Spodoptera exigua caterpillar feeding induces rapid defense responses in maize leaves

ABSTRACTInsects such as beet armyworm caterpillars (Spodoptera exigua) cause extensive damage to maize (Zea mays) by consuming foliar tissue. Maize plants respond to such insect attack by triggering defense mechanisms that involve large changes in gene expression and the biosynthesis of specialized metabolites and defense signaling molecules. To investigate dynamic maize responses to herbivore feeding, leaves of maize inbred line B73 were infested with S. exigua caterpillars for 1 to 24 hours, followed by comprehensive transcriptomic and metabolomic characterization. Our results show that the most significant gene expression responses of maize to S. exigua feeding occur at early time points, within 4 to 6 hours after caterpillar infestation. However, both gene expression and metabolite profiles continued changing during the entire 24-hour experiment while photosynthesis genes were gradually decreased. The primary and specilaze metabolism shift maught be temporal and dynamic processes in the infested leaf tissue. We analyzed the effects of mutating genes in two major defense-related pathways, benzoxazinoids (Bx1 and Bx2) and jasmonic acid (Lox8), using Dissociation (Ds) transposon insertions in maize inbred line W22. Together, these results show that maize leaves shift to implementation of chemical defenses within one hour after the initiation of caterpillar attack. Thus, the induced biosynthesis of specialized metabolites can have major effects in maize-caterpillar interactions.HIGHLIGHTA comprehensive transcriptic and metabolomic profiling time course of maize foliar responses to caterpillar feeding identifies genes for the synthesis of benzoxazinoids and phytohormones.

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Caterpillar salivary enzymes: "eliciting" a response

Phytoprotection ◽

10.7202/008904ar ◽

2004 ◽

Vol 85 (1) ◽

pp. 33-37 ◽

Cited By ~ 14

Author(s):

Magali Merkx-Jacques ◽

Jacqueline C. Bede

Keyword(s):

Artificial Diet ◽

Spodoptera Exigua ◽

Induced Defense ◽

Defense Responses ◽

Beet Armyworm ◽

Herbivorous Insect ◽

Plant Responses ◽

Plant Defense Responses ◽

Induced Defense Responses ◽

Bertha Armyworm

Abstract Plants exhibit remarkable plasticity in their ability to differentiate between herbivorous insect species and subtly adjust their defense responses to target distinct pests. One key mechanism used by plants to recognize herbivorous caterpillars is elicitors present in their oral secretions; however, these elicitors not only cause the induction of plant defenses but recent evidence suggests that they may also suppress plant responses. The absence of “expected changes” in induced defense responses of insect-infested plants has been attributed to hydrogen peroxide produced by caterpillar salivary glucose oxidase (GOX). Activity of this enzyme is variable among caterpillar species; it was detected in two generalist caterpillars, the beet armyworm (Spodoptera exigua) and the bertha armyworm (Mamestra configurata), but not in other generalist or specialist caterpillar species tested. In the beet armyworm, GOX activity fluctuated over larval development with high activity associated with the salivary glands of fourth instars. Larval salivary GOX activity of the beet armyworm and the bertha armyworm was observed to be significantly higher in caterpillars reared on artificial diet as compared with those reared on Medicago truncatula plants. This implies that a factor in the diet is involved in the regulation of caterpillar salivary enzyme activity. Therefore, plant diet may be regulating caterpillar oral elicitors that are involved in the regulation of plant defense responses: our goal is to understand these two processes.

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The race goes on: A fall armyworm-resistant maize inbred line influences insect oral secretion elicitation activity and nullifies herbivore suppression of plant defense

10.1101/2021.05.17.444416 ◽

2021 ◽

Author(s):

Saif ul Malook ◽

Xiao-Feng Liu ◽

Wende Liu ◽

Jinfeng Qi ◽

Shaoqun Zhou

Keyword(s):

Plant Defense ◽

Host Plant ◽

Inbred Line ◽

Defense Mechanisms ◽

Molecular Mechanisms ◽

Fall Armyworm ◽

Defense Responses ◽

Feeding Preference ◽

Maize Inbred Line ◽

Oral Secretion

Fall armyworm (Spodoptera frugiperda) is an invasive lepidopteran pest with strong feeding preference towards maize (Zea mays). Its success on maize is facilitated by a suite of specialized detoxification and manipulation mechanisms that curtail host plant defense responses. In this study, we identified a Chinese maize inbred line Xi502 that was able to mount effective defense in response to fall armyworm attack. Comparative transcriptomics analyses, phytohormonal measurements, and targeted benzoxazinoid quantification consistently demonstrate significant inducible defense responses in Xi502, but not in the susceptible reference inbred line B73. In 24 hours, fall armyworm larvae feeding on B73 showed accelerated maturation-oriented transcriptomic responses and more changes in detoxification gene expression compared to their Xi502-fed sibling. Interestingly, oral secretions collected from larvae fed on B73 and Xi502 leaves demonstrated distinct elicitation activity when applied on either host genotypes, suggesting that variation in both insect oral secretion composition and host plant alleles could influence plant defense response. These results revealed host plant adaptation towards counter-defense mechanisms in a specialist insect herbivore, adding yet another layer to the evolutionary arms race between maize and fall armyworm. This could facilitate future investigation into the molecular mechanisms in this globally important crop-pest interaction system.

