; insect herbivore; jasmonic acid; metabolite profile; time course; transcriptome.

Figures

Fig. 1.
Fig. 1.
Benzoxazinoid biosynthesis in maize. (A) Structures of maize benzoxazinoids. (B) The benzoxazinoid biosynthesis pathway in maize. Known enzymes and key pathway metabolites are indicated.
Fig. 2.
Fig. 2.
Transcriptomic and metabolomic overview of a time course of S. exigua feeding on maize inbred line B73 foliage. (A) PCA plot generated using 20 825 genes (FPKM>0 in at least 18 samples). Ovals indicate 95% confidence intervals. (B) Total number of transcripts that were significantly up- or down-regulated. (C) Venn diagram illustrating the number of genes up- or down-regulated by caterpillar infestation in the time course. P<0.05 FDR and fold change >2 or <0.5. (D, E) Untargeted metabolomics of maize leaf responses to caterpillar feeding. (D) PCA plot of negative (1024 electrospray ionization; ESI) and positive (1274 ESI) mass signals, filtered using Metaboanalyst software. Ovals indicate 95% confidence intervals. (E) Total number of mass signals that were significantly up- or down-regulated. (This figure is available in color at JXB online.)
Fig. 3.
Fig. 3.
Plant hormone signatures based on transcriptomic data generated after S. exigua feeding on maize leaves. Red indicates a positive correlation between the maize S. exigua caterpillar treatment and a particular hormonal response; blue indicates a negative correlation. ABA, abscisic acid; ACC, 1-aminocyclopropane-1-caroxylic acid (precursor of ethylene); BR, brassinosteroid; GA, gibberelic acid; IAA, indole-3-acetic acid; MJ, methyl jasmonate; SA, salicylic acid. The analysis was conducted using the Hormonometer tool (Volodarsky et al., 2009). (This figure is available in color at JXB online.)
Fig. 4.
Fig. 4.
Plant phytohormones produced after S. exigua feeding on maize leaves. ABA, abscisic acid; JA, jasmonic acid; SA, salicylic acid. Mean±SE of n=5. *P<0.05, Student’s t-test relative to uninfested control.
Fig. 5.
Fig. 5.
Effects of caterpillar feeding on jasmonic acid biosynthesis. (A) Heat map of gene expression that is related to jasmonic acid (JA) metabolism. Values are presented as fold change relative to untreated control samples. Mean±SE, n=4. (B) JA and JA conjugate levels in a lox8/ts1::Ds gene knockout line in response to caterpillar attack. Black bars, untreated; white bars, caterpillar infestation for 24 h. Different letters above the bars indicate significant differences, P<0.05, ANOVA followed by Tukey’s HSD test. (This figure is available in color at JXB online.)
Fig. 6.
Fig. 6.
Effects of caterpillar feeding on benzoxazinoid-related genes and metabolites. (A) Heat map of gene expression and (B) DIMBOA-Glc and HDMBOA-Glc abundance over time after caterpillar feeding. Values are presented as fold change relative to untreated control. Mean±SE of n=4 for transcriptomic data, n=5 for metabolomic data). (C) Abundance of DIMBOA-Glc and HDMBOA-Glc in wild-type W22, bx1::Ds, and bx2::Ds, with and without caterpillar feeding. Different letters above the bars indicate significant differences, P<0.05, ANOVA followed by Tukey’s HSD test. (D) S. exigua caterpillar body weight after 4 d on wild-type W22, bx1::Ds, and bx2::Ds mutant plants. (This figure is available in color at JXB online.)

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