The genomic history and global migration of a windborne pest.

Many insect pests, including the brown planthopper (BPH), undergo windborne migration that is challenging to observe and track. It remains controversial about their migration patterns and largely unknown regarding the underlying genetic basis. By analyzing 360 whole genomes from around the globe, we clarify the genetic sources of worldwide BPHs and illuminate a landscape of BPH migration showing that East Asian populations perform closed-circuit journeys between Indochina and the Far East, while populations of Malay Archipelago and South Asia undergo one-way migration to Indochina. We further find round-trip migration accelerates population differentiation, with highly diverged regions enriching in a gene desert chromosome that is simultaneously the speciation hotspot between BPH and related species. This study not only shows the power of applying genomic approaches to demystify the migration in windborne migrants but also enhances our understanding of how seasonal movements affect speciation and evolution in insects.

Knocking down a DNA demethylase gene affects potato plant defense against a specialist insect herbivore.

DNA demethylase (DML) is involved in plant development and responses to biotic and abiotic stresses; however, its role in plant-herbivore interaction remains elusive. Here, we found that herbivory by the potato tuber moth, Phthorimaea operculella, rapidly induced the genome-wide DNA methylation and accumulation of DML gene transcripts in potato plants. Herbivory induction of DML transcripts was suppressed in jasmonate-deficient plants, whereas exogenous application of methyl jasmonate (MeJA) improved DML transcripts, indicating that the induction of DML transcripts by herbivory is associated with jasmonate signaling. Moreover, P. operculella larvae grew heavier on DML gene (StDML2) knockdown plants than on wild-type plants, and the decreased biosynthesis of jasmonates in the former may be responsible for this difference, since the larvae feeding on these two genotypes supplemented with MeJA showed similar growth. In addition, P. operculella adult moths preferred to oviposit on StDML2 knockdown plants than on wild-type plants, which was associated with the reduced emission of ß-caryophyllene in the former. In addition, supplementing ß-caryophyllene to these two genotypes further disrupted moths' oviposit choice preference for them. Interestingly, in StDML2 knockdown plants, hypermethylation was found at the promoter regions for the key genes StAOS and StAOC in the jasmonate biosynthetic pathway, as well as for the key gene StTPS12 in ß-caryophyllene production. Our findings suggest that knocking down StDML2 can affect herbivore defense via jasmonate signaling and defense compound production in potato plants.

Megalurothrips usitatus Directly Causes the Black-Heads and Black-Tail Symptoms of Cowpea along with the Production of Insect-Resistance Flavonoids.

The thrip (Megalurothrips usitatus) damages the flowers and pods of the cowpea, causing "black-heads and black-tails" (BHBT) symptoms and negatively affecting its economic value. However, the mechanism by which BHBT symptoms develop is still unknown. Our results showed that the microstructure of the pod epidermis was altered and the content of the plant's resistance-related compounds increased after a thrip infestation. However, the contents of protein and free amino acids did not change significantly, suggesting that the nutritional value was not altered. Pathogens were found not to be involved in the formation of BHBT symptoms, as fungi and pathogenic bacteria were not enriched in damaged pods. Two herbivory-induced flavonoids-7,4'-dihydroxyflavone and coumestrol-were found to exert insecticidal activity. Our study clarified that BHBT symptoms are directly caused by the thrip. Thresholds for pest control need to be reconsidered as thrip herbivory did not degrade cowpea nutrition.

The Alternaria alternata StuA transcription factor interacting with the pH-responsive regulator PacC for the biosynthesis of host-selective toxin and virulence in citrus.

IMPORTANCE: In this study, we used Alternaria alternata as a biological model to report the role of StuA in phytopathogenic fungi. Our findings indicated that StuA is required for Alternaria citri toxin (ACT) biosynthesis and fungal virulence. In addition, StuA physically interacts with PacC. Disruption of stuA or pacC led to decreased expression of seven toxin biosynthetic genes (ACCT) and toxin production. PacC could recognize and bind to the promoter regions of ACTT6 and ACTTR. Our results revealed a previously unrecognized (StuA-PacC)→ACTTR module for the biosynthesis of ACT in A. alternata, which also provides a framework for the study of StuA in other fungi.

Agricultural diversification promotes sustainable and resilient global rice production.

