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Plants typically release large quantities of volatiles in response to herbivory by insects. This benefits the plants by, for instance, attracting the natural enemies of the herbivores. We show that the brown planthopper (BPH) has cleverly turned this around by exploiting herbivore-induced plant volatiles (HIPVs) that provide safe havens for its offspring. BPH females preferentially oviposit on rice plants already infested by the rice striped stem borer (SSB), which are avoided by the egg parasitoid Anagrus nilaparvatae , the most important natural enemy of BPH. Using synthetic versions of volatiles identified from plants infested by BPH and/or SSB, we demonstrate the role of HIPVs in these interactions. Moreover, greenhouse and field cage experiments confirm the adaptiveness of the BPH oviposition strategy, resulting in 80% lower parasitism rates of its eggs. Besides revealing a novel exploitation of HIPVs, these findings may lead to novel control strategies against an exceedingly important rice pest.

Background Mymaridae is an ancient insect group and is a basal lineage of the superfamily Chalcidoidea. Species of Mymaridae have great potential for biological control. Anagrus nilaparvatae , a representative species of Mymaridae, is ideal for controlling rice planthopper due to its high rate of parasitism and ability to find hosts efficiently in paddy ridges and fields. Results Using both PacBio single-molecule real-time and Illumina sequencing, we sequenced and assembled the whole genome of A. nilaparvatae , a first for the family Mymaridae. The assembly consists of 394 scaffolds, totaling 488.8 Mb. The assembly is of high continuity and completeness, indicated by the N50 value of 25.4 Mb and 98.2% mapping rate of Benchmarking Universal Single-Copy Orthologs. In total, 16,894 protein-coding genes in the genome were annotated. A phylogenomic tree constructed for A. nilaparvatae and other 12 species of Hymenoptera confirmed that the family Mymaridae is sister to all remaining chalcidoids. The divergence time between A. nilaparvatae and the other seven Chalcidoidea species was dated at ~ 126.9 Mya. Chemoreceptor and mechanoreceptor genes are important in explaining parasitic behavior. We identified 17 odorant binding proteins, 11 chemosensory proteins, four Niemann-Pick type C2 proteins, 88 olfactory receptors, 12 gustatory receptors, 22 ionotropic receptors and 13 sensory neuron membrane proteins in the genome of A. nilaparvatae , which are associated with the chemosensory functions. Strikingly, there is only one pickpocket receptors and nine transient receptor potential genes in the genome that have a mechanosensory function. Conclusions We obtained a high-quality genome assembly for A. nilaparvatae using PacBio single-molecule real-time sequencing, which provides phylogenomic insights for its evolutionary history. The small numbers of chemo- and mechanosensory genes in A. nilaparvatae indicate the species-specific host detection and oviposition behavior of A. nilaparvatae might be regulated by relatively simple molecular pathways.

Pseudoligosita yasumatsui and Anagrus nilaparvatae are both egg parasitoids of the brown planthopper, Nilaparvata lugens (Stål) (BPH). In this study, we obtained a stable strain of P. yasumatsui reproduced via thelytoky through indoor rearing and screening. We assessed the parasitism capacity of this strain on eggs of N. lugens by comparing the parasitism preference and circadian rhythm of this strain to that of A. nilaparvatae, which is proved as the dominant egg parasitoid species of BPH in rice fields. The findings indicated that both egg parasitoids could parasitize fertilized and unfertilized BPH eggs, however, with a significant preference for fertilized eggs. The daily parasitization volume of P. yasumatsui was slightly higher than that of A. nilaparvatae. Both egg parasitoids preferred parasitizing 1–3-day-old BPH eggs, but the parasitism amount of 5–6-day-old BPH eggs by P. yasumatsui is higher than that by A. nilaparvatae. The parasitism events of both species of egg parasitoid wasps occurred primarily from 7:00–15:00 and the parasitism amount at night accounted for less than 15% of the total amount. The results indicate that this strain of P. yasumatsui reproduced via thelytoky could be valuable for rice planthopper control.

