ABSTRACT
Damage caused by the rice striped stem borer (SSB), Chilo suppressalis (Walker) (Lepidoptera: Pyralidae), is much more severe on indica/xian rice than on japonica/geng rice (Oryza sativa) which matches pest outbreak data in cropping regions of China. The mechanistic basis of this difference among rice subspecies remains unclear. Using transcriptomic, metabolomic and genetic analyses in combination with insect bioassay experiments, we showed that japonica and indica rice utilise different defence responses to repel SSB, and that SSB exploited plant nutrition deficiencies in different ways in the subspecies. The more resistant japonica rice induced patterns of accumulation of methyl jasmonate (MeJA-part of a defensive pathway) and vitamin B1 (VB1-a nutrition pathway) distinct from indica cultivars. Using gene-edited rice plants and SSB bioassays, we found that MeJA and VB1 jointly affected the performance of SSB by disrupting juvenile hormone levels. In addition, genetic variants of key biosynthesis genes in the MeJA and VB1 pathways (OsJMT and OsTH1, respectively) differed between japonica and indica rice and contributed to performance differences; in indica rice, SSB avoided the MeJA defence pathway and hijacked the VB1 nutrition-related pathway to promote development. The findings highlight important genetic and mechanistic differences between rice subspecies affecting SSB damage which could be exploited in plant breeding for resistance.
Subject(s)
Acetates , Cyclopentanes , Moths , Oryza , Oxylipins , Oryza/genetics , Oryza/parasitology , Oryza/physiology , Animals , Cyclopentanes/metabolism , Oxylipins/metabolism , Moths/physiology , Acetates/pharmacology , Acetates/metabolism , Gene Expression Regulation, Plant , Plant Growth Regulators/metabolism , Plant Defense Against HerbivoryABSTRACT
Herbivore-induced plant defence responses share common components with plant responses to abiotic stresses. However, whether abiotic stress-responsive factors influence the resistance of plants to herbivores by regulating these components remains largely unknown. Here, we cloned a dehydration-responsive element-binding gene in rice, OsDREB1A, and investigated its role in the resistance of rice to the phloem-feeding herbivore, brown planthopper (BPH, Nilaparvata lugens), under normal and low temperatures. We found that OsDREB1A localized to the nucleus, and its transcripts in rice were up-regulated in response to BPH infestation, low temperatures and treatment with methyl jasmonate or salicylic acid. Silencing OsDREB1A changed transcript levels of two defence-related WRKY and two PLD genes, enhanced levels of jasmonic acid (JA), JA-isoleucine and abscisic acid, and decreased the ethylene level in rice; these changes subsequently enhanced the resistance of plants to BPH, especially at 17°C, by decreasing the hatching rate and delaying the development of BPH eggs. Moreover, silencing OsDREB1A increased the growth of rice plants. These findings suggest that OsDREB1A, which positively regulates the resistance of rice to abiotic stresses, negatively regulates the resistance of rice to BPH.
Subject(s)
Hemiptera , Oryza , Animals , Cyclopentanes/pharmacology , Dehydration , Gene Expression Regulation, Plant , Hemiptera/physiology , Herbivory , Oryza/physiology , Oxylipins/pharmacology , Phloem/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified/metabolismABSTRACT
Deploying toxins in complex mixtures is thought to be advantageous and is observed during antagonistic interactions in nature. Toxin mixtures are widely utilized in medicine and pest control, as they are thought to slow the evolution of detoxification counterresponses in the targeted organisms. Here we show that caterpillars rearrange key constituents of two distinct plant defense pathways to postingestively disable the defensive properties of both pathways. Specifically, phenolic esters of quinic acid, chlorogenic acids (CAs), potent herbivore and ultraviolet (UV) defenses, are reesterified to decorate particular sugars of 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) and prevent their respective antiherbivore defense functions. This was discovered through the employment of comparative metabolomics of the leaves of Nicotiana attenuata and the frass of this native tobacco's specialist herbivore, Manduca sexta larvae. Feeding caterpillars on leaves of transgenic plants abrogated in each of the two pathways, separately and together, revealed that one of the fully characterized frass conjugates, caffeoylated HGL-DTG, originated from ingested CA and HGL-DTGs and that both had negative effects on the defensive function of the other compound class, as revealed by rates of larval mass gain. This negative defensive synergy was further explored in 183 N. attenuata natural accessions, which revealed a strong negative covariance between the two defense pathways. Further mapping analyses in a biparental recombinant inbred line (RIL) population imputed quantitative trait loci (QTLs) for the two pathways at distinct genomic locations. The postingestive repurposing of defense metabolism constituents reveals a downside of deploying toxins in mixtures, a downside which plants in nature have evolved to counter.
