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 plant DNA virus replicates in the salivary glands of its insect vector via recruitment of host DNA synthesis machinery.

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses. So far, only some plant RNA viruses have been demonstrated to replicate in insect vectors and plant hosts. How plant viruses evolved to replicate in the animal kingdom remains largely unknown. Geminiviruses comprise a large family of plant-infecting, single-stranded DNA viruses that cause serious crop losses worldwide. Here, we report evidence and insight into the replication of the geminivirus tomato yellow leaf curl virus (TYLCV) in the whitefly (Bemisia tabaci) vector and that replication is mainly in the salivary glands. We found that TYLCV induces DNA synthesis machinery, proliferating cell nuclear antigen (PCNA) and DNA polymerase δ (Polδ), to establish a replication-competent environment in whiteflies. TYLCV replication-associated protein (Rep) interacts with whitefly PCNA, which recruits DNA Polδ for virus replication. In contrast, another geminivirus, papaya leaf curl China virus (PaLCuCNV), does not replicate in the whitefly vector. PaLCuCNV does not induce DNA-synthesis machinery, and the Rep does not interact with whitefly PCNA. Our findings reveal important mechanisms by which a plant DNA virus replicates across the kingdom barrier in an insect and may help to explain the global spread of this devastating pathogen.

Effects of heat stress on virus transmission and virus-mediated apoptosis in whitefly Bemisia tabaci.

Tomato yellow leaf curl virus (TYLCV), a plant DNA virus of the genus Begomovirus, is transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner. Our previous study indicated that activation of the apoptosis pathway in whiteflies could facilitate TYLCV accumulation and transmission. Considering that temperature change can influence the spread of insect-borne plant viruses, we focused on plant virus induced-apoptosis to investigate the underlying mechanism of temperature regulation on plant virus transmission via an insect vector. We found that heat stress (40°C) on whiteflies could facilitate TYLCV accumulation and increase transmission to tomato plants. Despite upregulation of caspase-1 and caspase-3 gene expression, heat stress failed to induce an increase in the activation of cleaved caspase-3 and DNA fragmentation in TYLCV-infected whiteflies. However, our data failed to determine the role of heat stress in apoptosis modulation of insect-plant virus interplay while still providing clues to understand insect vectors and their transmitted plant viruses.

Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors.

Most plant viruses are vectored by insects and the interactions of virus-plant-vector have important ecological and evolutionary implications. Insect vectors often perform better on virus-infected plants. This indirect mutualism between plant viruses and insect vectors promotes the spread of virus and has significant agronomical effects. However, few studies have investigated how plant viruses manipulate plant defenses and promote vector performance. Begomoviruses are a prominent group of plant viruses in tropical and sub-tropical agro-ecosystems and are transmitted by whiteflies. Working with the whitefly Bemisia tabaci, begomoviruses and tobacco, we revealed that C2 protein of begomoviruses lacking DNA satellites was responsible for the suppression of plant defenses against whitefly vectors. We found that infection of plants by tomato yellow leaf curl virus (TYLCV), one of the most devastating begomoviruses worldwide, promoted the survival and reproduction of whitefly vectors. TYLCV C2 protein suppressed plant defenses by interacting with plant ubiquitin. This interaction compromised the degradation of JAZ1 protein, thus inhibiting jasmonic acid defense and the expression of MYC2-regulated terpene synthase genes. We further demonstrated that function of C2 protein among begomoviruses not associated with satellites is well conserved and ubiquitination is an evolutionarily conserved target of begomoviruses for the suppression of plant resistance to whitefly vectors. Taken together, these results demonstrate that ubiquitination inhibition by begomovirus C2 protein might be a general mechanism in begomovirus, whitefly and plant interactions.

A newly recorded Rickettsia of the Torix group is a recent intruder and an endosymbiont in the whitefly Bemisia tabaci.

The bacterium Rickettsia is found widely in phytophagous insects and often exerts profound effects on the phenotype and fitness of its hosts. Here, we decrypt a new, independent, phylogenetically ancient Torix Rickettsia endosymbiont found constantly in a laboratory line of an economically important insect Asia II 7, a putative species of the Bemisia tabaci whitefly complex (Hemiptera: Aleyrodidae), and occasionally in field whitefly populations. This new Rickettsia distributes throughout the body of its whitefly host. Genetically, compared to Rickettsia_bellii_MEAM1 found earlier in whiteflies, the new Rickettsia species has more gene families and pathways, which may be important factors in shaping specific symbiotic relationships. We propose the name 'Candidatus Rickettsia_Torix_Bemisia_tabaci (RiTBt)' for this new endosymbiont associated with whiteflies. Comparative genomic analyses indicate that RiTBi may be a relatively recent intruder in whiteflies given its low abundance in the field and relatively larger genome compared to Rickettsia_bellii_MEAM1.

