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Plant‐mediated interactions between herbivores play an important role in regulating the composition of herbivore community. The fall armyworm (FAW), Spodoptera frugiperda, which has become one of the most serious pests on corn in China since it invaded in 2018, has been found feeding rice in the field. However, how FAW interacts with native rice insect pests remains largely unknown. Here, we investigated the interaction between FAW and a resident herbivore, striped stem borer (SSB, Chilo suppressalis) on rice. The infestation of rice leaf sheaths (LSs) by SSB larvae systemically enhanced the level of jasmonic acid (JA), abscisic acid (ABA), and trypsin proteinase inhibitors (TPIs), reduced relative water content (RWC) in leaf blades (LBs), and suppressed the growth of FAW larvae. In contrast, because FAW larvae infested LBs and did not affect defence responses in LSs, they did not influence the performance of SSB larvae. Using different mutants, together with bioassays and chemical analysis, we revealed that SSB‐induced suppression of FAW larvae growth depended on both the SSB‐activated JA pathway and RWC in LBs, whereas the ABA pathway activated by SSB larvae promoted the growth of FAW larvae by impeding water loss. These results provide new insights into mechanisms underlying plant‐mediated interactions between herbivores. Summary Statement: Striped stem borer (SSB) larvae infestation (at rice leaf sheaths [LSs]) suppresses the growth of fall armyworm (FAW) larvae (feeding on rice leaf blades) by systemically activating JA and trypsin proteinase inhibitors, as well as reducing relative water content in rice. In contrast, infestation by FAW larvae had no impact on the performance of SSB larvae because it did not influence defence responses in LSs. [ABSTRACT FROM AUTHOR]

Green leaf volatiles (GLVs) play pivotal roles in plant anti-herbivore defense. This study investigated whether the rice 13-lipoxygense gene OsRCI-1 is involved in GLV production and plant defense in rice. The overexpression of OsRCI-1 (oeRCI lines) in rice resulted in increased wound-induced levels of two prominent GLVs, cis-3-hexen-1-ol and cis-3-hexenal. In a previous study, we found that the overexpression of OsRCI-1 reduced the colonization by the rice brown planthopper (BPH, Nilaparvata lugens) but increased the attractiveness to the egg parasitoid Anagrus nilaparvatae compared to wild-type (WT) plants. This study found that when cis-3-hexen-1-ol, but not cis-3-hexenal, was added to WT plants, it could change the BPH's colonization preference, i.e., more BPHs preferred to colonize the oeRCI lines. The exogenous application of cis-3-hexen-1-ol or cis-3-hexenal to BPH-infested WT plants could weaken or overturn the preference of A. nilaparvatae for oeRCI lines. However, field experiments revealed that only cis-3-hexenal was attractive to the parasitoid and increased the parasitism rates of BPH eggs. These results indicate that OsRCI-1 is involved in rice GLV production and therefore modulates both direct and indirect defense in rice. [ABSTRACT FROM AUTHOR]

The ATP-dependent caseinolytic protease (Clp) system has been reported to play an important role in plant growth, development, and defense against pathogens. However, whether the Clp system is involved in plant defense against herbivores remains largely unclear. We explore the role of the Clp system in rice defenses against brown planthopper (BPH) Nilaparvata lugens by combining chemical analysis, transcriptome, and molecular analyses, as well as insect bioassays. We found the expression of a rice Clp proteolytic subunit gene, OsClpP6, was suppressed by infestation of BPH gravid females and mechanical wounding. Silencing OsClpP6 enhanced the level of BPH-induced jasmonic acid (JA), JA-isoleucine (JA-Ile), and ABA, which in turn promoted the production of BPH-elicited rice volatiles and increased the resistance of rice to BPH. Field trials showed that silencing OsClpP6 decreased the population densities of BPH and WBPH. We also observed that silencing OsClpP6 decreased chlorophyll content in rice leaves at early developmental stages and impaired rice root growth and seed setting rate. These findings demonstrate that an OsClpP6-mediated Clp system in rice was involved in plant growth-defense trade-offs by affecting the biosynthesis of defense-related signaling molecules in chloroplasts. Moreover, rice plants, after recognizing BPH infestation, can enhance rice resistance to BPH by decreasing the Clp system activity. The work might provide a new way to breed rice varieties that are resistant to herbivores. [ABSTRACT FROM AUTHOR]

