Aboveground Herbivory Influences Belowground Defense Responses in Maize

Lise Pingault,Gautam Sarath,W Paul Williams,Joe Louis,Saumik Basu,Nathan Palmer,Prince Zogli

doi:10.3389/fevo.2021.765940

Lise Pingault, Gautam Sarath + Show 5 more

Open Access

https://doi.org/10.3389/fevo.2021.765940

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Abstract

The European corn borer (ECB; Ostrinia nubilalis) is an economically damaging insect pest of maize (Zea mays L.), an important cereal crop widely grown globally. Among inbred lines, the maize genotype Mp708 has shown resistance to diverse herbivorous insects, although several aspects of the defense mechanisms of Mp708 plants are yet to be explored. Here, the changes in root physiology arising from short-term feeding by ECB on the shoot tissues of Mp708 plants was evaluated directly using transcriptomics, and indirectly by monitoring changes in growth of western corn rootworm (WCR; Diabrotica virgifera virgifera) larvae. Mp708 defense responses negatively impacted both ECB and WCR larval weights, providing evidence for changes in root physiology in response to ECB feeding on shoot tissues. There was a significant downregulation of genes in the root tissues following short-term ECB feeding, including genes needed for direct defense (e.g., proteinase inhibitors and chitinases). Our transcriptomic analysis also revealed specific regulation of the genes involved in hormonal and metabolite pathways in the roots of Mp708 plants subjected to ECB herbivory. These data provide support for the long-distance signaling-mediated defense in Mp708 plants and suggest that altered metabolite profiles of roots in response to ECB feeding of shoots likely negatively impacted WCR growth.

Highlights

Plants have evolved various strategies to defend themselves against insect attack, mostly through direct and indirect defenses (War et al, 2018; Nalam et al, 2019)
It was suggested that the indole-3-acetic acid (IAA) present in the oral secretions (OS) of European corn borer (ECB) may function as a herbivore-associated molecular patterns (HAMPs) in modulating maize defense responses (Dafoe et al, 2013)
Our results show that ECB growth was lower on the Mp708 plants compared to the maize inbred line Tx601 (Figure 1A)

Summary

Introduction

Plants have evolved various strategies to defend themselves against insect attack, mostly through direct and indirect defenses (War et al, 2018; Nalam et al, 2019). Among HAMPs, oral secretions (OS), saliva, frass, and herbivoreassociated endosymbionts from chewing insects have been identified in influencing plant defenses (Basu et al, 2018). Plants presumably use surface immune receptors to recognize these insect HAMPs (Steinbrenner et al, 2020), and further induce a multitude of downstream defenses to curb the insect growth and/or colonization on host plants (Basu et al, 2018; Acevedo et al, 2019; Zogli et al, 2020). ECB feeds on the aboveground parts of the maize plants and uses OS or saliva to modulate the plant defense responses. In addition to ECB OS/saliva, ECB frass was reported to modulate maize defense responses (Ray et al, 2016b)

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