Vector development and vitellogenin determine the transovarial transmission of begomoviruses.

The majority of plant viruses are transmitted by insect vectors between hosts, and transovarial transmission of viruses from vector parents to offspring has great significance to their epidemiology. Begomoviruses are transmitted by the whitefly Bemisia tabaci in a circulative manner and are maintained through a plant-insect-plant cycle. Other routes of begomovirus transmission are not clearly known. Here, we report that transovarial transmission from female whiteflies to offspring often happens for one begomovirus, Tomato yellow leaf curl virus (TYLCV), and may have contributed significantly to its global spread. We found that TYLCV entry of the reproductive organ of its vector mainly depended on the developmental stage of the whitefly ovary, and the transovarial transmission of TYLCV to offspring increased with whitefly adult age. The specific interaction between virus coat protein (CP) and whitefly vitellogenin (Vg) was vital for virus entry into whitefly ovary. When knocking down the expression of Vg, the entry of TYLCV into ovary was inhibited and the transovarial transmission efficiency decreased. In contrast, another begomovirus, Papaya leaf curl China virus (PaLCuCNV), CP did not interact with whitefly Vg, and PaLCuCNV could not be transovarially transmitted by whiteflies. We further showed that TYLCV could be maintained for at least two generations in the absence of virus-infected plants, and the adult progenies were able to infect healthy plants in both the laboratory and field. This study reports the transovarial transmission mechanism of begomoviruses, and it may help to explain the evolution and global spread of some begomoviruses.

The inherited bacterial symbiont Hamiltonella influences the sex ratio of an insect host.

In many intracellular symbioses, the microbial symbionts provide nutrients advantageous to the host. However, the function of Hamiltonella defensa, a symbiotic bacterium localized in specialized host cells (bacteriocytes) of a whitefly Bemisia tabaci, is uncertain. We eliminate this bacterium from its whitefly host by two alternative methods: heat treatment and antibiotics. The sex ratio of the host progeny and subsequent generations of Hamiltonella-free females was skewed from 1 : 1 (male : female) to an excess of males, often exceeding a ratio of 20 : 1. B. tabaci is haplodiploid, with diploid females derived from fertilized eggs and haploid males from unfertilized eggs. The Hamiltonella status of the insect did not affect copulation frequency or sperm reserve in the spermathecae, indicating that the male-biased sex ratio is unlikely due to the limitation of sperm but likely to be associated with events subsequent to sperm transfer to the female insects, such as failure in fertilization. The host reproductive response to Hamiltonella elimination is consistent with two alternative processes: adaptive shift in sex allocation by females and a constitutive compensatory response of the insect to Hamiltonella-mediated manipulation. Our findings suggest that a bacteriocyte symbiont influences the reproductive output of female progeny in a haplodiploid insect.

Transcriptome profiling of whitefly guts in response to Tomato yellow leaf curl virus infection.

BACKGROUND: Plant viruses in agricultural crops are of great concern worldwide, and over 75% of them are transmitted from infected to healthy plants by insect vectors. Tomato yellow leaf curl virus (TYLCV) is a begomovirus, which is the largest and most economically important group of plant viruses, transmitted by the whitefly Bemisia tabaci. The circulation of TYLCV in the insect involves complex insect-virus interactions, whereas the molecular mechanisms of these interactions remain ambiguous. The insect gut as a barrier for viral entry and dissemination is thought to regulate the vector specificity. However, due to its tiny size, information for the responses of whitefly gut to virus infection is limited. METHODS: We investigated the transcriptional response of the gut of B. tabaci Middle East-Asia Minor 1 species to TYLCV infection using Illumina sequencing. RESULTS: A total of 5207 differentially expressed genes (DEGs) between viruliferous and non-viruliferous whitefly guts were identified. Enrichment analyses showed that cargo receptor and ATP-binding cassette (ABC) transporters were enriched in DEGs, and might help the virus to cross gut barrier. TYLCV could perturb cell cycle and DNA repair as a possible result of its replication in the whitefly. Our data also demonstrated that TYLCV can activate whitefly defense responses, such as antimicrobial peptides. Meanwhile, a number of genes involved in intracellular signaling were activated by TYLCV infection. CONCLUSIONS: Our results reveal the complex insect-virus relationship in whitefly gut and provide substantial molecular information for the role of insect midguts in virus transmission.

