Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway.

Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in plants, betasatellite-encoded ßC1 proteins interfere with SA signaling and reduce the activation of antiviral resistance. ßC1 inhibits SA-induced degradation of NbNPR3 (Nicotiana benthamiana nonexpressor of pathogenesis-related genes 3), a negative regulator of SA signaling. ßC1 does not bind directly to NbNPR3, but regulates NbNPR3 degradation via heat shock protein 90s (NbHSP90s). NbHSP90s bind to both NbNPR3 and ßC1 and suppress SA signaling. This viral success strategy appears to be conserved as it is also documented for viral proteins encoded by two aphid-borne viruses. Our findings reveal an exquisite mechanism that facilitates the persistence of vector-borne plant viruses and provide important insights into the intricacies of the virus life cycle.

Using salicylic acid-responsive promoters to drive the expression of jasmonic acid-regulated genes enhances plant resistance to whiteflies.

BACKGROUND: Jasmonic acid (JA) is an important phytohormone used to defend against herbivores, but it does not respond to whitefly feeding. Conversely, another phytohormone, salicylic acid (SA), is induced when plants are fed upon by whiteflies. JA has a better anti-whitefly effect than SA; however, there is limited research on how to effectively improve plant resistance by utilizing the different responses of these phytohormones to whitefly feeding. RESULTS: We discovered that protease inhibitors 8 (PI8) and terpene synthase 10 (TPS10) located downstream of the JA-regulated pathway in plants have anti-whitefly effects, but these two genes were not induced by whitefly feeding. To identify whitefly-inducible promoters, we compared the transcriptome data of tobacco fed upon by Bemisia tabaci with the control. We focused on pathogenesis-related (PR) genes because they are known to be induced by SA. Among these PR genes, we found that expression levels of pathogenes-related protein 1C-like (PR1) and glucose endo-1,3-beta-glucosidase (BGL) can be significantly induced by whitefly feeding and regulated by SA. We then engineered the whitefly-inducible promoters of BGL and PR1 to drive the expression of PI8 and TPS10. We found that compared with control plants that did not induce the expression of PI8 or TPS10, transformed plants expressing PI8 or TPS10 under the PR1 or BGL promoter showed a significant increase in the expression levels of PI8 and TPS10 after whitefly infection, significantly improving their resistance to whiteflies. CONCLUSION: Our findings suggest that using SA-inducible promoters as tools to drive the expression of JA-regulated defense genes can enhance plant resistance to whiteflies. Our study provides a novel pathway for the enhancement of plant resistance against insects. © 2024 Society of Chemical Industry.

Attraction of Nicotiana benthamiana to Bemisia tabaci is related to a chemical signal in plant volatile, undecane.

BACKGROUND: The whitefly Bemisia tabaci is one of the world's foremost agricultural pests. Recently, we found that a wild relative of tobacco (Nicotiana benthamiana) demonstrates remarkable attractiveness and nearly 100% lethality towards whiteflies. Therefore, it can act as a dead-end trap crop for whitefly control in the field. However, the underlying mechanism of the significant attractiveness of N. benthamiana towards whiteflies is unclear. RESULTS: Binary-choice assays and olfactory experiments showed that compared to common tobacco (N. tabacum), the volatile of N. benthamiana has a greater attraction to whiteflies. Then we analyzed and compared volatiles from these two Nicotiana species by thermal desorption-gas chromatography-mass spectrometry (TD-GC-MS). We identified 16 chemical compounds that are more abundant in N. benthamiana than in N. tabacum. Seven compounds were further tested with olfactometer assays and we found that, among them, undecane strongly attracted whiteflies. Further experiments revealed that even 0.005 µg mL-1 undecane is attractive to whiteflies. We also silenced the genes that may influence the biosynthesis of undecane and found the production of undecane decreased after silencing NbCER3, and that N. benthamiana plants with less undecane lost their attraction to whiteflies. In addition, we found that applying 0.005 µg mL-1 undecane on yellow sticky traps can increase the number of stuck insects on the traps by ≈40%. CONCLUSION: Undecane from the volatile of N. benthamiana is a critical chemical signal that attracts whiteflies and NbCER3 involved in the biosynthesis of undecane. Undecane may be used to improve the efficiency of yellow sticky traps for whitefly control. © 2024 Society of Chemical Industry.

Metabolic and Molecular Insights Into Nicotiana benthamiana Trichome Exudates: An Ammunition Depot for Plant Resistance Against Insect Pests.

