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

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.

Abstract

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.     

Mechanisms of optimal defense patterns in Nicotiana attenuata: flowering attenuates herbivory-elicited ethylene and jasmonate signaling

To defend themselves against herbivore attack, plants produce secondary metabolites, which are variously inducible and constitutively deployed, presumably to optimize their fitness benefits in light of their fitness costs. Three phytohormones, jasmonates (JA) and their active forms, the JA-isoleucine (JA-Ile) and ethylene (ET), are known to play central roles in the elicitation of induced defenses, but little is known about how this mediation changes over ontogeny. The Optimal Defense Theory (ODT) predicts changes in the costs and benefits of the different types of defenses and has been usefully extrapolated to their modes of deployment. Here we studied whether the herbivore-induced accumulation of JA, JA-Ile and ET changed over ontogeny in Nicotiana attenuata, a native tobacco in which inducible defenses are particularly well studied. Herbivore-elicited ET production changed dramatically during six developmental stages, from rosette through flowering, decreasing with the elongation of the first corollas during flower development. This decrease was largely recovered within a day after flower removal by decapitation. A similar pattern was found for the herbivore-induced accumulation of JA and JA-Ile. These results are consistent with ODT predictions and suggest that the last steps in floral development control the inducibility of at least three plant hormones, optimizing defense-growth tradeoffs.     

Overexpression of OsJAC1, a Lectin Gene, Suppresses the Coleoptile and Stem Elongation in Rice

Lectin plays an Important role In defense signaling In plants, but its function In plant growth and development is not well known. Previously, we cloneds rice （Oryza sativa L.） gene OsJAC1 encoding s msnnose-blndlng Jscslln-relsted lectln, and found that OsJAC1 was Jssmonlc acid （JA） Inducible. Here we cloned the promoter of OsJAC1, and GUS activity was detected In young roots, coleoptlles, sheaths, leaves, nodes of stems, stems, rschlses, pistils, stsmens and lemmss of OsJAC1：：GUS trsnsgenlc rice, suggesting that OsJAC1 Is s constitutive expression gene In rice. Moreover, OsJAC1-overexpressed （Ubi：：OsJAC1） rice showed dwarfism with shorter coleptlles resulting from the failure of cell elongation of coleoptlles. In addition, compared with coleoptlles of wild-type plants, those of OsJAC1 overexpresslon rice were more sensitive to JA treatment. These data revealed that, besides Its roles in defense response, lectin plays an Important role in rice growth and development.     

Jasmonic acid and salicylic acid activate a common defense system in rice

Jasmonic acid (JA) and salicylic acid (SA) play important roles in plant defense systems. JA and SA signaling pathways interact antagonistically in dicotyledonous plants, but, the status of crosstalk between JA and SA signaling is unknown in monocots. Our rice microarray analysis showed that more than half of the genes upregulated by the SA analog BTH are also upregulated by JA, suggesting that a major portion of the SA-upregulated genes are regulated by JA-dependent signaling in rice. A common defense system that is activated by both JA and SA is thus proposed which plays an important role in pathogen defense responses in rice.     

Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense

The pea leafminer, Liriomyza huidobrensis, is an important pest species affecting ornamental crops worldwide. Plant damage consists of oviposition and feeding punctures created by female adult flies as well as larva-bored mines in leaf mesophyll tissues. How plants indirectly defend themselves from these two types of leafminer damage has not been sufficiently investigated. In this study, we compared the indirect defense responses of bean plants infested by either female adults or larvae. Puncturing of leaves by adults released green leaf volatiles and terpenoids, while larval feeding caused plants to additionally emit methyl salicylate and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT). Puncturing of plants by female adults induced increases in jasmonic acid (JA) and JA-related gene expressions but reduced the expressions of salicylic acid (SA)-related genes. In contrast, JA and SA and their-related gene expression levels were increased significantly by larval feeding. The exogenous application of JA+SA significantly triggered TMTT emission, thereby significantly inducing the orientation behavior of parasitoids. Our study has confirmed that larval feeding can trigger TMTT emission through the activation of both JA and SA pathways to attract parasitoids; however, TMTT alone is less attractive than the complete blend of volatiles released by infested plants.     