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Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding

Journal of Experimental Botany ◽

10.1093/jxb/erx274 ◽

2017 ◽

Vol 68 (16) ◽

pp. 4709-4723 ◽

Cited By ~ 28

Author(s):

Vered Tzin ◽

Yuko Hojo ◽

Susan R Strickler ◽

Lee J Bartsch ◽

Cairo M Archer ◽

...

Keyword(s):

Spodoptera Exigua ◽

Defense Responses ◽

Maize Leaves

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The panorama of physiological responses and gene expression of whole plant of maize inbred line YQ7-96 at the three-leaf stage under water deficit and re-watering

Theoretical and Applied Genetics ◽

10.1007/s00122-011-1638-0 ◽

2011 ◽

Vol 123 (6) ◽

pp. 943-958 ◽

Cited By ~ 18

Author(s):

Hai-Feng Lu ◽

Hai-Tao Dong ◽

Chang-Bin Sun ◽

Dong-Jin Qing ◽

Ning Li ◽

...

Keyword(s):

Gene Expression ◽

Water Deficit ◽

Inbred Line ◽

Physiological Responses ◽

Maize Inbred Line ◽

Leaf Stage ◽

Whole Plant

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Transcriptomic Responses of Fall Armyworms (Spodoptera frugiperda) Feeding on a Resistant Maize Inbred Line Xi502 with High Benzoxazinoid Content

Agronomy ◽

10.3390/agronomy11122503 ◽

2021 ◽

Vol 11 (12) ◽

pp. 2503

Author(s):

Saif ul Malook ◽

Xiao-Feng Liu ◽

Caiyan Ma ◽

Jinfeng Qi ◽

Wende Liu ◽

...

Keyword(s):

Inbred Line ◽

Spodoptera Frugiperda ◽

Genetic Material ◽

Resistance Mechanism ◽

Fall Armyworm ◽

Structural Analog ◽

Defense Responses ◽

Preliminary Evidence ◽

Maize Inbred Line ◽

Detoxification Mechanisms

The fall armyworm (Spodoptera frugiperda) is a devastating invasive insect herbivore. Its success on its preferred host plant, maize (Zea mays), is supported by numerous specialized detoxification mechanisms that suppress the defense responses of maize. In this study, we used a resistant Chinese maize cultivar, Xi502, which showed slower growth and lower yield-related phenotypes compare with maize inbred line B73. Comparative transcriptomic analyses demonstrated that B73-fed fall armyworm larvae have a significantly faster transcriptomic re-configuration toward maturation compared to their siblings fed with Xi502 leaves, whereas a number of putative aromatic breakdown -related DEGs were specifically induced when feeding on Xi502. Targeted metabolomic quantification demonstrated that Xi502 contains significantly higher levels of various benzoxazinoid compounds. Artificial feeding with the structural analog of a benzoxazinoid compound preferentially accumulated in Xi502 demonstrated a significant growth inhibition effect on FAW larvae. These results provide important genetic material and preliminary evidence for further dissection of the FAW-resistance mechanism in maize.

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Comprehensive Analysis of Gene Expression Profiles of the Beet Armyworm Spodoptera exigua Larvae Challenged with Bacillus thuringiensis Vip3Aa Toxin

PLoS ONE ◽

10.1371/journal.pone.0081927 ◽

2013 ◽

Vol 8 (12) ◽

pp. e81927 ◽

Cited By ~ 32

Author(s):

Yolanda Bel ◽

Agata K. Jakubowska ◽

Juliana Costa ◽

Salvador Herrero ◽

Baltasar Escriche

Keyword(s):

Gene Expression ◽

Bacillus Thuringiensis ◽

Spodoptera Exigua ◽

Expression Profiles ◽

Gene Expression Profiles ◽

Comprehensive Analysis ◽

Beet Armyworm

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Whole-genome and time-course dual RNA-Seq analyses reveal chronic pathogenicity-related gene dynamics in the ginseng rusty root rot pathogen Ilyonectria robusta

Scientific Reports ◽

10.1038/s41598-020-58342-7 ◽

2020 ◽

Vol 10 (1) ◽

Cited By ~ 1

Author(s):

Yiming Guan ◽

Meili Chen ◽

Yingying Ma ◽

Zhenglin Du ◽

Na Yuan ◽

...

Keyword(s):

Gene Expression ◽

Root Rot ◽

Time Course ◽

Expression Patterns ◽

Defense Responses ◽

Infection Process ◽

Ginseng Root ◽

Gene Expression Patterns ◽

Rna Seq ◽

First Time

Abstract Ilyonectria robusta causes rusty root rot, the most devastating chronic disease of ginseng. Here, we for the first time report the high-quality genome of the I. robusta strain CD-56. Time-course (36 h, 72 h, and 144 h) dual RNA-Seq analysis of the infection process was performed, and many genes, including candidate effectors, were found to be associated with the progression and success of infection. The gene expression profile of CD-56 showed a trend of initial inhibition and then gradually returned to a profile similar to that of the control. Analyses of the gene expression patterns and functions of pathogenicity-related genes, especially candidate effector genes, indicated that the stress response changed to an adaptive response during the infection process. For ginseng, gene expression patterns were highly related to physiological conditions. Specifically, the results showed that ginseng defenses were activated by CD-56 infection and persisted for at least 144 h thereafter but that the mechanisms invoked were not effective in preventing CD-56 growth. Moreover, CD-56 did not appear to fully suppress plant defenses, even in late stages after infection. Our results provide new insight into the chronic pathogenesis of CD-56 and the comprehensive and complex inducible defense responses of ginseng root to I. robusta infection.

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