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

Vered Tzin,Georg Jander,Ivan Galis,Yuko Hojo,Susan R Strickler,Shaoqun Zhou,Shawn A Christensen,Lee J Bartsch,Kevin R Ahern,Cairo M Archer,Lukas A Mueller

doi:10.1093/jxb/erx274

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.

Highlights

Plants perceive herbivory through mechanical cues from feeding damage, oviposition, and even insects walking on the leaf surface (Mithöfer et al, 2005; Hilker and Meiners, 2006), as well as through chemical cues from insect oral secretions and frass (Alborn et al, 1997; Ray et al, 2015)
A comparison of transcriptome data (Illumina RNAseq) with annotated gene models found in the B73 reference genome sequence (AGPv3.22; www.maizegdb.org) (Zhong et al, 2011) revealed approximately 40 000 transcripts (Supplementary Table S5)
We evaluated similarities in the expression profiles elicited by caterpillar herbivory and those induced by application of the plant hormones methyl-jasmonate, 1-aminocyclopropane-1-carboxylic acid, abscisic acid (ABA), indole-3-acetic acid, cytokinin, brassinosteroid, gibberellic acid, and salicylic acid

Summary

Introduction

Plants perceive herbivory through mechanical cues from feeding damage, oviposition, and even insects walking on the leaf surface (Mithöfer et al, 2005; Hilker and Meiners, 2006), as well as through chemical cues from insect oral secretions and frass (Alborn et al, 1997; Ray et al, 2015). In some graminaceous plants, including maize (Zea mays), wheat (Triticum aestivum), and rye (Secale cereale), JA induces the production of benzoxazinoids (Fig. 1A), a class of metabolites that can provide protection against insect herbivores, pathogens, and competing plants (Oikawa et al, 2001, 2004; Frey et al, 2009; Adhikari et al, 2015; Wouters et al, 2016). Induced benzoxazinoid accumulation and methylation of DIMBOA-Glc to produce HDMBOA-Glc in response to caterpillar feeding (Oikawa et al, 2004; Tzin et al, 2015b) has been associated with increased resistance to several lepidopteran herbivores, including Spodoptera exigua (beet armyworm), Spodoptera littoralis (Egyptian cotton leafworm), Spodoptera frugiperda (fall armyworm), and Diatraea grandiosella (southwestern corn borer) (Hedin et al, 1993; Oikawa et al, 2001; Niemeyer, 2009; Glauser et al, 2011)

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Results

Conclusion