Chemical elicitors can increase plant defense against herbivorous insects and pathogens. The use of synthetic chemical elicitors is likely to be an alternative to traditional pesticides for crop pest control. However, only a few synthetic chemicals are reported to protect plants by regulating signaling pathways, increasing the levels of defense metabolites and interfering with insect feeding. Here, we found that the exogenous application of a phenoxycarboxylic compound, 4-chlorophenoxyacetic acid (4-CPA), can induce chemical defenses to protect rice plants from white-backed planthoppers (WBPH, Sogatella furcifera). Four-CPA was rapidly taken up by plant roots and degraded to 4-chlorophenol (4-CP). Four-CPA treatment modulated the activity of peroxidase (POD) and directly induced the deposition of lignin-like polymers using hydrogen peroxide (H2O2) as the electron acceptor. The polymers, which are thought to prevent the planthopper's stylet from reaching the phloem, were broken down by WBPH nymphs. Meanwhile, 4-CPA increased the levels of flavonoids and phenolamines (PAs). The increased flavonoids and PAs, together with the degradation product of the polymers, avoided nymphal feeding and prolonged the nymphal period for 1 day. These results indicate that 4-CPA has the potential to be used as a chemical elicitor to protect rice from planthoppers. Moreover, these findings also open a pathway for molecule structure design of phenoxycarboxylic compounds as chemical elicitors. [ABSTRACT FROM AUTHOR]

Leucine-rich repeat receptor-like kinases (LRR-RLKs) are an important subfamily of receptor-like kinases (RLKs) in plants that play key roles in sensing different biotic and abiotic stress. However, the role of LRR-RLKs in herbivore-induced plant defense remains largely elusive. Here, we found that the expression of a rice gene, OsRLK7-1, was induced by mechanical wounding, but was slightly suppressed by the infestation of gravid females of brown planthopper (BPH, Nilaparvata lugens) or white-backed planthopper (WBPH, Sogatella furcifera). Through targeted disruption of OsRLK7-1 (resulting in the ko-rlk lines), we observed an augmentation in transcript levels of BPH-induced OsMPK3, OsWRKY30, OsWRKY33, and OsWRKY45, alongside heightened levels of planthopper-induced jasmonic acid, JA-isoleucine, and abscisic acid in plant tissues. These dynamic changes further facilitated the biosynthesis of multiple phenolamides within the rice plants, culminating in an enhanced resistance to planthopper infestations under both lab and field conditions. In addition, knocking out OsRLK7-1 impaired plant growth and reproduction. These results suggest that OsRLK7-1 plays an important role in regulating rice growth, development, and rice-planthopper interactions. [ABSTRACT FROM AUTHOR]

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. Summary statement: OsDREB1A, a positive modulator of rice tolerance to abiotic stress, negatively regulates the resistance of rice to BPH by influencing the biosynthesis of jasmonic acid (JA), JA‐isoleucine, abscisic acid, and ethylene. Brown planthopper appears able to use OsDREB1A to benefit itself by suppressing rice defences and resisting abiotic stresses. [ABSTRACT FROM AUTHOR]

Simple Summary: Previous studies have proved that brown planthopper (BPH), Nilaparvata lugens, a piercing–sucking herbivore, activates strong local defenses in rice. However, whether a BPH infestation elicits systemic responses in rice remains largely unknown. By detecting the change in transcript levels of 12 jasmonic acid (JA) and/or salicylic acid (SA) signaling-responsive marker genes in different tissues of rice plants upon a BPH attack, we demonstrate that an infestation of gravid BPH females systemically activates JA- and SA-dependent defenses in rice, which may in turn influence the composition and structure of the community in the rice ecosystem. It has been well documented that an infestation of the piercing–sucking herbivore, brown planthopper (BPH), Nilaparvata lugens, activates strong local defenses in rice. However, whether a BPH infestation elicits systemic responses in rice remains largely unknown. In this study, we investigated BPH-induced systemic defenses by detecting the change in expression levels of 12 JA- and/or SA-signaling-responsive marker genes in different rice tissues upon a BPH attack. We found that an infestation of gravid BPH females on rice leaf sheaths significantly increased the local transcript level of all 12 marker genes tested except OsVSP, whose expression was induced only weakly at a later stage of the BPH infestation. Moreover, an infestation of gravid BPH females also systemically up-regulated the transcription levels of three JA-signaling-responsive genes (OsJAZ8, OsJAMyb, and OsPR3), one SA-signaling-responsive gene (OsWRKY62), and two JA- and SA- signaling-responsive genes (OsPR1a and OsPR10a). Our results demonstrate that an infestation of gravid BPH females systemically activates JA- and SA-dependent defenses in rice, which may in turn influence the composition and structure of the community in the rice ecosystem. [ABSTRACT FROM AUTHOR]

