OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice

Abstract

KEY MESSAGE : Silencing OsMPK3 decreased elicited JA levels, which subsequently reduced levels of herbivore-induced trypsin protease inhibitors (TrypPIs) and improved the performance of SSB larvae, but did not influence BPH. Mitogen-activated protein kinases (MPKs) are known to play an important role in plant defense by transferring biotic and abiotic signals into programmed cellular responses. However, their functions in the herbivore-induced defense response in rice remain largely unknown. Here, we identified a MPK3 gene from rice, OsMPK3, and found that its expression levels were up-regulated in response to infestation by the larvae of the striped stem borer (SSB) (Chilo suppressalis), to mechanical wounding and to treatment with jasmonic acid (JA), but not to infestation by the brown planthopper (BPH) Nilaparvata lugens or to treatment with salicylic acid. Moreover, mechanical wounding and SSB infestation induced the expression of OsMPK3 strongly and quickly, whereas JA treatment induced the gene more weakly and slowly. Silencing OsMPK3 (ir-mpk3) reduced the expression of the gene by 50-70 %, decreased elicited levels of JA and diminished the expression of a lipoxygenase gene OsHI-LOX and an allene oxide synthase gene OsAOS1. The reduced JA signaling in ir-mpk3 plants decreased the levels of herbivore-induced trypsin protease inhibitors (TrypPIs) and improved the performance of SSB larvae, but did not influence BPH. Our findings suggest that the gene OsMPK3 responds early in herbivore-induced defense and can be regulated by rice plants to activate a specific and appropriate defense response to different herbivores.

The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of map kinase activity

“…The importance of JA, SA, and ET in rice defense against herbivores has also been reported previously (Zhou et al, 2009;Lu et al, 2011;Li et al, 2013;Wang et al, 2013). To evaluate whether the altered expression of OsWRKY53 affected the production of JA, JA-Ile, SA, and ET, levels of these phytohormones were quantified …”

“…We used the antisense expression lines OsMPK3 (as-mpk3) and OsMPK6 (as-mpk6), which had expression levels of 30% and 40% of OsMPK3 and OsMPK6 transcripts compared with wild-type plants Wang et al, 2013). Transcript levels of OsWRKY53 were significantly reduced in as-mpk3 and as-mpk6 plants compared with wild-type plants measured 30 and 60 min after infestation with SSB larvae (Fig.…”

“…Given the fact that MPK3 and MPK6 play an important role in plant defense responses by regulating defense-related signaling pathways, such as JA, SA, and ET (Schweighofer et al, 2007;Li et al, 2012;Tsuda et al, 2013;Wang et al, 2013), and that herbivore Mean transcript levels (+SE, n = 5) of OsWRKY53 in as-acs (A), as-lox (B), asaos1 (C), and as-aos2 (D) lines and wild-type (WT) plants that were individually infested by a third-instar SSB larva. Asterisks indicate significant differences in as-acs, as-lox, as-aos1, and as-aos2 lines compared with wild-type plants (*, P , 0.05; and **, P , 0.01, Student's t tests).…”

“…1), we propose that OsWRKY53 may function mainly as a regulator for herbivoreinduced defense responses and may allow plants to control the strength of their defense response and investment during early signaling. SSB infestation elicits a MPK3-dependent JA burst (Wang et al, 2013) that reaches a maximum at 3 h after infestation and subsides to control levels at 8 h . The early expression pattern of OsWRKY53 upon SSB attack fits its role as a negative regulator that contributes to bringing JA signaling down after the initial burst (Fig.…”

“…SSB larvae bore into and feed on rice stems, which results in dead heart and white heads symptoms at the vegetative and reproductive stage, respectively (Cheng and He, 1996). SSB attack in rice induces the biosynthesis of a variety of phytohormones, including JA, SA, and ET, which, in turn, regulate defense responses, such as the production of herbivore-induced volatiles and the accumulation of trypsin protease inhibitors (TrypPIs; Lou et al, 2005;Zhou et al, 2009;Lu et al, 2011;Qi et al, 2011;Li et al, 2013;Wang et al, 2013). Given the importance of WRKYs in mediating signaling pathways and defense responses, we isolated the rice group I WRKY TF OsWRKY53 and elucidated its roles in herbivore-induced defense responses.…”