Rice is a staple food for half of the human population, but the effects of diversification on yields, economy, biodiversity and ecosystem services have not been synthesized. Here we quantify diversification effects on environmental and socio-economic aspects of global rice production. We performed a second-order meta-analysis based on 25 first-order meta-analyses covering four decades of research, showing that diversification can maintain soil fertility, nutrient cycling, carbon sequestration and yield. We used three individual first-order meta-analyses based on 39 articles to close major research gaps on the effects of diversification on economy, biodiversity and pest control, showing that agricultural diversification can increase biodiversity by 40%, improve economy by 26% and reduce crop damage by 31%. Trade-off analysis showed that agricultural diversification in rice production promotes win-win scenarios between yield and other ecosystem services in 81% of all cases. Knowledge gaps remain in understanding the spatial and temporal effects of specific diversification practices and trade-offs.

Identification and transcriptional profiling of UV-A-responsive genes in Bemisia tabaci.

Ultraviolet-A (UV-A) radiation directly impacts the growth and spread of Bemisia tabaci. However, the mechanistic pathways of this phenomenon remain unknown. We analyzed B. tabaci transcriptome data after exposure to UV-A radiation for 6 h. The 453 genes were identified whose expression were significantly altered in response to the stress induced by UV-A irradiation. Forty genes were up-regulated, while 413 genes were down-regulated. Enrichment analysis using GO, KEGG, and Genomes databases revealed that the DEGs play key roles in antioxidation and detoxification, protein turnover, metabolic, developmental processes, and immunological response. Among the gene families involved in detoxification, shock, and development, down-regulated DEGs in transcriptional factor gene families were significantly greater than those up-regulated DEGs. Our findings demonstrated that exposure to UV-A stress can suppress immunity and affect the growth and biological parameters of B. tabaci by altering gene regulation. These results suggest a potential utility of UV-A stress in managing B. tabaci under greenhouse conditions.

Formation of 8-hydroxylinalool in tea plant Camellia sinensis var. Assamica 'Hainan dayezhong'.

Linalool and its derivatives contribute greatly to tea aroma. Here, 8-hydroxylinalool was found to be one of the major linalool-derived aroma compounds in Camellia sinensis var. assamica 'Hainan dayezhong', a tea plant grown in Hainan Province, China. Both (Z)-8-hydroxylinalool and (E)-8-hydroxylinalool were detected, and the E type was the main compound. Its content fluctuated in different months and was the highest in the buds compared with other tissues. CsCYP76B1 and CsCYP76T1, located in the endoplasmic reticulum, were identified to catalyze the formation of 8-hydroxylinalool from linalool in the tea plant. During withering of black tea manufacturing, the content of both (Z)-8-hydroxylinalool and (E)-8-hydroxylinalool significantly increased. Further study suggested that jasmonate induced gene expression of CsCYP76B1 and CsCYP76T1, and the accumulated precursor linalool may also contribute to 8-hydroxylinalool accumulation. Thus, this study not only reveals 8-hydroxylinalool biosynthesis in tea plants but also sheds light on aroma formation in black tea.

The microRNA pathway core genes are indispensable for development and reproduction in the brown planthopper, Nilaparvata lugens.

MicroRNAs (miRNAs) are small single-stranded non-coding RNAs involved in a variety of cellular events by regulating gene expression at the post-transcriptional level. Several core genes in miRNA biogenesis have been reported to participate in a wide range of physiological events, in some insect species. However, the functional significance of miRNA pathway core genes in Nilaparvata lugens remains unknown. In the present study, we conducted a systematic characterisation of five core genes involved in miRNA biogenesis. We first performed spatiotemporal expression analysis and found that miRNA core genes exhibited similar expression patterns, with high expression levels in eggs and relatively high transcriptional levels in the ovaries and fat bodies of females. RNA interference experiments showed that injecting third-instar nymphs with dsRNAs targeting the miRNA core genes, NlAgo1, NlDicer1, and NlDrosha resulted in high mortality rates and various degrees of body melanism, moulting defects, and wing deformities. Further investigations revealed that the suppression of miRNA core genes severely impaired ovarian development and oocyte maturation, resulting in significantly reduced fecundity and disruption of intercellular spaces between follicle cells. Moreover, the expression profiles of miR-34-5p, miR-275-3p, miR-317-3p, miR-14, Let-7-1, and miR-2a-3p were significantly altered in response to the knockdown of miRNA core genes mixture, suggesting that they play essential roles in regulating miRNA-mediated gene expression. Therefore, our results provide a solid theoretical basis for the miRNA pathway in N. lugens and suggest that the NlAgo1, NlDicer1, and NlDrosha-dependent miRNA core genes are essential for the development and reproduction of this agricultural pest.