This study reports the first complete mitochondrial genomes of three egg parasitoid wasps parasitizing Nilaparvata lugens—Pseudoligosita nephotetticum, Anagrus frequens, and Anagrus nilaparvatae. Genome sizes ranged from 15,429 to 15,889 bp, with all three mitogenomes displaying strong A + T bias, standard gene content, and characteristic strand asymmetries. While A. frequens and A. nilaparvatae exhibited conserved gene orders, extensive gene rearrangements, including multiple inversions in both protein-coding genes (PCGs) and tRNAs, were observed in P. nephotetticum. Codon usage analyses revealed a preference for codons ending in A or U. The non-synonymous (Ka) to synonymous (Ks) substitution ratio analysis identified signs of positive selection in multiple PCGs, particularly in atp8, nad6, and nad3, suggesting possible adaptive evolution related to host-searching behavior. Secondary structure analyses showed the loss of trnL1 in all Anagrus species, while trnS1 and trnR lacked the DHU arm, indicating possible derived traits in Mymaridae. Phylogenetic analysis was the first time to describe the relationship of the genus Anagrus within Mymaridae from the perspective of 13 protein genes. Furthermore, the grouping of (Pseudoligosita + Megaphragma) + Trichogramma was supporting the distinct evolutionary lineage of Pseudoligosita. This work provides new molecular resources and phylogenetic insight for Chalcidoidea, with implications for parasitoid evolution and biological control strategies.

A common rice pest can avoid its natural parasite by settling on plants that smell like they have been damaged by a species of caterpillar.A common rice pest can avoid its natural parasite by settling on plants that smell like they have been damaged by a species of caterpillar.

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.

Anagrus nilaparvatae is an important egg parasitoid wasp of pests such as the rice planthopper. Based on the powerful olfactory system of sensing chemical information in nature, A. nilaparvatae shows complicated life activities and behaviors, such as feeding, mating, and hosting. We constructed a full‐length transcriptome library and used this to identify the characteristics of soluble chemical communication proteins. Through full‐length transcriptome sequencing, splicing, assembly, and data correction by Illumina, we obtained 163.59 Mb of transcriptome data and 501,179 items with annotation information. We then performed Gene Ontology (GO) functional classification of the transcriptome's unigenes. We analyzed the sequence characteristics of soluble chemical communication protein genes and identified eight genes: AnilOBP2, AnilOBP9, AnilOBP23, AnilOBP56, AnilOBP83, AnilCSP5, AnilCSP6, and AnilNPC2. After sequence alignment and conserved domain prediction, the eight proteins encoded by the eight genes above were found to be consistent with the typical characteristics of odorant‐binding proteins (OBPs), chemosensory proteins (CSPs), and Niemann‐pick type C2 proteins (NPC2s) in other insects. Phylogenetic tree analysis showed that the eight genes share low homology with other species of Hymenoptera. Quantitative real‐time polymerase chain reaction (RT‐qPCR) was used to analyze the expression responses of the eight genes in different sexes and upon stimulation by volatile organic compounds. The relative expression levels of AnilOBP9, AnilOBP26, AnilOBP83, AnilCSP5, and AnilNPC2 in males were significantly higher than those in females, while the relative expression level of AnilCSP6 was higher in females. The expression levels of AnilOBP9 and AnilCSP6 were significantly altered by the stimulation of β‐caryophyllene, suggesting that these two genes may be related to host detection. This study provides the first data for A. nilaparvatae's transcriptome and the molecular characteristics of soluble chemical communication proteins, as well as an opportunity for understanding how A. nilaparvatae behaviors are mediated via soluble chemical communication proteins. The structure predicted of 5 AnilOBPs and 2 AnilCSPs are spherical structures formed by α‐helices, and AnilNPC2 are spherical structures formed by β‐folded.