The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway

As important signal molecules, jasmonates (JAs) and green leaf volatiles (GLVs) play diverse roles in plant defense responses against insect pests and pathogens. However, how plants employ their specific defense responses by modulating the levels of JA and GLVs remains unclear. Here, we describe identification of a role for the rice HPL3 gene, which encodes a hydroperoxide lyase (HPL), OsHPL3/CYP74B2, in mediating plant‐specific defense responses. The loss‐of‐function mutant hpl3‐1 produced disease‐resembling lesions spreading through the whole leaves. A biochemical assay revealed that OsHPL3 possesses intrinsic HPL activity, hydrolyzing hydroperoxylinolenic acid to produce GLVs. The hpl3‐1 plants exhibited enhanced induction of JA, trypsin proteinase inhibitors and other volatiles, but decreased levels of GLVs including (Z)‐3‐hexen‐1‐ol. OsHPL3 positively modulates resistance to the rice brown planthopper [BPH, Nilaparvata lugens (Stål)] but negatively modulates resistance to the rice striped stem borer [SSB, Chilo suppressalis (Walker)]. Moreover, hpl3‐1 plants were more attractive to a BPH egg parasitoid, Anagrus nilaparvatae, than the wild‐type, most likely as a result of increased release of BPH‐induced volatiles. Interestingly, hpl3‐1 plants also showed increased resistance to bacterial blight (Xanthomonas oryzae pv. oryzae). Collectively, these results indicate that OsHPL3, by affecting the levels of JA, GLVs and other volatiles, modulates rice‐specific defense responses against different invaders.     

Herbivore-specific plant volatiles prime neighboring plants for nonspecific defense responses

Plants produce species-specific herbivore-induced plant volatiles (HIPVs) after damage. We tested the hypothesis that herbivore-specific HIPVs prime neighboring plants to induce defenses specific to the priming herbivore. Since Manduca sexta (specialist) and Heliothis virescens (generalist) herbivory induced unique HIPV profiles in Nicotiana benthamiana, we used these HIPVs to prime receiver plants for defense responses to simulated herbivory (mechanical wounding and herbivore regurgitant application). Jasmonic acid (JA) accumulations and emitted volatile profiles were monitored as representative defense responses since JA is the major plant hormone involved in wound and defense signaling and HIPVs have been implicated as signals in tritrophic interactions. Herbivore species-specific HIPVs primed neighboring plants, which produced 2 to 4 times more volatiles and JA after simulated herbivory when compared to similarly treated constitutive volatile-exposed plants. However, HIPV-exposed plants accumulated similar amounts of volatiles and JA independent of the combination of priming or challenging herbivore. Furthermore, volatile profiles emitted by primed plants depended only on the challenging herbivore species but not on the species-specific HIPV profile of damaged emitter plants. This suggests that feeding by either herbivore species primed neighboring plants for increased HIPV emissions specific to the subsequently attacking herbivore and is probably controlled by JA.     

Previous infestation of pea aphids Acyrthosiphon pisum on broad bean plants resulted in the increased performance of conspecific nymphs on the plants

Abstract

We studied the effects of previous infestation of broad bean plants by pea aphids Acyrthosiphon pisum on the performance of conspecific nymphs on the plants and the involvement of jasmonic acid (JA)-related defenses. The time needed for newly emerged nymphs to become reproductive adults on broad bean plants previously infested by conspecifics (pre-infested plants) was significantly shorter than on uninfested (control) broad bean plants. The total numbers of nymphs produced by aphids on preinfested and control plants were not significantly different. Preinfested plants produced significantly less endogenous JA than that control plants did. To test the effect of JA decreases, we conducted experiments on the developmental duration of nymphs on broad bean plants treated with JA (JA-treated plants) before infestation. The time needed for nymphs to become reproductive adults on JA treated preinfested broad bean plants was not significantly different from that on JA-treated control plants. The results suggested a possible parental care by pea aphids: the adult aphids manipulated JA-related defenses in broad bean plants that had positive effects for their offspring.     