Nicotiana benthamiana, a widely acknowledged laboratory model plant for molecular studies, exhibits lethality to certain insect pests and can serve as a dead-end trap plant for pest control in the field. However, the underlying mechanism of N. benthamiana's resistance against insects remains unknown. Here, we elucidate that the lethal effect of N. benthamiana on the whitefly Bemisia tabaci arises from the toxic glandular trichome exudates. By comparing the metabolite profiles of trichome exudates, we found that 51 metabolites, including five O-acyl sugars (O-AS) with medium-chain acyl moieties, were highly accumulated in N. benthamiana. Silencing of two O-AS biosynthesis genes, branched-chain keto acid dehydrogenase (BCKD) and Isopropyl malate synthase-C (IPMS-C), significantly reduced the O-AS levels in N. benthamiana and its resistance against whiteflies. Additionally, we demonstrated that the higher expression levels of BCKD and IPMS-C in the trichomes of N. benthamiana contribute to O-AS synthesis and consequently enhance whitefly resistance. Furthermore, overexpression of NbBCKD and NbIPMS-C genes in the cultivated tobacco Nicotiana tabacum enhanced its resistance to whiteflies. Our study revealed the metabolic and molecular mechanisms underlying the lethal effect of N. benthamiana on whiteflies and presents a promising avenue for improving whitefly resistance.

miR-148b-5p regulates hypercalciuria and calcium-containing nephrolithiasis.

Calcium-containing stones represent the most common form of kidney calculi, frequently linked to idiopathic hypercalciuria, though their precise pathogenesis remains elusive. This research aimed to elucidate the molecular mechanisms involved by employing urinary exosomal microRNAs as proxies for renal tissue analysis. Elevated miR-148b-5p levels were observed in exosomes derived from patients with kidney stones. Systemic administration of miR-148b-5p in rat models resulted in heightened urinary calcium excretion, whereas its inhibition reduced stone formation. RNA immunoprecipitation combined with deep sequencing identified miR-148b-5p as a suppressor of calcitonin receptor (Calcr) expression, thereby promoting urinary calcium excretion and stone formation. Mice deficient in Calcr in distal epithelial cells demonstrated elevated urinary calcium excretion and renal calcification. Mechanistically, miR-148b-5p regulated Calcr through the circRNA-83536/miR-24-3p signaling pathway. Human kidney tissue samples corroborated these results. In summary, miR-148b-5p regulates the formation of calcium-containing kidney stones via the circRNA-83536/miR-24-3p/Calcr axis, presenting a potential target for novel therapeutic interventions to prevent calcium nephrolithiasis.

The value of 3D printing model combined PCNL in kidney stones: a systematic review and meta-analysis.

INTRODUCTION: With the continuous advancement of medical imaging, 3D printing technology is emerging. This technology allows for the representation of complex objects in a model form. This research aims to delve into the irreplaceable value of percutaneous nephrolithotomy (PCNL) in conjunction with 3D printed models in urinary stone surgery. This forward-looking approach provides doctors with a new perspective, enabling them to plan and execute surgeries with greater precision, ultimately delivering a safer and more efficient treatment experience for patients. We evaluated the literature on PCNL for the kidney stones with the introduction of 3D printing models and conducted a meta-analysis. The assessed parameters included stone clearance rate, operation time, hospital stay, blood loss, puncture accuracy, and the rate of complications. EVIDENCE ACQUISITION: We systematically searched the EMBASE, PubMed, Cochrane Library, SCIE, and Chinese Biomedical Literature Search databases for articles related to PCNL (Percutaneous Nephrolithotomy) with 3D printing models from January 2000 to January 2023. Data were managed and screened using Excel . Meta-analysis was performed for operation time, stone clearance rate, blood loss, puncture accuracy, length of hospital stay, and complications in PCNL combined with 3D printing model for kidney stone treatment. The quality of included articles was assessed using the risk of bias tool by the Cochrane Collaboration. Sensitivity analysis was conducted to assess the reliability of the results. Data were recorded using StataSE 17 software, and publication bias was examined using Egger's linear regression test. EVIDENCE SYNTHESIS: We followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines to conduct a systematic search and screening of literature relevant to the use of 3D printed models in the treatment of kidney stones. We conducted an extensive literature search across several major academic databases, including EMBASE, PubMed, Cochrane Library, SCIE, and Chinese Biomedical Literature Search databases, to ensure comprehensive coverage of relevant studies. Following the PRISMA process of screening and analysis, we ultimately included 10 randomized controlled trials with a combined sample of 608 for systematic review. CONCLUSIONS: Across these studies, we identified the introduction of 3D printing models prior to surgery for kidney stones resulted in significant advantages for the experimental group compared to the control group in terms of operation time, stone clearance rates, puncture accuracy, hospital stay, blood loss, and the incidence of complications, providing valuable insights for further research and clinical practice.