Subject(s)
Manduca , Animals , Herbivory , Insecta/metabolism , Larva/metabolism , Manduca/metabolism , Plant Proteins/metabolism , Nicotiana/metabolismABSTRACT
Covering: up to 2022The recent dramatic advances in our understanding of the biosynthetic pathways that produce diverse bouquets of plant-derived natural products have far surpassed our understanding of the function of these compounds for plants: how they influence a plant's Darwinian fitness in nature. Our understanding of their mechanisms, the life-processes targeted by these compounds, is similarly poorly resolved. Many plant specialized metabolites (PSMs) are further modified after ingestion by herbivores, and these post-ingestive modifications are frequently essential for PSM function. Here we summarize the biosynthesis and functional mechanisms of 17-hydroxygeranyllinalool diterpene glycosides in the ecological model plant Nicotiana attenuata, and summarize the post-ingestive modifications known from other two-component PSMs. We propose that parallel comparisons of plant natural product biosynthetic pathways and insect post-ingestive metabolism of the same plant tissues ("frassomics") will facilitate the often-elusive identification of the molecular targets of these effective chemical defenses, contribute to elucidations of post-ingestive metabolite interactions in insect guts, and predicate the rapid evolutions of resistance against insecticides inspired by PSMs. We highlight the value of conducting these parallel investigations at the level of the entire metabolome so as to include the multiple interacting pathways in both natural product biosynthesis as well as their post-ingestive processing. We introduce the concept of frass metabolite QTL (fmQTL) analysis that integrates powerful forward genetic approaches with frassomics, and suggest that insect-guided high-throughput forward- and reverse-genetics approaches in natural habitats will advance our understanding of PSM biosynthesis and function.
Subject(s)
Biological Products , Acyclic Monoterpenes , Biological Products/metabolism , Herbivory , Plants , Nicotiana/genetics , Nicotiana/metabolismABSTRACT
The native diploid tobacco Nicotiana attenuata produces abundant, potent anti-herbivore defense metabolites known as 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) whose glycosylation and malonylation biosynthetic steps are regulated by jasmonate signaling. To characterize the biosynthetic pathway of HGL-DTGs, we conducted a genome-wide analysis of uridine diphosphate glycosyltransferases (UGTs) and identified 107 family-1 UGT members. The transcript levels of three UGTs were highly correlated with the transcript levels two key HGL-DTG biosynthetic genes: geranylgeranyl diphosphate synthase (NaGGPPS) and geranyllinalool synthase (NaGLS). NaGLS's role in HGL-DTG biosynthesis was confirmed by virus-induced gene silencing. Silencing the Uridine diphosphate (UDP)-rhamnosyltransferase gene UGT91T1 demonstrated its role in the rhamnosylation of HGL-DTGs. In vitro enzyme assays revealed that UGT74P3 and UGT74P4 use UDP-glucose for the glucosylation of 17-hydroxygeranyllinalool (17-HGL) to lyciumoside I. Plants with stable silencing of UGT74P3 and UGT74P5 were severely developmentally deformed, pointing to a phytotoxic effect of the aglycone. The application of synthetic 17-HGL and silencing of the UGTs in HGL-DTG-free plants confirmed this phytotoxic effect. Feeding assays with tobacco hornworm (Manduca sexta) larvae revealed the defensive functions of the glucosylation and rhamnosylation steps in HGL-DTG biosynthesis. Glucosylation of 17-HGL is therefore a critical step that contributes to the resulting metabolites' defensive function and solves the autotoxicity problem of this potent chemical defense.