Alkaline ceramidase (ClAC) inhibition enhances heat stress response in Cyrtorhinus lividipennis (Reuter).

Ceramidases (CDases) are vital sphingolipid enzymes involved in organismal growth and development. They have been reported as key mediators of thermal stress response. However, whether and how CDase responds to heat stress in insects remain unclear. Herein, we identified two CDase genes, C. lividipennis alkaline ceramidase (ClAC) and neutral ceramidase (ClNC), by searching the transcriptome and genome databases of the mirid bug, Cyrtorhinus lividipennis, an important natural predator of planthoppers. Quantitative PCR (qPCR) analysis showed that both ClNC and ClAC were highly expressed in nymphs than in adults. ClAC was especially highly expressed in the head, thorax, and legs, while ClNC was widely expressed in the tested organs. Only the ClAC transcription was significantly affected by heat stress. Knocking down ClAC increased the C. lividipennis nymph survival rate under heat stress. The transcriptome and lipidomics data showed that the RNA interference-mediated suppression of ClAC significantly upregulated the transcription level of catalase (CAT) and the content of long-chain base ceramides, including C16-, C18-, C24-, and C31- ceramides. In C. lividipennis nymphs, ClAC played an important role in heat stress response, and the upregulation of nymph survival rate might be caused by variation in the ceramide levels and transcriptional changes in CDase downstream genes. This study improves our understanding of the physiological functions of insect CDase under heat stress and provides valuable insights into the nature enemy application.

Tissue-specific regulation of volatile emissions moves predators from flowers to attacked leaves.

Plant-predator mutualisms have been widely described in nature.1,2 How plants fine-tune their mutualistic interactions with the predators they recruit remains poorly understood. In the wild potato (Solanum kurtzianum), predatory mites, Neoseiulus californicus, are recruited to flowers of undamaged plants but rapidly move downward when the herbivorous mites, Tetranychus urticae, damage leaves. This "up-down" movement within the plant corresponds to the shift of N. californicus from palynivory to carnivory, as they change from feeding on pollen to herbivores when moving between different plant organs. This up-down movement of N. californicus is mediated by the organ-specific emissions of volatile organic compounds (VOCs) in flowers and herbivory-elicited leaves. Experiments with exogenous applications, biosynthetic inhibitors, and transient RNAi revealed that salicylic acid and jasmonic acid signaling in flowers and leaves mediates both the changes in VOC emissions and the up-down movement of N. californicus. This alternating communication between flowers and leaves mediated by organ-specific VOC emissions was also found in a cultivated variety of potato, suggesting the agronomic potential of using flowers as reservoirs of natural enemies in the control of potato pests.

Understanding of formation and change of chiral aroma compounds from tea leaf to tea cup provides essential information for tea quality improvement.

Abundant secondary metabolites endow tea with unique quality characteristics, among which aroma is the core component of tea quality. The ratio of chiral isomers of aroma compounds greatly affects the flavor of tea leaves. In this paper, we review the progress of research on chiral aroma compounds in tea. With the well-established GC-MS methods, the formation of, and changes in, the chiral configuration of tea aroma compounds during the whole cycle of tea leaves from the plant to the tea cup has been studied in detail. The ratio of aroma chiral isomers varies among different tea varieties and finished teas. Enzymatic reactions involving tea aroma synthases and glycoside hydrolases participate the formation of aroma compound chiral isomers during tea tree growth and tea processing. Non-enzymatic reactions including environmental factors such as high temperature and microbial fermentation involve in the change of aroma compound chiral isomers during tea processing and storage. In the future, it will be interesting to determine how changes in the proportions of chiral isomers of aroma compounds affect the environmental adaptability of tea trees; and to determine how to improve tea flavor by modifying processing methods or targeting specific genes to alter the ratio of chiral isomers of aroma compounds.

Silver and copper-oxide nanoparticles prepared with GA3 induced defense in rice plants and caused mortalities to the brown planthopper, Nilaparvata lugens (Stål).