Tip bendable suction ureteral access sheath versus traditional sheath in retrograde intrarenal stone surgery: an international multicentre, randomized, parallel group, superiority study.

Background: Retrograde intrarenal surgery (RIRS) is the main treatments for upper urinary tract stones. The Ureteral Access Sheath (UAS) serves as a supplementary tool, facilitating direct kidney access during RIRS. High quality of evidence comparing tip bendable suction ureteral access sheath (S-UAS) with traditional UAS in RIRS for the treatment of renal and ureteral stones is lacking. The purpose of the study is to compare the efficacy and safety of S-UAS with traditional UAS in RIRS for the treatment of renal or ureteral stones ≤30 mm. Methods: An international, multicenter, and superiority randomized controlled trial included 320 intention-to-treat patients across 8 medical centers in China, the Philippines, Malaysia and Turkey from August 2023 to February 2024. The inclusion criteria were patients ≥18 years old with renal or ureteral stones ≤30 mm. RIRS was performed using either S-UAS or traditional UAS. The primary outcome was the immediately stone-free rate (SFR). Secondary outcomes included SFR 3 months after operation, operating time, hospital stay, auxiliary procedures, complications (using the Clavien-Dindo grading system), and improvement in the Quality of Life (QoL) score. Differences between proportions [risk difference (RD)]/means [mean difference (MD)] and 95% confidence intervals (CI) were presented. This study is registered at ClinicalTrials.gov: NCT05952635. Findings: The S-UAS group demonstrated a significantly higher immediately SFR (81.3% versus 49.4%; RD 31.9%; 95% CI 22.5%-41.7%; p = 0.004) compared to the traditional UAS group, as determined by the one-side superiority test. Additionally, the S-UAS group exhibited a higher SFR at 3 months post-operation (87.5% versus 70.0%; RD 17.5%; 95% CI 8.7%-26.3%; p < 0.001), lower postoperative fever rate (RD -11.9%; 95% CI -18.7% to -4.9%; p < 0.001), reduced use of stone baskets (RD -70.6%; 95% CI -77.8% to -63.5%; p < 0.001), and better QoL improvement (MD 7.25; 95% CI 2.21-12.29; p = 0.005). No statistically significant differences were observed in operation time, hospital stay, or the need for second-stage RIRS. Interpretation: In RIRS for upper urinary tract stones ≤30 mm, S-UAS exhibited superior performance compared to traditional UAS, demonstrating higher SFR, reduced postoperative fever rate, and improved QoL outcomes. S-UAS emerges as a prudent and advantageous alternative to traditional UAS for RIRS. Funding: National Natural Science Foundation of China and Guangdong Province, and Zhejiang Medicine and Health Program.

Cotton leaf curl Multan virus subverts the processing of hydroxyproline-rich systemin to suppress tobacco defenses against insect vectors.

Insect vector-virus-plant interactions have important ecological and evolutionary implications. The constant struggle of plants against viruses and insect vectors has driven the evolution of multiple defense strategies in the host as well as counter-defense strategies in the viruses and insect vectors. Cotton leaf curl Multan virus (CLCuMuV) is a major causal agent of cotton leaf curl disease in Asia and is exclusively transmitted by the whitefly Bemisia tabaci. Here, we report that plants infected with CLCuMuV and its betasatellite CLCuMuB enhance the performance of the B. tabaci vector, and ßC1 encoded by CLCuMuB plays an important role in begomovirus-whitefly-tobacco tripartite interactions. We showed that CLCuMuB ßC1 suppresses the jasmonic acid signaling pathway by interacting with the subtilisin-like protease 1.7 (NtSBT1.7) protein, thereby enhancing whitefly performance on tobacco plants. Further studies revealed that in wild-type plants, NtSBT1.7 could process tobacco preprohydroxyproline-rich systemin B (NtpreproHypSysB). After CLCuMuB infection, CLCuMuB ßC1 could interfere with the processing of NtpreproHypSysB by NtSBT1.7, thereby impairing plant defenses against whitefly. These results contribute to our understanding of tripartite interactions among virus, plant, and whitefly, thus offering ecological insights into the spread of vector insect populations and the prevalence of viral diseases.

