Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory

Abstract

Plants defend against attack from herbivores by direct and indirect defence mechanisms mediated by the accumulation of phytoalexins and release of volatile signals, respectively. While the defensive arsenals of some plants, such as tobacco and Arabidopsis are well known, most of rice's (Oryza sativa) defence metabolites and their effectiveness against herbivores remain uncharacterized. Here, we used a non-biassed metabolomics approach to identify many novel herbivory-regulated metabolic signatures in rice. Most were up-regulated by herbivore attack while only a few were suppressed. Two of the most prominent up-regulated signatures were characterized as phenolamides (PAs), p-coumaroylputrescine and feruloylputrescine. PAs accumulated in response to attack by both chewing insects, i.e. feeding of the lawn armyworm (Spodoptera mauritia) and the rice skipper (Parnara guttata) larvae, and the attack of the sucking insect, the brown planthopper (Nilaparvata lugens, BPH). In bioassays, BPH insects feeding on 15% sugar solution containing p-coumaroylputrescine or feruloylputrescine, at concentrations similar to those elicited by heavy BPH attack in rice, had a higher mortality compared to those feeding on sugar diet alone. Our results highlight PAs as a rapidly expanding new group of plant defence metabolites that are elicited by herbivore attack, and deter herbivores in rice and other plants.

Modulation of plant defense responses to herbivores by simultaneous recognition of different herbivore-associated elicitors in rice

“…1a), and additionally, it elicited two diterpene phytoalexins, momilactone A (MoA) and momilactone B (MoB) in rice leaves. This was in contrast with the previous report on low and inconsistent elicitation of MoA and MoB in rice leaves by two other chewing herbivores, S. mauritia and P. guttata 2324.…”

“…For example, tobacco and periwinkle ( Catharanthus roseus ) cell cultures treated with MeJA (volatile form of JA), and rice cells treated with JA produced large amounts of secondary metabolites that were also found in the intact plants214647. Non-green rice cells used in our study accumulated high levels of PAs, CoP and FP, known to act in defense against sucking insects23. Although we could not yet demonstrate the efficacy of phenolamides against rice chewing herbivores, by supplying them in artificial diet to M. lorey i or S. mauritia larvae, previous work with tobacco silenced in the expression of the master phenolamide regulator MYB8 showed that PAs are important players in plant defense against leaf chewers22.…”

“…Subsequently, we chose PAs (CoP and FP) as the main guide compounds for tracing OS MYL -associated elicitor activities in rice cell system. Although MYL was used as primary source of the elicitor-active OS, we also included a specialist insect, rice skipper P. guttata 23 (abbreviated as “PAG” hereafter) in our current study. We assumed that in adaptive evolution, the insects with different levels of specialization to their host plants might have evolved somewhat different spectrum of elicitor and/or effector activities in the OS.…”

“…Notably, the suppression of PAs, p- coumaroylputrescine (CoP), caffeoylputrescine (CP) and feruloylputrescine (FP) by down-regulating the key transcriptional regulator MYB8 significantly compromised the N. attenuata defense against chewing herbivores22. Recently, the accumulation and defense function of CoP and FP in rice against sucking insects has also been reported2324.…”

“…Succinct metabolic responses to herbivores23, large variety of natural pests, and multitude of genetic resources indicated rice as prime model for the study of plant-insect interactions in monocots. In addition to PAs, rice plants accumulate momilactone diterpenes25, proteinase inhibitors26, and emit many VOCs in response to herbivore attack27.…”