Subject(s)
Acyclic Monoterpenes/metabolism , Diterpenes/metabolism , Glycosides/metabolism , Nicotiana/metabolism , Acyclic Monoterpenes/chemistry , Animals , Biosynthetic Pathways , Gene Silencing , Glycosylation , Glycosyltransferases/metabolism , Herbivory , Larva/physiology , Manduca/physiology , Metabolomics , Necrosis , Plant Leaves/metabolism , Plants, Genetically Modified , Recombinant Proteins/metabolismABSTRACT
Many plant specialized metabolites function in herbivore defense, and abrogating particular steps in their biosynthetic pathways frequently causes autotoxicity. However, the molecular mechanisms underlying their defense and autotoxicity remain unclear. Here, we show that silencing two cytochrome P450s involved in diterpene biosynthesis in the wild tobacco Nicotiana attenuata causes severe autotoxicity symptoms that result from the inhibition of sphingolipid biosynthesis by noncontrolled hydroxylated diterpene derivatives. Moreover, the diterpenes' defensive function is achieved by inhibiting herbivore sphingolipid biosynthesis through postingestive backbone hydroxylation products. Thus, by regulating metabolic modifications, tobacco plants avoid autotoxicity and gain herbivore defense. The postdigestive duet that occurs between plants and their insect herbivores can reflect the plant's solutions to the "toxic waste dump" problem of using potent chemical defenses.
Subject(s)
Diterpenes/metabolism , Glucosides/biosynthesis , Herbivory , Manduca/physiology , Nicotiana/metabolism , Sphingolipids/biosynthesis , Animals , Cytochrome P-450 Enzyme System/genetics , Cytochrome P-450 Enzyme System/metabolism , Hydroxylation , Manduca/enzymology , Oxidoreductases/antagonists & inhibitors , Oxidoreductases/metabolism , Nicotiana/enzymologyABSTRACT
Long non-coding RNA (lncRNA) are important regulators of many biological processes in plants, including defence against pathogens; whether lncRNAs mediate defence against herbivore attack is yet to be explored. With wild tobacco, Nicotiana attenuata, and its well-characterized interactions with herbivores, we identified a total of 1,290 significantly up- or down-regulated lncRNAs in response to a precise herbivore elicitation treatment. Of these, long intergenic non-coding RNAs (lincRNAs) were the most abundant. Based on their expression patterns, these up-regulated lincRNAs were classified as early (<1 hr) or late (>3 hr) responders. The early responding lincRNAs had accumulation patterns that tracked the herbivore-elicited burst of bioactive jasmonates (JAs) and the expression of regulator genes in JA signalling which regulate plant defences against herbivores. Silencing two of these early responders in N. attenuata (JAL1 and JAL3) significantly attenuated the accumulation of JAs, JA-mediated defensives and the plant's resistance to M. sexta attack, suggesting roles in regulating JA-mediated plant defence. By lincRNA sequencing of JA-deficient lines, many late responder lincRNAs were found to be transcriptionally regulated by JA signalling. This study uncovers a new role of lncRNAs in JA-mediated herbivore resistance.
Subject(s)
Cyclopentanes/metabolism , Oxylipins/metabolism , Plant Defense Against Herbivory , Plant Growth Regulators/metabolism , RNA, Long Noncoding/metabolism , RNA, Plant/metabolism , Animals , Gene Expression Regulation, Plant/genetics , Manduca , Plant Defense Against Herbivory/genetics , Plant Defense Against Herbivory/physiology , Plant Growth Regulators/physiology , RNA, Long Noncoding/genetics , RNA, Long Noncoding/physiology , RNA, Plant/genetics , RNA, Plant/physiology , Reverse Transcriptase Polymerase Chain Reaction , Signal Transduction , Nicotiana/genetics , Nicotiana/metabolism , Nicotiana/physiologyABSTRACT
Mitogen-activated protein kinases (MAPKs) play important roles in plant development and adaptive responses to biotic and abiotic stresses. Recently, a rice MAPK gene, OsMAPK20-5, has been reported to protect rice plants against autotoxicity by suppressing herbivore-induced ethylene and nitric oxide signaling. In this context, we observed that silencing OsMAPK20-5 increased the percentage of leaf roll caused by leaf folder Cnaphalocrocis medinalis and the severity of rice blast caused by Magnaporthe grisea but decreased the severity of sheath blight caused by Rhizoctonia solani. These findings show that silencing OsMAPK20-5 has different effects on rice pests in the field, and these differences have important implications for the evolution and exploitation of resistance strategies in plants.