A comprehensive framework for the delimitation of species within the Bemisia tabaci cryptic complex, a global pest-species group.

Identifying cryptic species poses a substantial challenge to both biologists and naturalists due to morphological similarities. Bemisia tabaci is a cryptic species complex containing more than 44 putative species; several of which are currently among the world's most destructive crop pests. Interpreting and delimiting the evolution of this species complex has proved problematic. To develop a comprehensive framework for species delimitation and identification, we evaluated the performance of distinct data sources both individually and in combination among numerous samples of the B. tabaci species complex acquired worldwide. Distinct datasets include full mitogenomes, single-copy nuclear genes, restriction site-associated DNA sequencing, geographic range, host speciation, and reproductive compatibility datasets. Phylogenetically, our well-supported topologies generated from three dense molecular markers highlighted the evolutionary divergence of species of the B. tabaci complex and suggested that the nuclear markers serve as a more accurate representation of B. tabaci species diversity. Reproductive compatibility datasets facilitated the identification of at least 17 different cryptic species within our samples. Native geographic range information provides a complementary assessment of species recognition, while the host range datasets provide low rate of delimiting resolution. We further summarized different data performances in species classification when compared with reproductive compatibility, indicating that combination of mtCOI divergence, nuclear markers, geographic range provide a complementary assessment of species recognition. Finally, we represent a model for understanding and untangling the cryptic species complexes based on the evidence from this study and previously published articles.

Quantitative analysis of microplastics in water environments based on Raman spectroscopy and convolutional neural network.

With the increasing interest in microplastics (MPs) pollutants, quantitative analysis of MPs in water environment is an important issue. Vibrational spectroscopy, represented by Raman spectroscopy, is widely used in MP detection because they can provide unique fingerprint characteristics of chemical components of MPs, but it is difficult to provide quantitative information. In this paper, an ingenious method for quantitative analysis of MPs in water environment by combining Raman spectroscopy and convolutional neural network (CNN) is proposed. It is innovatively proposed to collect the average mapping spectra (AMS) of the samples to improve the uniformity of Raman spectroscopy detection, and to increase the effective detection range of concentration by filtering different volumes of the same MP solutions. In order to verify the universality and effectiveness of the proposed method, 6 different sizes of Polyethylene (PE) MPs were used as detection objects and mixed into 5 different actual water environments. The R2 and RMSE of CNN for identifying the concentration of PE solutions could reach 0.9972 and 0.033, respectively. Meanwhile, by comparing machine learning models such as Random Forest (RF) and Support Vector Machine (SVM) were compared, and CNN combined with Raman spectroscopy has significant advantages in identifying the concentration of MPs.

A theoretical framework to improve the adoption of green Integrated Pest Management tactics.

Sustainable agriculture relies on implementing effective, eco-friendly crop protection strategies. However, the adoption of these green tactics by growers is limited by their high costs resulting from the insufficient integration of various components of Integrated Pest Management (IPM). In response, we propose a framework within IPM termed Multi-Dimensional Management of Multiple Pests (3MP). Within this framework, a spatial dimension considers the interactive effects of soil-crop-pest-natural enemy networks on pest prevalence, while a time dimension addresses pest interactions over the crop season. The 3MP framework aims to bolster the adoption of green IPM tactics, thereby extending environmental benefits beyond crop protection.

The essential role of clathrin-mediated endocytosis and early endosomes in the trafficking of begomoviruses through the primary salivary glands of their whitefly vectors.

IMPORTANCE: Many plant viruses are transmitted by insect vectors in a circulative manner. For efficient transmission, the entry of the virus from vector hemolymph into the primary salivary gland (PSG) is a step of paramount importance. Yet, vector components mediating virus entry into PSG remain barely characterized. Here, we demonstrate the role of clathrin-mediated endocytosis and early endosomes in begomovirus entry into whitefly PSG. Our findings unravel the key components involved in begomovirus transport within the whitefly body and transmission by their whitefly vectors and provide novel clues for blocking begomovirus transmission.

A chromosome-level genome assembly of the parasitoid wasp Eretmocerus hayati.