Summary: The production of defensive metabolites in plants can be induced by signaling chemicals released by neighboring plants. Induction is mainly known from volatile aboveground signals, with belowground signals and their underlying mechanisms largely unknown.We demonstrate that (−)‐loliolide triggers defensive metabolite responses to competitors, herbivores, and pathogens in seven plant species. We further explore the transcriptional responses of defensive pathways to verify the signaling role of (−)‐loliolide in wheat and rice models with well‐known defensive metabolites and gene systems.In response to biotic and abiotic stressors, (−)‐loliolide is produced and secreted by roots. This, in turn, induces the production of defensive compounds including phenolic acids, flavonoids, terpenoids, alkaloids, benzoxazinoids, and cyanogenic glycosides, regardless of plant species. (−)‐Loliolide also triggers the expression of defense‐related genes, accompanied by an increase in the concentration of jasmonic acid and hydrogen peroxide (H2O2). Transcriptome profiling and inhibitor incubation indicate that (−)‐loliolide‐induced defense responses are regulated through pathways mediated by jasmonic acid, H2O2, and Ca 2+.These findings argue that (−)‐loliolide functions as a common belowground signal mediating chemical defense in plants. Such perception‐dependent plant chemical defenses will yield critical insights into belowground signaling interactions. See also the Commentary on this article by Frost, 238: 1749–1751. [ABSTRACT FROM AUTHOR]

Summary: The phytohormones, jasmonates (JAs), mediate many plant developmental processes and their responses to important environmental stresses, such as herbivore attack. Bioactive JAs are perceived by CORONATINE INSENSITIVE (COI)‐receptors, and associated JAZ proteins, to activate downstream responses. To date, the JA receptors of the important monocot crop plant, rice, remain to be explored.Here, we studied all three rice COI proteins, OsCOI1a, OsCOI1b, and OsCOI2, by ligand binding, genome editing, and phenotyping and examining some of the responsible mechanisms for the different responses.OsCOI2 binds to most individual OsJAZs in the presence of endogenous JA ligands, as OsCOI1a /1b do, albeit with greater partner selectivity. Single mutants of each OsCOI and OsCOI1a/1b double mutants were constructed by CRIPSR‐Cas9‐based genome editing and used to phenotype developmental and defense responses. OsCOI1b is involved in root growth and grain‐size control and plays overlapping roles with OsCOI1a in spikelet development, while OsCOI2 regulates leaf senescence, male sterility, root growth, and grain size. All OsCOIs mediated resistance to the devastating rice pest, the brown planthopper. However, the defense sectors regulated by OsCOI1a/1b and OsCOI2 clearly differed.Our results revealed that all three OsCOIs are functional JA receptors that play diverse roles in regulating downstream JA responses. [ABSTRACT FROM AUTHOR]

The fall armyworm (FAW), Spodoptera frugiperda, has become one of the most important pests on corn in China since it invaded in 2019. Although FAW has not been reported to cause widespread damage to rice plants in China, it has been sporadically found feeding in the field. If FAW infests rice in China, the fitness of other insect pests on rice may be influenced. However, how FAW and other insect pests on rice interact remains unknown. In this study, we found that the infestation of FAW larvae on rice plants prolonged the developmental duration of the brown planthopper (BPH, Nilaparvata lugens (Stål)) eggs and plants damaged by gravid BPH females did not induce defenses that influenced the growth of FAW larvae. Moreover, co-infestation by FAW larvae on rice plants did not influence the attractiveness of volatiles emitted from BPH-infested plants to Anagrus nilaparvatae, an egg parasitoid of rice planthoppers. FAW larvae were able to prey on BPH eggs laid on rice plants and grew faster compared to those larvae that lacked available eggs. Studies revealed that the delay in the development of BPH eggs on FAW-infested plants was probably related to the increase in levels of jasmonoyl-isoleucine, abscisic acid and the defensive compounds in the rice leaf sheaths on which BPH eggs were laid. These findings indicate that, if FAW invades rice plants in China, the population density of BPH may be decreased by intraguild predation and induced plant defenses, whereas the population density of FAW may be increased. [ABSTRACT FROM AUTHOR]

