Silencing a Simple Extracellular Leucine-Rich Repeat Gene OsI-BAK1 Enhances the Resistance of Rice to Brown Planthopper Nilaparvata lugens.

Miaofen Ye,Lingfei Hu,Shuting Chen,Na Lin,Meng Ye,Peng Kuai,Yonggen Lou

doi:10.3390/ijms222212182

Miaofen Ye, Lingfei Hu + Show 5 more

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https://doi.org/10.3390/ijms222212182

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Abstract

Many plant proteins with extracellular leucine-rich repeat (eLRR) domains play an important role in plant immunity. However, the role of one class of eLRR plant proteins—the simple eLRR proteins—in plant defenses against herbivores remains largely unknown. Here, we found that a simple eLRR protein OsI-BAK1 in rice localizes to the plasma membrane. Its expression was induced by mechanical wounding, the infestation of gravid females of brown planthopper (BPH) Nilaparvata lugens or white-backed planthopper Sogatella furcifera and treatment with methyl jasmonate or abscisic acid. Silencing OsI-BAK1 (ir-ibak1) in rice enhanced the BPH-induced transcript levels of three defense-related WRKY genes (OsWRKY24, OsWRKY53 and OsWRKY70) but decreased the induced levels of ethylene. Bioassays revealed that the hatching rate was significantly lower in BPH eggs laid on ir-ibak1 plants than wild-type (WT) plants; moreover, gravid BPH females preferred to oviposit on WT plants over ir-ibak1 plants. The exogenous application of ethephon on ir-ibak1 plants eliminated the BPH oviposition preference between WT and ir-ibak1 plants but had no effect on the hatching rate of BPH eggs. These findings suggest that OsI-BAK1 acts as a negative modulator of defense responses in rice to BPH and that BPH might exploit this modulator for its own benefit.

Highlights

When attacked by herbivorous insects, plants recognize patterns associated with damage and with herbivores via pattern recognition receptors (PRRs) and respond by activating a series of early signaling events: increasing cytosolic Ca2+ concentrations, triggering a burst of reactive oxygen species (ROS) and activating mitogen-activated protein kinase (MPK) cascades [1,2]
We found that a simple extracellular leucin-rich repeat (eLRR) gene in rice, OsI-brassinosteroid insensitive 1–associated kinase 1 (BAK1), is induced by brown planthopper (BPH) or white-backed planthopper (WBPH) infestation, mechanical wounding and treatment with methyl jasmonate (MeJA) or abscisic acid (ABA)
OsI-BAK1 increased the transcript levels of defense-related genes OsMPK3, OsWRKY24, OsWRKY53 and OsWRKY70 and decreased the BPH-induced ET levels, which subsequently enhanced the resistance of rice to BPH

Summary

Introduction

When attacked by herbivorous insects, plants recognize patterns associated with damage and with herbivores via pattern recognition receptors (PRRs) and respond by activating a series of early signaling events: increasing cytosolic Ca2+ concentrations, triggering a burst of reactive oxygen species (ROS) and activating mitogen-activated protein kinase (MPK) cascades [1,2] These early events trigger signaling pathways mediated by phytohormones consisting mainly of jasmonic acid (JA), ethylene (ET) and salicylic acid (SA), which reorganize the transcriptome, proteome and metabolome, respectively, of the plant and thereby enhance plants’ resistance to herbivores [3,4,5,6]. The fitness of leaf beetles Phaedon cochleariae fed on PGIP (AtPGIP1 or AtPGIP2)-deficient plants is higher than the fitness of those fed on wild-type (WT) plants [24]

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