Hymenoptera is an order accounting for a large proportion of species in Insecta, among which Chalcidoidea contains many parasitoid species of biocontrol significance. Currently, some species genomes in Chalcidoidea have been assembled, but the chromosome-level genomes of Aphelinidae are not yet available. Using Illumina, PacBio HiFi and Hi-C technologies, we assembled a genome assembly of Eretmocerus hayati (Aphelinidae, Hymenoptera), a worldwide biocontrol agent of whiteflies, at the chromosome level. The assembled genome size is 692.1 Mb with a contig N50 of 7.96 Mb. After Hi-C scaffolding, the contigs was assembled onto four chromosomes with a mapping rate of > 98%. The scaffold N50 length is 192.5 Mb, and Benchmarking Universal Single-Copy Orthologues (BUSCO) value is 95.9%. The genome contains 370.8 Mb repeat sequences and total of 24471 protein coding genes. P450 gene families were identified and analyzed. In conclusion, our chromosome-level genome assembly provides valuable support for future research on the evolution of parasitoid wasps and the interaction between hosts and parasitoid wasps.

Plant resistance against whitefly and its engineering.

Plants face constant threats from insect herbivores, which limit plant distribution and abundance in nature and crop productivity in agricultural ecosystems. In recent decades, the whitefly Bemisia tabaci, a group of phloem-feeding insects, has emerged as pests of global significance. In this article, we summarize current knowledge on plant defenses against whitefly and approaches to engineer plant resistance to whitefly. Physically, plants deploy trichome and acylsugar-based strategies to restrain nutrient extraction by whitefly. Chemically, toxic secondary metabolites such as terpenoids confer resistance against whitefly in plants. Moreover, the jasmonate (JA) signaling pathway seems to be the major regulator of whitefly resistance in many plants. We next review advances in interfering with whitefly-plant interface by engineering of plant resistance using conventional and biotechnology-based breeding. These breeding programs have yielded many plant lines with high resistance against whitefly, which hold promises for whitefly control in the field. Finally, we conclude with an outlook on several issues of particular relevance to the nature and engineering of plant resistance against whitefly.

Constant ratio between the genomic components of bipartite begomoviruses during infection and transmission.

The genomic components of multipartite viruses are encapsidated in separate virus particles, and the frequencies of genomic components represent one of the key genetic features. Many begomoviruses of economic significance are bipartite, and the details of the association between their genomic components remain largely unexplored. We first analyzed the temporal dynamics of the quantities of DNA-A and DNA-B and the B/A ratio of the squash leaf curl China virus (SLCCNV) in plants and found that while the quantities of DNA-A and DNA-B varied significantly during infection, the B/A ratio remained constant. We then found that changes in the B/A ratio in agrobacteria inoculum may significantly alter the B/A ratio in plants at 6 days post inoculation, but the differences disappeared shortly thereafter. We next showed that while the quantities of DNA-A and DNA-B among plants infected by agrobacteria, sap transmission and whitefly-mediated transmission differed significantly, the B/A ratios were similar. Further analysis of gene expression revealed that the ratio of the expression of genes encoded by DNA-A and DNA-B varied significantly during infection. Finally, we monitored the temporal dynamics of the quantities of DNA-A and DNA-B and the B/A ratio of another bipartite begomovirus, and a constant B/A ratio was similarly observed. Our findings highlight the maintenance of a constant ratio between the two genomic components of bipartite begomoviruses during infection and transmission, and provide new insights into the biology of begomoviruses.

A shift of vector specificity acquired by a begomovirus through natural homologous recombination.

Recombination is common in plant viruses such as geminiviruses, but the ecological and pathogenic consequences have been explored only in a few cases. Here, we found that a new begomovirus, tomato yellow leaf curl Shuangbai virus (TYLCSbV), probably originated from the recombination of Ageratum yellow vein China virus (AYVCNV) and tobacco curl shoot virus (TbCSV). Agrobacterium-mediated inoculation showed that TYLCSbV and AYVCNV have similar levels of infectivity on tomato and tobacco plants. However, the two viruses exhibit contrasting specificities for vector transmission, that is, TYLCSbV was efficiently transmitted by the whitefly Bemisia tabaci Mediterranean (MED) rather than by the whitefly B. tabaci Middle East-Asia Minor 1 (MEAM1), whereas AYVCNV was more efficiently transmitted by MEAM1. We also showed that the transmission efficiencies of TYLCSbV and AYVCNV are positively correlated with the accumulation of the viruses in whitefly whole bodies and organs/tissues. The key coat protein amino acids that determine their accumulation are between positions 147 and 256. Moreover, field surveys suggest that MED has displaced MEAM1 in some regions where TYLCSbV was collected. Viral competition assays indicated that TYLCSbV outcompeted AYVCNV when transmitted by MED, while the outcome was the opposite when transmitted by MEAM1. Our findings suggest that recombination has resulted in a shift of vector specificity that could provide TYLCSbV with a potential selective transmission advantage, and the population shift of whitefly cryptic species could have influenced virus evolution towards an extended trajectory of transmission.