Subject(s)
Gene Silencing , Magnaporthe/physiology , Oryza/genetics , Oryza/microbiology , Plant Proteins/genetics , Oryza/growth & development , Plant Proteins/metabolism , Plants, Genetically ModifiedABSTRACT
The mechanisms by which plants activate and enhance defense responses have been well studied; however, the regulatory mechanisms that allow plants to avoid excessive defense responses are poorly understood. Here, we identified a group D mitogen-activated protein kinase (MAPK) gene from rice (Oryza sativa), OsMAPK20-5, whose expression was rapidly induced by infestation of gravid female adults of a destructive rice pest, brown planthopper (BPH, Nilaparvata lugens), but not by BPH nymphs. Expression silencing of OsMAPK20-5 (irMAPK) increased the accumulation of ethylene and nitric oxide (NO) after gravid female BPH infestation, and thereby increased rice plant resistance to BPH adults and oviposited eggs. However, when exposed to high densities of gravid BPH females, irMAPK plants wilted earlier than wild-type plants, which could be attributed to the hyperaccumulation of ethylene and NO in irMAPK plants. Interestingly, when released into the field, irMAPK plants displayed broad resistance to BPH and white-backed planthopper (Sogatella furcifera), the two most destructive pests of rice, and produced higher yield. Taken together, our study shows that although OsMAPK20-5 can reduce the resistance of rice plants to planthoppers, it also enables rice plants to control excessive defense responses and thereby prevents defense-response-related autotoxicity.
Subject(s)
Hemiptera/physiology , Mitogen-Activated Protein Kinases/metabolism , Oryza/enzymology , Animals , Ethylenes/metabolism , Mitogen-Activated Protein Kinases/genetics , Nitric Oxide/metabolism , Oryza/genetics , Oryza/growth & development , Oviposition , TranscriptomeABSTRACT
Plants produce many different specialized (secondary) metabolites that function in solving ecological challenges; few are known to function in growth or other primary processes. 17-Hydroxygeranylinalool diterpene glycosides (DTGs) are abundant herbivory-induced, structurally diverse and commonly malonylated defense metabolites in Nicotiana attenuata plants. By identifying and silencing a malonyltransferase, NaMaT1, involved in DTG malonylation, we found that DTG malonylation percentages are normally remarkably uniform, but when disrupted, result in DTG-dependent reduced floral style lengths, which in turn result from reduced stylar cell sizes, IAA contents, and YUC activity; phenotypes that could be restored by IAA supplementation or by silencing the DTG pathway. Moreover, the Nicotiana genus-specific JA-deficient short-style phenotype also results from alterations in DTG malonylation patterns. Decorations of plant specialized metabolites can be tuned to remarkably uniform levels, and this regulation plays a central but poorly understood role in controlling the development of specific plant parts, such as floral styles.
Subject(s)
Flowers/growth & development , Nicotiana/genetics , Plant Growth Regulators/genetics , Transferases/genetics , Cell Size , Diterpenes/chemistry , Diterpenes/metabolism , Flowers/cytology , Flowers/metabolism , Gene Expression Regulation, Plant , Gene Silencing , Glycosides/chemistry , Glycosides/metabolism , Herbivory/genetics , Herbivory/physiology , Plant Growth Regulators/metabolism , Nicotiana/growth & development , Transferases/chemistryABSTRACT
Mitogen-activated protein kinases (MPKs) play a central role not only in plant growth and development, but also in plant responses to abiotic and biotic stresses, including pathogens. Yet, their role in herbivore-induced plant defenses and their underlying mechanisms remain largely unknown. Here, we cloned a rice MPK gene, OsMPK4, whose expression was induced by mechanical wounding, infestation of the striped stem borer (SSB) Chilo suppressalis, and treatment with jasmonic acid (JA), but not by treatment with salicylic acid (SA). The overexpression of OsMPK4 (oe-MPK4) enhanced constitutive and/or SSB-induced levels of JA, jasmonoyl-l-isoleucine (JA-Ile), ethylene (ET), and SA, as well as the activity of elicited trypsin proteinase inhibitors (TrypPIs), and reduced SSB performance. On the other hand, compared to wild-type plants, oe-MPK4 lines in the greenhouse showed growth retardation. These findings suggest that OsMPK4, by regulating JA-, ET-, and SA-mediated signaling pathways, functions as a positive regulator of rice resistance to the SSB and a negative regulator of rice growth.