Vector and nonvector insect feeding reduces subsequent plant susceptibility to virus transmission.

The interactions of vector-virus-plant have important ecological and evolutionary implications. While the tripartite interactions have received some attention, little is known about whether vector infestation affects subsequent viral transmission and infection. Working with the whitefly Bemisia tabaci, begomovirus and tobacco/tomato, we demonstrate that pre-infestation of plants by the whitefly vector reduced subsequent plant susceptibility to viral transmission. Pre-infestation by the cotton bollworm, a nonvector of the virus, likewise repressed subsequent viral transmission. The two types of insects, with piercing and chewing mouthparts, respectively, activated different plant signaling pathways in the interactions. Whitefly pre-infestation activated the salicylic acid (SA) signaling pathway, leading to deposition of callose that inhibited begomovirus replication/movement. Although cotton bollworm infestation elicited the jasmonic acid (JA) defense pathway and was beneficial to virus replication, the pre-infested plants repelled whiteflies from feeding and so decreased virus transmission. Experiments using a pharmaceutical approach with plant hormones or a genetic approach using hormone transgenic or mutant plants further showed that SA played a negative but JA played a positive role in begomovirus infection. These novel findings indicate that both vector and nonvector insect feeding of a plant may have substantial negative consequences for ensuing viral transmission and infection.

Differential responses of the whitefly Bemisia tabaci symbionts to unfavorable low and high temperatures.

The whitefly Bemisia tabaci complex contains many cryptic species, of which the Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) are notorious invasive pests. In our field-collected whitefly samples, MEAM1 harbors an obligate primary symbiont "Candidatus Portiera aleyrodidarum" and two secondary symbionts, "Candidatus Hamiltonella defensa" and Rickettsia sp., whereas MED has only "Ca. Portiera aleyrodidarum" and "Ca. Hamiltonella defensa." Both "Ca. Portiera aleyrodidarum" and "Ca. Hamiltonella defensa" are intracellular endosymbionts residing in the bacteriomes, whereas Rickettsia sp. has a scattered distribution throughout the host body cavity. We examined responses of these symbionts to adverse temperatures as well as survival of the host insects. After cold treatment at 5 or 10 °C or heat treatment at 35 or 40 °C for 24 h, respectively, the infection rates of all symbionts were not significantly decreased based on diagnosis PCR. However, quantitative PCR assays indicated significant reduction of "Ca. Hamiltonella defensa" at 40 °C, and the reduction became greater as the duration increased. Compared with "Ca. Hamiltonella defensa," "Ca. Portiera aleyrodidarum" was initially less affected in the first day but then showed more rapid reduction at days 3-5. The density of Rickettsia sp. fluctuated but was not reduced significantly at 40 °C. Meanwhile, the mortality rates of the host whiteflies elevated rapidly as the duration of exposure to heat treatment increased. The differential responses of various symbionts to adverse temperatures imply complex interactions among the symbionts inside the same host insect and highlight the importance of taking the whole bacterial community into account in studies of symbioses.

Effects of reproductive interference on the competitive displacement between two invasive whiteflies.

Reproductive interference is one of the major factors mediating species exclusion among insects. The cryptic species Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) of the whitefly Bemisia tabaci complex have invaded many parts of the world and often exhibit niche overlap and reproductive interference. However, contrasting patterns of competitive displacement between the two invaders have been observed between regions such as those in USA and China. Understanding the roles of reproductive interference in competitive interactions between populations of the two species in different regions will help unravel other factors related to their invasion. We integrated laboratory population experiments, behavioural observations and simulation modelling to investigate the role of reproductive interference on species exclusion between MEAM1 and MED in China. In mixed cohorts of the two species MEAM1 always excluded MED in a few generations when the initial proportion of MEAM1 was ⩾0.25. Even when the initial proportion of MEAM1 was only 0.10, however, MEAM1 still had a higher probability of excluding MED than that for MED to exclude MEAM1. Importantly, we show that as MEAM1 increased in relative abundance, MED populations became increasingly male-biased. Detailed behavioural observations confirmed that MEAM1 showed a stronger reproductive interference than MED, leading to reduced frequency of copulation and female progeny production in MED. Using simulation modelling, we linked our behavioural observations with exclusion experiments to show that interspecific asymmetric reproductive interference predicts the rate of species exclusion of MED by MEAM1. These findings not only reveal the importance of reproductive interference in the competitive interactions between the two invasive whiteflies as well as the detailed behavioural mechanisms, but also provide a valuable framework against which the effects of other factors mediating species exclusion can be explored.