Summary: Vitellogenins (Vgs) are critical for the development and fecundity of insects. As such, these essential proteins can be used by plants to reliably sense the presence of insects.We addressed this with a combination of molecular and chemical analyses, genetic transformation, bioactivity tests, and insect performance assays.The small N‐terminal subunit of Vgs of the planthopper Nilaparvata lugens (NlVgN) was found to trigger strong defense responses in rice when it enters the plants during feeding or oviposition by the insect. The defenses induced by NlVgN not only decreased the hatching rate of N. lugens eggs, but also induced volatile emissions in plants, which rendered them attractive to a common egg parasitoid. VgN of other planthoppers triggered the same defenses in rice. We further show that VgN deposited during planthopper feeding compared with during oviposition induces a somewhat different response, probably to target the appropriate developmental stage of the insect.We also confirm that NlVgN is essential for planthopper growth, development, and fecundity. This study demonstrates that VgN in planthopper eggs and saliva acts as a reliable and unavoidable elicitor of plant defenses. Its importance for insect performance precludes evolutionary adaptions to prevent detection by rice plants. [ABSTRACT FROM AUTHOR]

Simple Summary: The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), is a voracious insect pest native to the Western Hemisphere, particularly in South America. The polyphagous fall armyworm feeds on more than 350 plants in such families, including Poaceae, Asteraceae, and Fabaceae. Transgenic plants that express Bacillus thuringiensis proteins (Bt plants) and synthetic insecticides are the main tactics to control Spodoptera frugiperda, although widespread usage of synthetic chemicals has resulted in the emergence of resistance. We assessed cross-resistance, resistance mechanism, and fitness costs based on the life history traits of Spodoptera frugiperda. Results indicated that after 24 generations of selection, the resistance to indoxacarb was increased by 472.67-fold as compared to the Ind-UNSEL. Significantly longer developmental time of larvae extended pupal duration, shorter adult longevity, and lower fecundity were observed in Ind-SEL as compared with the Ind-UNSEL population. Butoxide synergist increased susceptibility to indoxacarb, indicating that P450 enzymes may be involved in indoxacarb resistance. Therefore, it is crucial that we comprehend how insecticides work and how resistance develops in order to develop techniques for managing resistance. These data are valuable to understand the indoxacarb resistance mechanism and provides vital information for scientific-based guidance of pest management decisions. The fall armyworm, Spodoptera frugiperda (J.E. Smith), is a voracious insect pest that is difficult to control due to resistance to insecticides and Bt proteins. We assessed cross-resistance, resistance mechanism, and fitness costs based on the life history traits of S. frugiperda. We established an S. frugiperda strain selected for resistance to indoxacarb (Ind-SEL) from a field-collected population and an unselected strain, Ind-UNSEL. Results indicated that after 24 generations of selection, the resistance to indoxacarb was increased by 472.67-fold as compared to the Ind-UNSEL. There was high cross-resistance to deltamethrin (31.23-fold) with very low or negligible cross-resistance to chlorantraniliprole, emamectin benzoate, and/or methoxyfenozide in the Ind-SEL population. Butoxide synergist increased susceptibility to indoxacarb, indicating that P450 enzymes may be involved in indoxacarb resistance. Significantly longer developmental time of larvae extended pupal duration, shorter adult longevity, and lower fecundity were observed in Ind-SEL as compared with the Ind-UNSEL population. The Net reproductive rate (R0) was the only growth parameter that differs between crosses of Ind-SEL♂ × Ind-UNSEL♀ (176 ± 46) and Ind-SEL♀ × Ind-UNSEL♂ (328 ± 57). On the other hand, all population growth parameters differ between Ind-SEL and Ind-UNSEL strains. Our work contributes to the growing body of research that demonstrates the importance of strain genetics in fitness cost experiments and helps resistance management programs make decisions. [ABSTRACT FROM AUTHOR]

The pathway mediated by jasmonic acid (JA), biosynthesized via 13‐lipoxygenases (LOX), plays a central role in both plant development and defense. In rice, there are at least fourteen 13‐LOXs. Yet, only two 13‐LOXs have been known to be involved in the biosynthesis of JA and plant defenses in rice. Here we cloned a chloroplast‐localized 13‐LOX gene from rice, OsRCI‐1, whose transcripts were upregulated following infestation by brown planthopper (BPH, Nilaparvata lugens), one of the most important pests in rice. Overexpression of OsRCI‐1 (oeRCI lines) increased levels of BPH‐induced JA, jasmonate‐isoleucine, trypsin protease inhibitors and three volatile compounds, 2‐heptanone, 2‐heptanol and α‐thujene. BPHs showed a decreased colonization, fecundity and mass, and developed slowly on oeRCI plants compared with wild‐type (WT) plants. Moreover, BPH‐infested oeRCI plants were more attractive to the egg parasitoid of BPH, Anagrus nilaparvatae than equally treated WT plants. The decreased attractiveness to BPH and enhanced attractiveness to the parasitoid of oeRCI plants correlated with higher levels of BPH‐induced 2‐heptanone and 2‐heptanol, and 2‐heptanone, respectively. Compared with oeRCI plants, WT plants had higher plant height and 1000‐grain weight. These results indicate that OsRCI‐1 is involved in herbivore‐induced JA bursts and plays a role in plant defense and growth. We demonstrate that a chloroplast‐localized 13‐lipoxygenase gene OsRCI‐1 in rice, whose expression is induced by brown planthopper (BPH) infestation, is involved in BPH‐induced JA bursts and plays a role in plant defense and growth. [ABSTRACT FROM AUTHOR]