Subject(s)
Disease Resistance , Mitogen-Activated Protein Kinases/genetics , Mitogen-Activated Protein Kinases/metabolism , Oryza/growth & development , Animals , Cloning, Molecular , Cyclopentanes/pharmacology , Ethylenes/pharmacology , Gene Expression Regulation, Plant/drug effects , Lepidoptera/physiology , Oryza/genetics , Oryza/metabolism , Oryza/parasitology , Oxylipins/pharmacology , Plant Development , Salicylic Acid/pharmacology , Signal TransductionABSTRACT
A high light-absorption coefficient and long-range hot-carrier transport of hybrid organic-inorganic perovskites give huge potential to their composites in solar energy conversion and environmental protection. Understanding interfacial interactions and their effects are paramount for designing perovskite-based heterostructures with desirable properties. Herein, we systematically investigated the interfacial interactions in monolayer and few-layer SnS/CH3 NH3 PbI3 heterostructures and their effects on the electronic and optical properties of these structures by density functional theory. It was found that the interfacial interactions in SnS/CH3 NH3 PbI3 heterostructures were van der Waals (vdW) interactions, and they were found to be insensitive to the layer number of 2D SnS sheets. Interestingly, although their band gap decreased upon increasing the layer number of SnS, the near-gap electronic states and optical absorption spectra of these heterostructures were found to be strikingly similar. This feature was determined to be critical for the design of 2D layered SnS-based heterostructures. Strong absorption in the ultraviolet and visible-light regions, typeâ II staggered band alignment at the interface, and few-layer SnS as an active co-catalyst make 2D SnS/CH3 NH3 PbI3 heterostructures promising candidates for photocatalysis, photodetectors, and solar energy harvesting and conversion. These results provide first insight into the nature of interfacial interactions and are useful for designing hybrid organic-inorganic perovskite-based devices with novel properties.
ABSTRACT
BACKGROUND: Plant-mediated RNAi (PMRi) silencing of insect genes has enormous potential for crop protection, but whether it works robustly under field conditions, particularly with lepidopteran pests, remains controversial. Wild tobacco Nicotiana attenuata and cultivated tobacco (N. tabacum) (Solanaceae) is attacked by two closely related specialist herbivores Manduca sexta and M. quinquemaculata (Lepidoptera, Sphingidae). When M. sexta larvae attack transgenic N. attenuata plants expressing double-stranded RNA(dsRNA) targeting M. sexta's midgut-expressed genes, the nicotine-ingestion induced cytochrome P450 monooxygenase (invert repeat (ir)CYP6B46-plants) and the lyciumoside-IV-ingestion induced ß-glucosidase1 (irBG1-plants), these larval genes which are important for the larvae's response to ingested host toxins, are strongly silenced. RESULTS: Here we show that the PMRi procedure also silences the homologous genes in native M. quinquemaculata larvae feeding on irCYP6B46 and irBG1-transgenic N. attenuata plants in nature. The PMRi lines shared 98 and 96% sequence similarity with M. quinquemaculata homologous coding sequences, and CYP6B46 and BG1 transcripts were reduced by ca. 90 and 80%, without reducing the transcripts of the larvae's most similar, potential off-target genes. CONCLUSIONS: We conclude that the PMRi procedure can robustly and specifically silence genes in native congeneric insects that share sufficient sequence similarity and with the careful selection of targets, might protect crops from attack by congeneric-groups of insect pests.