Temporal Dynamic of the Ratio between Monopartite Begomoviruses and Their Associated Betasatellites in Plants, and Its Modulation by the Viral Gene ßC1.

The begomovirus-betasatellite complex constantly threatens crops in Asia. However, the quantitative relationship between begomoviruses and betasatellites remains largely unknown. The quantities of tobacco curly shoot virus (TbCSV) and its betasatellite (TbCSB) and their ratio varied significantly in initial infection, and thereafter, the ratio tended to become constant. The TbCSB/TbCSV ratio in agrobacteria inoculum significantly affected that in plants in the initial infection but not thereafter. Null-mutation of ßC1 that encodes a multifunctional protein important for pathogenesis in TbCSB significantly reduced the TbCSB/TbCSV ratio in plants. Viral inoculum plants with higher TbCSB/TbCSV ratios promoted whitefly transmission of the virus. The expression of AV1 encoded by TbCSV, ßC1 encoded by TbCSB and the ßC1/AV1 ratio varied significantly in the initial infection and thereafter the ratio tended to become constant. Additionally, the temporal dynamics of the ratio between another begomovirus and its betasatellite was similar to that of TbCSV and was positively regulated by ßC1. These results indicate that the ratio between monopartite begomoviruses and betasatellites tend to become constant as infection progresses, and is modulated by ßC1, but a higher betasatellite/begomovirus ratio in virally inoculated plants promotes virus transmission by whiteflies. Our findings provide novel insights into the association between begomoviruses and betasatellites.

Manipulation of Whitefly Behavior by Plant Viruses.

Whiteflies of the Bemisia tabaci complex transmit hundreds of plant viruses belonging to the genera Begomovirus and Crinivirus, among others. Tripartite interactions of whitefly-virus-plant frequently occur during virus infection and transmission. Specifically, virus transmission-related behavior of whitefly, such as preference and feeding, may be altered by viruses and thus exert significant impacts on the outcome of virus spread and epidemics. Here, we provide an overview on the current understanding of the manipulation of whitefly behavior by plant viruses. Plant viruses can significantly modulate whitefly preference and feeding behavior, either directly or in a plant-mediated manner. In general, non-viruliferous whiteflies tend to prefer virus-infected plants, and viruliferous whiteflies are more likely to prefer uninfected plants. In most cases, virus infection of plants and/or whitefly seems to exhibit positive or no effects on whitefly feeding on plants. The significance and evolution of these patterns are then discussed. Finally, we suggest several future directions of research, such as the exploration of temporal dynamics and the dissection of underlying mechanisms of virus-induced changes in whitefly behavior.

A balance between vector survival and virus transmission is achieved through JAK/STAT signaling inhibition by a plant virus.

Viruses pose a great threat to animal and plant health worldwide, with many being dependent on insect vectors for transmission between hosts. While the virus-host arms race has been well established, how viruses and insect vectors adapt to each other remains poorly understood. Begomoviruses comprise the largest genus of plant-infecting DNA viruses and are exclusively transmitted by the whitefly Bemisia tabaci. Here, we show that the vector Janus kinase/signal transducer and activator of transcription (JAK/STAT) pathway plays an important role in mediating the adaptation between the begomovirus tomato yellow leaf curl virus (TYLCV) and whiteflies. We found that the JAK/STAT pathway in B. tabaci functions as an antiviral mechanism against TYLCV infection in whiteflies as evidenced by the increase in viral DNA and coat protein (CP) levels after inhibiting JAK/STAT signaling. Two STAT-activated effector genes, BtCD109-2 and BtCD109-3, mediate this anti-TYLCV activity. To counteract this vector immunity, TYLCV has evolved strategies that impair the whitefly JAK/STAT pathway. Infection of TYLCV is associated with a reduction of JAK/STAT pathway activity in whiteflies. Moreover, TYLCV CP binds to STAT and blocks its nuclear translocation, thus, abrogating the STAT-dependent transactivation of target genes. We further show that inhibition of the whitefly JAK/STAT pathway facilitates TYLCV transmission but reduces whitefly survival and fecundity, indicating that this JAK/STAT-dependent TYLCV-whitefly interaction plays an important role in keeping a balance between whitefly fitness and TYLCV transmission. This study reveals a mechanism of plant virus-insect vector coadaptation in relation to vector survival and virus transmission.