The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), is a pest of many important crops globally. Effective control is challenging, with the pest exhibiting resistance to different synthetic pesticides across various groups. However, the mechanisms employed by resistant insects for overexpression of relevant detoxification genes remain unclear. The activity of detoxification enzymes was investigated in this study. Additionally, using RNA interference (RNAi), a functional analysis was completed of two P450s genes in an indoxacarb resistant population of fall armyworms. Elevated resistance levels (resistance ratio = 31.37-fold) in indoxacarb-selected populations of FAW were observed after 14 generations. The qRT-PCR showed higher expression of two cytochrome P450 genes, CYP321A7 and CYP6AE43 , in this selected population compared to the control population. RNAi was applied to knock down the P450 ds CYP321A7 and ds CYP6AE43 genes in the FAW larvae. Droplet feeding of the dsRNAs (CYP321A7 and CYP6AE43) via an artificial diet significantly increased mortality rates in the indoxacarb treated population. A shorter larval developmental time of FAW was detected in all dsRNAs-fed larvae. Correspondingly, larval mass was reduced by dsRNAs in indoxacarb resistant populations of fall armyworm. Larval feeding assays demonstrate that dsRNAs targeting, specifically of CYP321A7 and CYP6AE43 enzymes, could be a beneficial technique in the management of indoxacarb resistant populations. Further study on the potential use of dsRNA and its application should be conducted in efforts to counter the development of resistance in FAW against various insecticides in the field. [ABSTRACT FROM AUTHOR]

The phytohormone jasmonic acid (JA) plays a core role in plant defence against herbivores. When attacked by herbivores, JA and its bioactive derivatives are accumulated at the damage site, and subsequently perceived by the jasmonate co‐receptors COI1 and JAZ proteins. The (+)‐7‐iso‐jasmonoyl‐L‐isoleucine (JA‐Ile) is known to be the main active JA derivative controlling vascular plant responses to herbivores as well as other JA‐regulated processes. However, whether other endogenous JA‐amino acid conjugates (JA‐AAs) are involved in herbivore‐induced defence responses remain unknown. Here, we investigated the role of herbivore‐elicited JA‐AAs in the crop plant rice. The levels of five JA‐AAs were significantly increased under the armyworm, leaf folder and brown planthopper attack. Of the elicited JA derivatives, JA‐Ile, JA‐Val and JA‐Leu could serve as ligands to promote the interaction between rice COI1 and JAZs, inducing OsJAZ4 degradation in vivo. JA‐Val or JA‐Leu treatment increased the expression of JA‐ and defence‐related pathway genes but not JA‐Ile levels, suggesting that these JA‐AAs may directly function in JA signalling. Furthermore, the application of JA‐Val or JA‐Leu resulted in JA‐mediated plant growth inhibition, while enhancing plant resistance to herbivore attack. This study uncovers that JA‐Val and JA‐Leu also play a role in rice defence against herbivores. Herbivore‐elicitation increased the accumulation of several JA‐AAs in rice. In addition to JA‐Ile, JA‐Val and JA‐Leu could also bind to rice jasmonate co‐receptors, degrade OsJAZ4 in vivo and inhibit rice root growth. JA‐Val and JA‐Leu treatments resulted in enhancing rice resistance to herbivores. [ABSTRACT FROM AUTHOR]

Applying chemical elicitors is considered a promising approach for controlling pests in the field. Our previous studies have shown that gibberellin (GA) signaling positively regulates the resistance of rice (Oryza sativa) to the brown planthopper (BPH) Nilaparvata lugens (Stål). Yet, whether the exogenous application of GAs can enhance the resistance of rice to BPH remains unknown. Here, we investigated the influence of exogenous GA3 on both defense responses in rice and BPH performance. We found that pretreating rice with GA3 decreased transcript levels of a mitogen-activated protein kinase (MAPK) and three WRKY transcription factors, as well as levels of BPH-elicited jasmonic acid (JA) and three phenolic acids but increased the release of ethylene. Moreover, GA3 treatment negatively affected the survival and development of BPH nymphs as well as the fecundity of BPH female adults. These findings suggest that GA3 promotes the resistance of rice to BPH and may, thus, be used to improve pest management in rice. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]