Subject(s)
Manduca/drug effects , Nicotiana/genetics , RNA Interference , RNA, Small Interfering/genetics , Animals , Animals, Congenic/genetics , Animals, Congenic/metabolism , Cytochrome P-450 Enzyme System/metabolism , Gastrointestinal Tract/metabolism , Gene Expression Regulation/drug effects , Genes, Insect/genetics , Genes, Insect/physiology , Manduca/metabolism , Plants, Genetically Modified , RNA, Double-Stranded/genetics , RNA, Double-Stranded/metabolism , RNA, Small Interfering/physiology , Sequence Alignment , Nicotiana/metabolismABSTRACT
The brown planthopper (BPH) Nilaparvata lugens is one of the most destructive insect pests on rice (Oryza sativa) in Asia. After landing on plants, BPH rapidly accesses plant phloem and sucks the phloem sap through unknown mechanisms. We discovered a salivary endo-ß-1,4-glucanase (NlEG1) that has endoglucanase activity with a maximal activity at pH 6 at 37°C and is secreted into rice plants by BPH NlEG1 is highly expressed in the salivary glands and midgut. Silencing NlEG1 decreases the capacity of BPH to reach the phloem and reduces its food intake, mass, survival, and fecundity on rice plants. By contrast, NlEG1 silencing had only a small effect on the survival rate of BPH raised on artificial diet. Moreover, NlEG1 secreted by BPH did not elicit the production of the defense-related signal molecules salicylic acid, jasmonic acid, and jasmonoyl-isoleucine in rice, although wounding plus the application of the recombination protein NlEG1 did slightly enhance the levels of jasmonic acid and jasmonoyl-isoleucine in plants compared with the corresponding controls. These data suggest that NlEG1 enables the BPH's stylet to reach the phloem by degrading celluloses in plant cell walls, thereby functioning as an effector that overcomes the plant cell wall defense in rice.
Subject(s)
Endo-1,3(4)-beta-Glucanase/metabolism , Feeding Behavior/physiology , Hemiptera/physiology , Insect Proteins/metabolism , Oryza/parasitology , Amino Acid Sequence , Animals , Base Sequence , Cell Wall/metabolism , Cellulose/metabolism , Cyclopentanes/metabolism , Endo-1,3(4)-beta-Glucanase/classification , Endo-1,3(4)-beta-Glucanase/genetics , Fertility/genetics , Gene Expression Regulation, Enzymologic , Hemiptera/enzymology , Hemiptera/genetics , Host-Parasite Interactions , Insect Proteins/classification , Insect Proteins/genetics , Oxylipins/metabolism , Phloem/parasitology , Phylogeny , RNA Interference , Reverse Transcriptase Polymerase Chain Reaction , Saliva/enzymology , Sequence Homology, Amino AcidABSTRACT
WRKY transcription factors play a central role not only in plant growth and development but also in plant stress responses. However, the role of WRKY transcription factors in herbivore-induced plant defenses and their underlying mechanisms, especially in rice, remains largely unclear. Here, we cloned a rice WRKY gene OsWRKY45, whose expression was induced by mechanical wounding, by infestation of the brown planthopper (BPH, Nilaparvata lugens) and by treatment with jasmonic acid (JA) or salicylic acid (SA). The antisense expression of OsWRKY45 (as-wrky) enhanced BPH-induced levels of H2O2 and ethylene, reduced feeding and oviposition preference as well as the survival rate of BPH, and delayed the development of BPH nymphs. Consistently, lower population densities of BPH on as-wrky lines, compared to those on wild-type (WT) plants, were observed in field experiments. On the other hand, as-wrky lines in the field had lower susceptibility to sheath blight (caused by Rhizoctonia solani) but higher susceptibility to rice blast (caused by Magnaporthe oryzae) than did WT plants. These findings suggest that OsWRKY45 plays important but contrasting roles in regulating the resistance of rice to pathogens and herbivores, and attention should be paid if OsWRKY45 is used to develop disease or herbivore-resistant rice.
Subject(s)
Disease Resistance , Hemiptera/physiology , Oryza/parasitology , Transcription Factors/genetics , Animals , Cloning, Molecular , Cyclopentanes/adverse effects , Gene Expression Regulation, Plant , Oryza/genetics , Oxylipins/adverse effects , Plant Proteins/genetics , Plants, Genetically Modified , Salicylic Acid/adverse effectsABSTRACT
Jasmonic acid (JA) and related metabolites play a key role in plant defense and growth. JA carboxyl methyltransferase (JMT) may be involved in plant defense and development by methylating JA to methyl jasmonate (MeJA) and thus influencing the concentrations of JA and related metabolites. However, no JMT gene has been well characterized in monocotyledon defense and development at the molecular level. After we cloned a rice JMT gene, OsJMT1, whose encoding protein was localized in the cytosol, we found that the recombinant OsJMT1 protein catalyzed JA to MeJA. OsJMT1 is up-regulated in response to infestation with the brown planthopper (BPH; Nilaparvata lugens). Plants in which OsJMT1 had been overexpressed (oe-JMT plants) showed reduced height and yield. These oe-JMT plants also exhibited increased MeJA levels but reduced levels of herbivore-induced JA and jasmonoyl-isoleucine (JA-Ile). The oe-JMT plants were more attractive to BPH female adults but showed increased resistance to BPH nymphs, probably owing to the different responses of BPH female adults and nymphs to the changes in levels of H2 O2 and MeJA in oe-JMT plants. These results indicate that OsJMT1, by altering levels of JA and related metabolites, plays a role in regulating plant development and herbivore-induced defense responses in rice.
