Molecular dissection of rice phytohormone signaling involved in resistance to a piercing‐sucking herbivore

Abstract

Summary Phytohormone, particularly jasmonate (JA) and salicylate (SA) signaling, plays a central role in plant responses to herbivore and pathogen attack. Generally, SA mediates resistance responses against biotrophic pathogens and phloem‐feeding insects, while JA mediates responses against necrotrophic pathogens and chewing insects. The phytohormonal responses mediating rice resistance to a piercing‐sucking herbivore, the brown planthopper (BPH), remains unknown. Here, we combined transcriptome analysis, hormone measurements, genetic analysis and a field study to address this issue. Infestation by BPH adult females resulted in significant transcriptional reprograming. The upregulated genes were enriched in the JA signaling pathway. Consistently, the concentrations of JAs, but not SA, were dramatically increased in response to BPH attack. Two JA‐deficient lines (AOC and MYC2 knockout) and two SA‐deficient lines (nahG overexpression and NPR1 knockout) were constructed. BPH performed better on JA‐deficient lines than on wild‐type (WT) plants, but similarly on SA‐deficient and WT plants. During BPH attack, the accumulation of defensive secondary metabolites was attenuated in JA‐deficient lines compared with WT plants. Moreover, MYC2 mutants were more susceptible to planthoppers than WT plants in nature. This study reveals that JA signaling functions in rice defense against BPH.

Function and Mechanism of Jasmonic Acid in Plant Responses to Abiotic and Biotic Stresses

“…To deter or poison herbivores or attract their natural enemies, plants have evolved specific and complex mechanisms that are regulated through phytohormone signaling, especially the JA signaling pathway [174]. Although JAs are widely accepted to play a critical role in inducing plant defenses against herbivorous insects, the process through which plants initially activate JA biosynthesis during herbivore encounters remains unclear.…”

Bph30 confers resistance to brown planthopper by fortifying sclerenchyma in rice leaf sheaths

“…Phytohormones, particularly salicylic acid (SA) and jasmonic acid (JA), play a central role in plant responses to insects (Pieterse et al, 2012). The antagonistic effect between JA and SA was the best studied; however, SA and JA can positively regulate rice defense against BPH, which may depend on the genotype studied (Du et al, 2009;Zhao et al, 2016;He et al, 2020;Xu et al, 2021). In Bph6 plants, SA and JA seem to have synergistic effects on BPH resistance (Guo et al, 2018).…”

Silencing an E3 Ubiquitin Ligase Gene OsJMJ715 Enhances the Resistance of Rice to a Piercing-Sucking Herbivore by Activating ABA and JA Signaling Pathways

“…Moreover, exogenous ABA increases the resistance of rice to BPH by promoting callose deposition, whereas resistant varieties that were treated with fluridone exhibit susceptibility to BPH with reduced callose deposition [ 45 ]. In addition to ABA-mediated signaling pathway, JA-mediated signaling pathway also plays an important role in modulating the resistance of rice to BPH by regulating the production of defensive compounds [ 26 , 31 ]. Thus, JA and ABA signaling pathways, both of which were strengthened in ir JMJ plants compared to WT plants, might contribute to the enhanced resistance of ir JMJ plants to BPH.…”

“…To answer this question, we cloned a gene in rice, OsJMJ715 , which contains a JmjC domain and a RING domain, and is induced by gravid BPH female infestation (according to transcriptome data in Xu et al [ 31 ]). By combining molecular biology, biochemistry, and bioassays, we found that OsJMJ715 specifically localized into the nucleus and had ubiquitination activity.…”