Elevated CO2 differentially affects tobacco and rice defense against lepidopteran larvae via the jasmonic acid signaling pathway

Atmospheric CO_2 levels are rapidly increasing due to human activities. However, the effects of elevated CO_2(ECO_2) on plant defense against insects and the underlying mechanisms remain poorly understood. Here we show that ECO_2 increased the photosynthetic rates and the biomass of tobacco and rice plants, and the chewing lepidopteran insects Spodoptera litura and Mythimna separata gained less and more mass on tobacco and rice plants, respectively. Consistently, under ECO_2, the levels of jasmonic acid(JA), the main phytohormone controlling plant defense against these lepidopteran insects, as well as the main defense-related metabolites, were increased and decreased in insectdamaged tobacco and rice plants. Importantly, bioassaysand quantification of defense-related metabolites in tobacco and rice silenced in JA biosynthesis and perception indicate that ECO_2 changes plant resistance mainly by affecting the JA pathway. We further demonstrate that the defensive metabolites, but not total N or protein, are the main factors contributing to the altered defense levels under ECO_2. This study illustrates that ECO_2 changes the interplay between plants and insects, and we propose that crops should be studied for their resistance to the major pests under ECO_2 to predict the impact of ECO_2 on future agroecosystems.     

Host plants alter their volatiles to help a solitary egg parasitoid distinguish habitats with parasitized hosts from those without

When attacked by herbivores, plants emit volatiles to attract parasitoids and predators of herbivores. However, our understanding of the effect of plant volatiles on the subsequent behaviour of conspecific parasitoids when herbivores on plants are parasitized is limited. In this study, rice plants were infested with gravid females of the brown planthopper (BPH) Nilaparvata lugens for 24 hr followed by another 24 hr in which the BPH eggs on plants were permitted to be parasitized by their egg parasitoid, Anagrus nilaparvatae; volatiles from rice plants that underwent such treatment were less attractive to subsequent conspecific parasitoids compared to the volatiles from plants infested with gravid BPH females alone. Chemical analysis revealed that levels of JA and JA-Ile as well as of four volatile compounds—linalool, MeSA, α-zingiberene and an unknown compound—from plants infested with BPH and parasitized by wasps were significantly higher than levels of these compounds from BPH-infested plants. Laboratory and field bioassays revealed that one of the four increased chemicals—α-zingiberene—reduced the plant's attractiveness to the parasitoid. These results suggest that host plants can fine-tune their volatiles to help egg parasitoids distinguish host habitats with parasitized hosts from those without.     

Effects of nitrogen on the tolerance of brown planthopper, Nilaparvata Lugens, to adverse environmental factors

The effect of nitrogen content in rice plants on the tolerance of brown planthopper (BPH), Nilaparvata lugens Stal to high temperature, starvation and insecticide, was studied in the laboratory at International Rice Research Institute (IRRI), Philippines. Survival of nymphs and adults, fecundity and egg hatchability were significantly increased by the increase of nitrogen content in host plants at 38℃. Moreover, the survival of nymphs,fecundity and egg hatchability were significantly higher in BPH populations on rice plants with a high nitrogen regimen than those on rice plants with a low nitrogen regimen.Meanwhile, the tolerance of female adults to starvation and nymphs to growth regulator buprofezin on rice plants with a high nitrogen regimen were slightly increased. This indicates that the tolerances of BPH to adverse environmental stresses were positively increased by the application of nitrogenous fertilizer. The outbreak potential of BPH induced by the excessive application of fertilizer in rice fields was also discussed.     

南方水稻黑条矮缩病对褐飞虱和白背飞虱体内三种保护酶活性的影响

为探寻植物感染病毒病后对刺吸性害虫体内生化酶活性的影响,本文研究了感染南方水稻矮缩病毒(Southern rice black-streaked dwarf virus,SRBSDV)的水稻对褐飞虱Nilaparvata lugens和白背飞虱Sogatella furcifera成虫及若虫体内三种保护酶活性的影响。结果表明,取食染病水稻的白背飞虱和褐飞虱成虫及若虫体内超氧化物歧化酶(superoxide dismutase,SOD)、过氧化物酶(peroxidase,POD)和过氧化氢酶(catalase,CAT)的活性均随取食时间的延长而增加。在带毒水稻上取食12 h后,白背飞虱成虫、褐飞虱成虫、若虫体内SOD活性与对照比差异不显著外,其他均显著高于对照;取食24 h后,白背飞虱若虫体内SOD、POD活性和褐飞虱若虫SOD活性虽高于对照但未达显著水平;取食5 d后,白背飞虱若虫、褐飞虱成虫、若虫POD活性未达显著外,其他均显著高于对照。以上研究结果可为进一步研究植物-病毒-寄主三种之间的关系提供参考。