Subject(s)
Cyclopentanes/metabolism , Herbivory/physiology , Methyltransferases/metabolism , Oryza/enzymology , Oryza/growth & development , Oryza/physiology , Oxylipins/metabolism , Plants, Genetically Modified/enzymology , Plants, Genetically Modified/physiology , Acetates/metabolism , Gene Expression Regulation, Plant , Herbivory/genetics , Isoleucine/analogs & derivatives , Isoleucine/metabolism , Methyltransferases/genetics , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified/growth & developmentABSTRACT
Plants generally respond to herbivore attack by increasing resistance and decreasing growth. This prioritization is achieved through the regulation of phytohormonal signaling networks. However, it remains unknown how this prioritization affects resistance against non-target herbivores. In this study, we identify WRKY70 as a specific herbivore-induced, mitogen-activated protein kinase-regulated rice transcription factor that physically interacts with W-box motives and prioritizes defence over growth by positively regulating jasmonic acid (JA) and negatively regulating gibberellin (GA) biosynthesis upon attack by the chewing herbivore Chilo suppressalis. WRKY70-dependent JA biosynthesis is required for proteinase inhibitor activation and resistance against C. suppressalis. In contrast, WRKY70 induction increases plant susceptibility against the rice brown planthopper Nilaparvata lugens. Experiments with GA-deficient rice lines identify WRKY70-dependent GA signaling as the causal factor in N. lugens susceptibility. Our study shows that prioritizing defence over growth leads to a significant resistance trade-off with important implications for the evolution and agricultural exploitation of plant immunity.
Subject(s)
Gene Expression Regulation, Plant , Hemiptera/growth & development , Lepidoptera/growth & development , Oryza/immunology , Oryza/parasitology , Plant Development , Transcription Factors/metabolism , Animals , Cyclopentanes/metabolism , Gibberellins/metabolism , Herbivory/immunology , Lepidoptera/immunology , Oryza/genetics , Oxylipins/metabolism , Plant Growth Regulators/metabolismABSTRACT
Ethylene is a stress hormone with contrasting effects on herbivore resistance. However, it remains unknown whether these differences are plant- or herbivore-specific. We cloned a rice 1-aminocyclopropane-1-carboxylic acid (ACC) synthase gene, OsACS2, whose transcripts were rapidly up-regulated in response to mechanical wounding and infestation by two important pests: the striped stem borer (SSB) Chilo suppressalis and the brown planthopper (BPH) Nilaparvata lugens. Antisense expression of OsACS2 (as-acs) reduced elicited ethylene emission, SSB-elicited trypsin protease inhibitor (TrypPI) activity, SSB-induced volatile release, and SSB resistance. Exogenous application of ACC restored TrypPI activity and SSB resistance. In contrast to SSB, BPH infestation increased volatile emission in as-acs lines. Accordingly, BPH preferred to feed and oviposit on wild-type (WT) plants--an effect that could be attributed to two repellent volatiles, 2-heptanone and 2-heptanol, that were emitted in higher amounts by as-acs plants. BPH honeydew excretion was reduced and natural enemy attraction was enhanced in as-acs lines, resulting in higher overall resistance to BPH. These results demonstrate that ethylene signaling has contrasting, herbivore-specific effects on rice defense responses and resistance against a chewing and a piercing-sucking insect, and may mediate resistance trade-offs between herbivores of different feeding guilds in rice.
Subject(s)
Ethylenes/biosynthesis , Hemiptera/physiology , Herbivory , Lyases/metabolism , Oryza/physiology , Plant Proteins/metabolism , Animals , Gene Expression Regulation, Plant , Lyases/genetics , Oryza/enzymology , Oryza/genetics , Plant Proteins/genetics , Plants, Genetically ModifiedABSTRACT
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.