Natural history–guided omics reveals plant defensive chemistry against leafhopper pests

Abstract

Although much is known about plant traits that function in nonhost resistance against pathogens, little is known about nonhost resistance against herbivores, despite its agricultural importance. Empoasca leafhoppers, serious agricultural pests, identify host plants by eavesdropping on unknown outputs of jasmonate (JA)–mediated signaling. Forward- and reverse-genetics lines of a native tobacco plant were screened in native habitats with native herbivores using high-throughput genomic, transcriptomic, and metabolomic tools to reveal an Empoasca -elicited JA-JAZi module. This module induces an uncharacterized caffeoylputrescine–green leaf volatile compound, catalyzed by a polyphenol oxidase in a Michael addition reaction, which we reconstitute in vitro; engineer in crop plants, where it requires a berberine bridge enzyme-like 2 (BBL2) for its synthesis; and show that it confers resistance to leafhoppers. Natural history–guided forward genetics reveals a conserved nonhost resistance mechanism useful for crop protection.

PROTEIN S‐ACYL TRANSFERASE 13/16 modulate disease resistance by S‐acylation of the nucleotide binding, leucine‐rich repeat protein R5L1 in Arabidopsis

“…Bacterial pathogens, pests and viruses reduce overall crop yield by up to 30% (Jones et al, 2016; Huang et al, 2021; Bai et al, 2022). Pst DC3000 causes bacterial speck on tomato and Arabidopsis leaves, and infection lessens tomato quality and retards the growth and development of Arabidopsis (Wang et al, 2021).…”

“…Plants have evolved complex and effective defense mechanisms in response to various pathogen attacks (Jones and Dangl, 2006; Bai et al, 2022). The first layer of plant defense is pathogen‐associated molecular patterns (PAMPs)‐triggered immunity (PTI), most likely via a set of pattern‐recognition receptors (Zhang and Zhou, 2010; Peng et al, 2022).…”

Damage of brown planthopper (BPH) Nilaparvata lugens and rice leaf folder (LF) Cnaphalocrocis medinalis in parent plants lead to distinct resistance in ratoon rice

“…(2022) reported that JA is a major component in tobacco defending against leafhopper, a sucking insect. 44 Actually, BPH can induce the expression of OsAOS at 6 h after infestation ( Figure 1d ), and LF can also induce the expression of OsPAL1 at 1 h ( Figure 1c ), while we did not find obviously higher SA accumulation in parent plants infested by LF ( Figure 2b ), in addition, silencing of OsAOS and OsCOI1 did not enhance parents’ ( Figure 3b,c ) and ratoons’ resistance to BPH ( Figure 7b,c ); thus, our data indicates a complex interaction between JA and SA signaling during infestation of these two insects with different feeding style, further work using SA deficient mutants will be needed to determine whether the priming resistance against BPH requires SA perception in subsequently generated ratoons.…”

Harmonizing biosynthesis with post-ingestive modifications to understand the ecological functions of plant natural products

“…When released into natural habitats, these forward genetic tools can be used to study the frassomics of multitrophic interactions mediated by PSMs. 64 This journal is © The Royal Society of Chemistry 2022 Nat. Prod.…”

“…This natural history guided approach can be an enormous boon for forward-genetics guided approaches, as exemplified by the recent discovery of new defense chemistry using this approach. 64 N. attenuata plants in nature interact with more than 30 different herbivore and pathogen taxa, and these can be used to screen large forward-genetic plant populations. Five of these interacting insects are being used as high-throughput screeners to phenotype traits of N. attenuata plants.…”