BACKGROUND: Nanoparticles have been employed as nanopesticides for pest control in agriculture. However, the harmful effects of their chemical synthesis on human and environmental health have resulted in increased use of green synthetic approaches, including the use of plant extracts. The brown planthopper, Nilaparvata lugens (Stål) (BPH), is a severe pest of rice plants (Oryza sativa L.), especially in Asia. It is usually controlled chemically but has developed resistance against many insecticides. RESULTS: In this study, we synthesized metallic silver (Ag-NPs) and copper-oxide (CuO-NPs) nanoparticles using the exogenous phytohormone, gibberellic acid (GA3), as a reducing agent. We then sprayed them separately on rice plants and BPH together and evaluated their effects on the plants and insects. SEM and TEM images showed that the synthesis was successful, indicated by the sizes (25-60 nm), uniform shape and spherical and cubical structures of Ag-NPs, as well as by the rugby sheet-like of CuO-NPs with lateral sizes of 150-340 nm and thickness of 30-70 nm. Independent applications of the nanoparticles and GA3 on rice plants induced different volatile profiles, of which the highest number emitted was under Ag-NPs, including the highest emission of linalool. Transcriptome analysis showed that Ag-NPs-treated rice plants showed different transcriptome profiles compared to the control, 24 h after treatment, including the upregulation of the linalool synthase gene, genes of plants transcription factors such as WRKY, bHLH and NAC and other genes involved in plant defense responses. In all treatments, the mortality rate of BPH increased with an increase in NPs concentrations over time but was prominent under Ag-NPs treatment. The LC50 values for Ag-NPs and CuO-NPs decreased with an increase in time. Also, the nanoparticles increased the activities of protective enzymes (POD, SOD and CAT), inhibited that of detoxification enzymes (A-CHE, ACP and AKP), and reduced total protein concentrations in the BPH. CONCLUSIONS: These results show that synthesizing nanoparticles using phytohormones may be a safer and environmentally friendly option, which also holds promise for controlling the BPH in rice production.

Corrigendum: Identification and functional characterization of two putative pheromone receptors in the potato tuber moth, Phthorimaea operculella.

[This corrects the article DOI: 10.3389/fphys.2020.618983.].

Heat stress affects potato's volatile emissions that mediate agronomically important trophic interactions.

Potato, a cool-weather crop, emits volatile organic compounds (VOCs) which attract the specialist herbivore, Phthorimaea operculella, but also this herbivore's parasitic wasp, Trichogramma chilonis, an important biocontrol agent. What happens to this trophic system when heat stress challenges this agro-ecosystem? We studied how high temperature (HT) pre-treatments influence potato's VOC emissions and their subsequent effects on the preferences of insects, as evaluated in oviposition assays and Y-tube olfactometers. HT pre-stressed plants were less attractive to P. operculella adult moths, which were repelled by HT VOCs, but increased the recruitment of the parasitoid, T. chilonis, which were attracted. VOC emissions, including the most abundant constituent, ß-caryophyllene, were enhanced by HT treatments; some constituents elicited stronger behavioural responses than others. Transcripts of many genes in the biosynthetic pathways of these VOCs were significantly enhanced by HT treatment, suggesting increases in de novo biosynthesis. HT increased the plant's stomatal apertures, and exogenous applications of the hormone, ABA, known to suppress stomatal apertures, reduced leaf volatile emissions and affected the HT-altered plant attractions to both insects. From these results, we infer that HT stress affects this plant-insect interaction through its influence on VOC emissions, potentially decreasing herbivore ovipositions while increasing ovipositions of the parasitoid.

Characterization of MicroRNAs Associated with Reproduction in the Brown Planthopper, Nilaparvata lugens.

Insects have a robust capacity to produce offspring for propagation, and the reproductive events of female insects have been achieved at the molecular and physiological levels via regulatory gene pathways. However, the roles of MicroRNAs (miRNAs) in the reproductive development of the brown planthopper (BPH), Nilaparvata lugens, remain largely unexplored. To understand the roles of miRNAs in reproductive development, miRNAs were identified by Solexa sequencing in short-winged (SW) female adults of BPH. Small RNA libraries derived from three developmental phases (1 day, 3 days, and 5 days after emergence) were constructed and sequenced. We identified 905 miRNAs, including 263 known and 642 novel miRNAs. Among them, a total of 43 miRNAs were differentially expressed in the three developmental phases, and 14,568 putative targets for 43 differentially expressed miRNAs (DEMs) were predicted by TargetScan and miRanda. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis of the predicted miRNA targets illustrated the putative roles for these DEMs in reproduction. The progress events were annotated, including oogenesis, lipid biosynthetic process, and related pathways such as apoptosis, ABC transporters, and amino acid metabolism. Four highly abundant DEMs (miR-9a-5p, miR-34-5p, miR-275-3p, and miR-317-3p) were further screened, and miR-34-5p was confirmed to be involved in the regulation of reproduction. Overexpression of miR-34-5p via injecting its mimics reduced fecundity and decreased Vg expression. Moreover, target genes prediction for miR-34-5p showed they might be involved in 20E signaling cascades, apoptosis, and gonadal development, including hormone receptor 4 (HR4), caspase-1 (Cp-1), and spermatogenesis-associated protein 20 (SPATA20). These findings provide a valuable resource for future studies on the role of miRNAs in BPH reproductive development.