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.

Competitive displacement between two invasive whiteflies: insecticide application and host plant effects.

The cryptic species Middle East-Asia Minor 1 (MEAM1), formerly referred to as 'B biotype', of the whitefly Bemisia tabaci complex entered China in the mid 1990s, and the Mediterranean (MED) cryptic species, formerly referred to as 'Q biotype', of the same whitefly complex entered China around 2003. Field surveys in China after 2003 indicate that in many regions MED has been replacing the earlier invader MEAM1. The factors underlying this displacement are unclear. We conducted laboratory experiments and field sampling to examine the effects of insecticide application on the competitive interactions between MEAM1 and MED. In the laboratory, on cotton, a plant showing similar levels of suitability to both whitefly species, MEAM1 displaced MED in five generations when initial populations of the two species were equal and no insecticide was applied. In contrast, MED displaced MEAM1 in seven and two generations, respectively, when 12.5 and 50.0 mg l⁻¹ imidacloprid was applied to the plants via soil drench. Field sampling indicated that in a single season MED displaced MEAM1 on crops heavily sprayed with neonicotinoid insecticides but the relative abundance of the two species changed little on crops without insecticide spray. We also examined the effects of host plants on the competitive interactions between the two species in the laboratory. When cohorts with equal abundance of MEAM1 and MED were set up on different host plants, MEAM1 displaced MED on cabbage and tomato in five and seven generations, respectively, but MED displaced MEAM1 on pepper in two generations. As field populations of MED have lower susceptibility than those of MEAM1 to nearly all commonly used insecticides including imidacloprid, insecticide application seems to have played a major role in shifting the species competitive interaction effects in favour of MED in the field across China. Host plants may also shape competition between the two species depending on the relative levels of plant suitability.

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.

Complete mitochondrial genome of the whitefly Aleyrodes shizuokensis Kuwana (Hemiptera: Aleyrodidae), new record from Chinese mainland.

The complete mitochondrial genome was determined for the whitefly Aleyrodes shizuokensis (Hemiptera: Aleyrodidae), the first record from Chinese mainland. The mitochondrial genome is 16,687 bp in length and contains 13 protein-coding genes (PCGs), 22 transfer RNAs, and two ribosomal RNAs. The overall base composition is 33.8% A, 47.0% T, 12.2% G, and 7.0% C. All PCGs start with ATN codon. COX1 ends with a T, and the other 12 PCGs use TAA or TAG as the stop codon. Gene arrangement of the 13 PCGs is identical to that of the giant whitefly Aleurodicus dugesii and greenhouse whitefly Trialeurodes vaporariorum. The resultant Bayesian inference and maximum-likelihood trees based on the sequence data of 13 PCGs support its close relationship with sugarcane whitefly Neomaskellia andropogonis.

Impact of a novel Rickettsia symbiont on the life history and virus transmission capacity of its host whitefly (Bemisia tabaci).

Rickettsia consists of some of the most prevalent symbionts of insects and often plays a significant role in the biology of its hosts. Recently, a maternally inherited Torix group Rickettsia, provisionally named as RiTBt, was recorded in a species of notorious pest whitefly, tentatively named as Asia II 1, from the Bemisia tabaci complex. The role of this Rickettsia in the biology of its host is unknown. Here we investigated the impact of RiTBt on the performance and virus transmission capacity of Asia II 1. RiTBt did not significantly affect the life history parameters of the whitefly when the host insect was reared on tobacco, tomato, and cotton, three host plants with relatively low, medium and high suitability to the whitefly. Intriguingly, RiTBt slightly enhanced whitefly transmission of cotton leaf curl Multan virus (CLCuMuV), a virus that is transmitted by the whitefly in the field and has caused extensive damage to cotton production. Specifically, compared with whiteflies without RiTBt, following a 48 h virus acquisition whiteflies with RiTBt had higher titer of virus and showed higher efficiency of virus transmission. A rickettsial secretory protein BtR242 was identified as a putative virus-binding protein, and was observed to interact with the coat protein of CLCuMuV in vitro. Viral infection of the whitefly downregulated gene transcript levels of the BtR242 gene. These observations indicate that RiTBt has limited impact on the biology of the Asia II 1 whitefly, and whether this symbiont has functions in the biology of other host whiteflies warrants future investigation.

