Attack from insect herbivores poses a major threat to plant survival, and accordingly, plants have evolved sophisticated defence systems. Maize is cultivated as a staple crop worldwide, and insect feeding causes large production losses. Despite its importance in agriculture, little is known about how maize reacts to insect herbivory. Taking advantage of advances in sequencing and mass spectrometry technology, we studied the response of maize to mechanical wounding and simulated Mythimna separata (a specialist insect) herbivory by applying its oral secretions (OS) to wounds. In comparison to the responses induced by mechanical wounding, OS elicited larger and longer-lasting changes in the maize transcriptome, proteome, metabolome and phytohormones. Specifically, many genes, proteins and metabolites were uniquely induced or repressed by OS. Nearly 290 transcription factor genes from 39 families were involved in OS-induced responses, and among these, more transcription factor genes were specifically regulated by OS than by wounding. This study provides a large-scale omics dataset for understanding maize response to chewing insects and highlights the essential role of OS in plant-insect interactions.
Maize ( Zea mays ) is a staple cereal crop cultivated all over the world but that is threatened by various insects. Feeding of the lepidopteran insect Mythimna separata triggers defence signalling and increases anti-herbivore benzoxazinoids (Bxs) in the insect-damaged maize leaves. However, the herbivory-elicited within-leaf and leaf-to-leaf systemic signalling in maize remains largely unexplored. Here, we show that simulated M. separata herbivory and mechanical wounding elicited increased levels of jasmonic acid (JA), JA–Ile (JA–isoleucine conjugate) and Bxs in the damaged areas and in specific systemic regions within a leaf. Importantly, increased contents of Bxs were detected in a systemic leaf, and consistently, this leaf exhibited increased defence against M. separata . Increased JA/JA–Ile and altered transcriptome, including Bx biosynthesis genes, were detected in systemic leaves after wounding or simulated herbivory treatments, although only simulated herbivory induced increase of the contents of Bxs systemically. Promoter and co-expression analysis revealed that transcription factors bHLH57 and WRKY34 may regulate Bx biosynthesis genes in systemic leaves. Moreover, leaf ablation experiment indicated that the systemic signal rapidly exited the local leaves within 30 min after elicitation. This study provides new insight into the temporal and spatial regulation of defence responses of maize against lepidopteran insects. This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.
Biotic and abiotic cues can trigger priming in plants, which enables plants to respond to subsequent challenge with stronger and/or faster responses. It is well known that herbivory activates defense-related responses in systemic leaves. However, little is known about whether insect feeding activates priming in systemic leaves. To determine whether and how herbivory induces priming and maize systemic leaves a combination of insect bioassays, phytohormone and defense metabolite quantification, and genetic and transcriptome analyses were performed. Actual and simulated Mythimna separata herbivory in maize local leaves primed the systemic leaves for enhanced accumulation of JA and Bxs and increased resistance to M. separata. Activation of priming in maize systemic leaves depends on both the duration of simulated herbivory and perception of M. separata OS in the local leaves, and genetic analysis indicated that JA and Bxs mediate the primed defenses in systemic leaves. Consistently, in response to simulated herbivory, compared with non-primed systemic leaves, the primed systemic leaves exhibited a large number of genes that were uniquely regulated or showed further up- or downregulation. This study provides new insight into the regulation and ecological function of priming in maize.
Both herbivory and jasmonic acid (JA) activate the biosynthesis of defensive metabolites in maize, but the mechanism underlying this remains unclear. We generated maize mutants in which ZmMYC2a and ZmMYC2b, two transcription factor genes important in JA signaling, were individually or both knocked out. Genetic and biochemical analyses were used to elucidate the functions of ZmMYC2 proteins in the maize response to simulated herbivory and JA. Compared with the wild-type (WT) maize, the double mutant myc2ab was highly susceptible to insects, and the levels of benzoxazinoids and volatile terpenes, and the levels of their biosynthesis gene transcripts, were much lower in the mutants than in
Background The oligophagous potato tuber moth (PTM), Phthorimaea operculella, and the polyphagous beet armyworm (BAW), Spodoptera exigua, are two destructive pests of potato, and infestations can lead to serious reduction in potato yield. However, potato plant responses to the two herbivories are only poorly understood. Endogenous jasmonoyl‐isoleucine (JA‐Ile) is a signal responsible for the induction of plant anti‐herbivore defenses. Elevation of JA‐Ile by blocking its catabolism is considered to be an effective and sustainable approach to enhance plant resistance to insect pests. However, it is not clear whether this approach can enhance potato resistance to PTM and BAW. Results We demonstrated that the transcriptional changes induced by simulated PTM and BAW feeding overlap to a large extent, and that 81.5% of the PTM‐ and 90.5% of the BAW‐responsive genes were commonly regulated. We also generated potato transgenic lines, irStCYP94B3s, in which the three JA‐Ile hydroxylases were all simultaneously silenced. These lines exhibited enhanced resistance only to BAW, but not to PTM, although levels of JA‐Ile and its downstream induced defensive chemicals, including caffeoylputrescine, dicaffeoylspermidine, lyciumoside II, and the nicotianosides I, II, and VII, were all present at higher levels in PTM‐infested than in BAW‐infested irStCYP94B3s lines. Conclusion Our results provide support for the hypothesis that StCYP94B3 genes are able to act as potential targets for the control of polyphagous insect pests in potato, and reveal that the oligophagous PTM has evolved an effective mechanism to cope with JA‐Ile‐induced anti‐herbivore defenses. © 2022 Society of Chemical Industry.
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