CRISPR screening uncovers a central requirement for HHEX in pancreatic lineage commitment and plasticity restriction.

The pancreas and liver arise from a common pool of progenitors. However, the underlying mechanisms that drive their lineage diversification from the foregut endoderm are not fully understood. To tackle this question, we undertook a multifactorial approach that integrated human pluripotent-stem-cell-guided differentiation, genome-scale CRISPR-Cas9 screening, single-cell analysis, genomics and proteomics. We discovered that HHEX, a transcription factor (TF) widely recognized as a key regulator of liver development, acts as a gatekeeper of pancreatic lineage specification. HHEX deletion impaired pancreatic commitment and unleashed an unexpected degree of cellular plasticity towards the liver and duodenum fates. Mechanistically, HHEX cooperates with the pioneer TFs FOXA1, FOXA2 and GATA4, shared by both pancreas and liver differentiation programmes, to promote pancreas commitment, and this cooperation restrains the shared TFs from activating alternative lineages. These findings provide a generalizable model for how gatekeeper TFs like HHEX orchestrate lineage commitment and plasticity restriction in broad developmental contexts.

Disentangling the Potato Tuber Moth-Induced Early-Defense Response by Simulated Herbivory in Potato Plants.

Plants rely on the perception of a multitude of herbivory-associated cues (HACs) to activate their defense response to insect herbivores. These stimuli are mainly derived from three functional components, namely, mechanical damage, insect-associated microbe, and insect's chemical cues. While simulated herbivory integrating these stimuli is widely exploited for complementing actual herbivory in clarifying the details of plant-herbivore interaction, breaking down these stimuli and identifying the mechanisms of plant responses associated with them have been less explored. In this study, the components of potato tuber moth (Phthorimaea operculella, PTM) herbivory were reorganized in a cumulative way and their impacts on the early defense responses of potato leaf were characterized. We found that simulated and actual herbivory of PTM triggered similar patterns of phytohormonal and transcriptomic responses in potato leaf. Moreover, the microbe in the PTM herbivory stimuli is associated with the regulation of the phytohormones jasmonic acid (JA) and abscisic acid (ABA) since reducing the microbe in HAC could reduce JA while increasing ABA. In addition, seven robust gene modules were identified to illustrate how potato plants respond to different PTM herbivory stimuli when herbivory components increased. Significantly, we found that mechanical damage mainly activated JA-mediated signaling; PTM-derived HACs contributed much more to potato early-defense response and induced signaling molecules such as multiple protein kinases; orally secreted bacteria stimuli could antagonize PTM-derived HACs and modulate plant defense, including repressing phenylpropanoid biosynthesis. Our study broadened the understanding of how potato plants integrate the responses to a multitude of stimuli upon PTM herbivory and evidenced that insect-associated microbes greatly modulated the plants response to insect herbivory.

The phyllosphere microbiome shifts toward combating melanose pathogen.