Functional Analysis of Alkaline Phosphatase in Whitefly Bemisia tabaci (Middle East Asia Minor 1 and Mediterranean) on Different Host Plants.

Alkaline phosphatases (ALPs: EC 3.1.3.1) are ubiquitous enzymes and play crucial roles in the fundamental phosphate uptake and secretory processes. Although insects are regarded as the most diverse group of organisms, the current understanding of ALP roles in insects is limited. As one type of destructive agricultural pest, whitefly Bemisia tabaci, a phloem feeder and invasive species, can cause extensive crop damage through feeding and transmitting plant diseases. In this study, we retrieved five ALP genes in MEAM1 whitefly, nine ALP genes in MED whitefly via comparative genomics approaches. Compared with nine other insects, whiteflies' ALP gene family members did not undergo significant expansion during insect evolution, and whiteflies' ALP genes were dispersed. Moreover, whiteflies' ALP gene family was conserved among insects and emerged before speciation via phylogenetic analysis. Whiteflies' ALP gene expression profiles presented that most ALP genes have different expression patterns after feeding on cotton or tobacco plants. Female/male MED whiteflies possessed higher ALP activities on both cotton and tobacco plants irrespective of sex, relative to MEAM1 whiteflies. Meanwhile, adult MED whiteflies possessed higher ALP activity in both whole insect and salivary samples, relative to MEAM1 whiteflies. We also found that both MED and MEAM1 whiteflies could upregulate ALP activities after feeding on cotton compared with feeding on tobacco plants. These findings demonstrated the functions of whiteflies ALPs and will assist the further study of the genomic evolution of insect ALPs.

Localization and Quantification of Begomoviruses in Whitefly Tissues by Immunofluorescence and Quantitative PCR.

Begomoviruses (genus Begomovirus, family Geminiviridae) are transmitted by whiteflies of the Bemisia tabaci complex in a persistent, circulative manner. Considering the extensive damage caused by begomoviruses to crop production worldwide, it is imperative to understand the interaction between begomoviruses and their whitefly vector. To do so, localization and quantification of the virus in the vector tissues is crucial. Here, using tomato yellow leaf curl virus (TYLCV) as an example, we describe a detailed protocol to localize begomoviruses in whitefly midguts, primary salivary glands, and ovaries by immunofluorescence. The method is based on the use of specific antibodies against a virus coat protein, dye-labeled secondary antibodies, and a confocal microscope. The protocol can also be used to colocalize begomoviral and whitefly proteins. We further describe a protocol for the quantification of TYLCV in whitefly midguts, primary salivary glands, hemolymph, and ovaries by quantitative PCR (qPCR). Using primers specifically designed for TYLCV, the protocols for quantification allow the comparison of the amount of TYLCV in different tissues of the whitefly. The described protocol is potentially useful for the quantification of begomoviruses in the body of a whitefly and a virus-infected plant. These protocols can be used to analyze the circulation pathway of begomoviruses in the whitefly or as a complement to other methods to study whitefly-begomovirus interactions.

Differential transmission of Sri Lankan cassava mosaic virus by three cryptic species of the whitefly Bemisia tabaci complex.

In recent years, Sri Lankan cassava mosaic virus (SLCMV), a begomovirus (genus Begmovirus, family Geminiviridae) causing cassava mosaic disease in Asia, poses serious threats to cassava cultivation in Asia. However, the transmission of SLCMV in the areas into which it has recently been introduced remain largely unexplored. Here we have compared the transmission efficiencies of SLCMV by three widely distributed whitefly species in Asia, and found that only Asia II 1 whiteflies were able to transmit this virus efficiently. The transmission efficiencies of SLCMV by different whitefly species were found to correlate positively with quantity of virus in whitefly whole body. Further, the viral transmission efficiency was found to be associated with varied ability of virus movement within different species of whiteflies. These findings provide detailed information regarding whitefly transmission of SLCMV, which will help to understand the spread of SLCMV in the field, and facilitate the prediction of virus epidemics.

Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission.

Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission.IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.