Synthetic chemical elicitors of plant defense have been touted as a powerful means for sustainable crop protection. Yet, they have never been successfully applied to control insect pests in the field. We developed a high-throughput chemical genetics screening system based on a herbivore-induced linalool synthase promoter fused to a β-glucuronidase (GUS) reporter construct to test synthetic compounds for their potential to induce rice defenses. We identified 2,4-dichlorophenoxyacetic acid (2,4-D), an auxin homolog and widely used herbicide in monocotyledonous crops, as a potent elicitor of rice defenses. Low doses of 2,4-D induced a strong defensive reaction upstream of the jasmonic acid and ethylene pathways, resulting in a marked increase in trypsin proteinase inhibitor activity and volatile production. Induced plants were more resistant to the striped stem borer Chilo suppressalis, but became highly attractive to the brown planthopper Nilaparvata lugens and its main egg parasitoid Anagrus nilaparvatae. In a field experiment, 2,4-D application turned rice plants into living traps for N. lugens by attracting parasitoids. Our findings demonstrate the potential of auxin homologs as defensive signals and show the potential of the herbicide to turn rice into a selective catch crop for an economically important pest.

Jasmonate signaling pathway plays an important role in induced plant defense against herbivores and pathogens, including the emission of volatiles that serve as attractants for natural enemies of herbivores. We studied the volatiles emitted from rice plants that were wounded and treated with jasmonic acid (JA) and their effects on the host-searching behavior of the rice brown planthopper, Nilaparvata lugens (Stangstroml), and its mymarid egg parasitoid Anagrus nilaparvatae Pang et Wang. Female adults of N. lugens significantly preferred to settle on JA-treated rice plants immediately after release. The parasitoid A. nilaparvatae showed a similar preference and was more attracted to the volatiles emitted from JA-treated rice plants than to volatiles from control plants. This was also evident from greenhouse and field experiments in which parasitism of N. lugens eggs by A. nilaparvatae on plants that were surrounded by JA-treated plants was more than twofold higher than on control plants. Analyses of volatiles collected from rice plants showed that JA treatment dramatically increased the release of volatiles, which included aliphatic aldehydes and alcohols, monoterpenes, sesquiterpenes, methyl salicylate, n-heptadecane, and several as yet unidentified compounds. These results confirm an involvement of the JA pathway in induced defense in rice plants and demonstrate that the egg parasitoid A. nilaparvatae exploits plant-provided cues to locate hosts. We explain the use of induced plant volatiles by the egg parasitoid by a reliable association between planthopper feeding damage and egg presence.

In order to clarify the impacts of southern rice black-streaked dwarf virus (SRBSDV) infection on rice plants, rice planthoppers and natural enemies, differences in nutrients and volatile secondary metabolites between infected and healthy rice plants were examined. Furthermore, the impacts of virus-mediated changes in plants on the population growth of non-vector brown planthopper (BPH), Nilaparvata lugens, and the selectivity and parasitic capability of planthopper egg parasitoid Anagrus nilaparvatae were studied. The results showed that rice plants had no significant changes in amino acid and soluble sugar contents after SRBSDV infection, and SRBSDV-infected plants had no significant effect on population growth of non-vector BPH. A. nilaparvatae preferred BPH eggs both in infected and healthy rice plants, and tended to parasitize eggs on infected plants, but it had no significant preference for infected plants or healthy plants. GC-MS analysis showed that tridecylic aldehyde occurred only in rice plants infected with SRBSDV, whereas octanal, undecane, methyl salicylate and hexadecane occurred only in healthy rice plants. However, in tests of behavioral responses to these five volatile substances using a Y-tube olfactometer, A. nilaparvatae did not show obvious selectivity between single volatile substances at different concentrations and liquid paraffin in the control group. The parasitic capability of A. nilaparvatae did not differ between SRBSDV-infected plants and healthy plant seedlings. The results suggested that SRBSDV-infected plants have no significant impacts on the non-vector planthopper and its egg parasitoid, A. nilaparvatae.