BACKGROUND: Plants can recruit beneficial microbes to enhance their ability to defend against pathogens. However, in contrast to the intensively studied roles of the rhizosphere microbiome in suppressing plant pathogens, the collective community-level change and effect of the phyllosphere microbiome in response to pathogen invasion remains largely elusive. RESULTS: Here, we integrated 16S metabarcoding, shotgun metagenomics and culture-dependent methods to systematically investigate the changes in phyllosphere microbiome between infected and uninfected citrus leaves by Diaporthe citri, a fungal pathogen causing melanose disease worldwide. Multiple microbiome features suggested a shift in phyllosphere microbiome upon D. citri infection, highlighted by the marked reduction of community evenness, the emergence of large numbers of new microbes, and the intense microbial network. We also identified the microbiome features from functional perspectives in infected leaves, such as enriched microbial functions for iron competition and potential antifungal traits, and enriched microbes with beneficial genomic characteristics. Glasshouse experiments demonstrated that several bacteria associated with the microbiome shift could positively affect plant performance under D. citri challenge, with reductions in disease index ranging from 65.7 to 88.4%. Among them, Pantoea asv90 and Methylobacterium asv41 identified as "recruited new microbes" in the infected leaves, exhibited antagonistic activities to D. citri both in vitro and in vivo, including inhibition of spore germination and/or mycelium growth. Sphingomonas spp. presented beneficial genomic characteristics and were found to be the main contributor for the functional enrichment of iron complex outer membrane receptor protein in the infected leaves. Moreover, Sphingomonas asv20 showed a stronger suppression ability against D. citri in iron-deficient conditions than iron-sufficient conditions, suggesting a role of iron competition during their antagonistic action. CONCLUSIONS: Overall, our study revealed how phyllosphere microbiomes differed between infected and uninfected citrus leaves by melanose pathogen, and identified potential mechanisms for how the observed microbiome shift might have helped plants cope with pathogen pressure. Our findings provide novel insights into understanding the roles of phyllosphere microbiome responses during pathogen challenge. Video abstract.

Knockdown of sphingomyelinase (NlSMase) causes ovarian malformation of brown planthopper, Nilaparvata lugens (Stål).

Sphingomyelinases (SMases) are a group of enzymes that catalyse the hydrolysis of sphingomyelins into ceramides and phosphorylcholine. They have been intensively investigated for their pathophysiological roles in mammals whereas much remains unclear about their counterparts in insects. Herein we report the cloning and functional characterization of four SMase homologue genes, designated NlSMase1-4, from brown planthopper (BPH). The phylogenetic analysis revealed that NlSMase1 and NlSMase2 were clustered into acid SMase family, and NlSMase3 and NlSMase4 with neutral SMase family. NlSMase1, NlSMase3 and NlSMase4 were highly expressed in BPH females, and NlSMaes2 in the 5th instar nymph. All four NlSMases had the lowest transcription in BPH males. NlSMase1 and NlSMase4 were highly expressed in BPH ovaries, while NlSMase2 and NlSMase3 in midgut and wings, respectively. Knocking-down of each NlSMase individual by RNA interference (RNAi) caused the ovarian malformation in BPH. The transcriptomic analysis revealed that NlSMase4 knockdown could strongly affect diacylglycerol (DAG)-related metabolisms and their downstream pathways. Further, qRT-PCR analysis of vitellogenin (Vg) genes indicates that the DAG metabolism disorder could interrupt the essential Vg accumulation for BPH oogenesis. Our study demonstrates the vital role of NlSMases in BPH reproductive development and provides new insights into the mediated mechanism of how SMases function.

Chromosome-level genome assembly of the mirid predator Cyrtorhinus lividipennis Reuter (Hemiptera: Miridae), an important natural enemy in the rice ecosystem.

Though the genomes of many rice herbivorous pests have recently been well characterized, little is known about the genome of their natural enemies. Here, by using the Illumina and PacBio platforms, we sequenced and assembled the whole genome of the mirid species Cyrtorhinus lividipennis Reuter (Hemiptera: Miridae), which is an economically and ecologically important natural enemy in the rice ecosystem acting as a dominant predator for planthoppers and leafhoppers in the field. Through Hi-C scaffolding, 1615 scaffolds with a total size of 338.08 Mb were successfully anchored onto 13 chromosomes. The assembled genome size was 345.75 Mb with a final scaffold N50 of 27.58 Mb. Approximately 107.51 Mb of sequences accounting for 31.10% of the genome were identified as repeat elements, and 14,644 protein-coding genes were annotated. Phylogenetic analysis showed that C. lividipennis clustered with other Hemipteran species and diverged from Apolygus lucorum about 66.7 million years ago. Gene families related to detoxification, environmental adaptation and digestion were analysed comparatively with other Hemipteran species, but no significant expansion or contraction was found in C. lividipennis. We also observed male meiosis in C. lividipennis, which showed a typical post-reduction of sex chromosomes and a karyotype of 2n = 22 + XY. As the first natural-enemy genome in the rice ecosystem, the genomic resource of C. lividipennis not only expands our understanding of the multitrophic interactions (host plant-prey-predator), but also provides a genomic basis for better understanding this dominant predator and therefore promotes sustainable rice pest management and food grain production.