Global emergence of begomoviruses in cucurbits: diversity, epidemiology, and management strategies

1 Introduction

Cucurbits (family Cucurbitaceae) are widely cultivated across tropical and subtropical regions. Besides providing important nutritional and health benefits, they contribute more than 200 million tonnes annually to global food production (1). However, cucurbit production is increasingly constrained by viral diseases, particularly those caused by begomoviruses (family Geminiviridae) (2–4).

Begomoviruses are whitefly-transmitted circular single-stranded DNA viruses with monopartite or bipartite genomes that infect a wide range of dicotyledonous hosts (5, 6). According to the latest ICTV Master Species List (MSL 41), the genus Begomovirus comprises 464 recognized species, making it the largest genus within the family Geminiviridae. Their remarkable evolutionary success is driven mainly by mutation, recombination, pseudorecombination, and frequent associations with satellite molecules (7–9).

The rapid expansion of Bemisia tabaci populations, together with climate-driven changes in vector distribution and changing agricultural practices, has further accelerated the emergence of begomovirus diseases in new geographical regions (10). Extensive research has substantially advanced our understanding of begomovirus diversity, genome organization, host interactions, epidemiology, and disease management. Nevertheless, important questions remain regarding the interacting biological and ecological factors driving viral emergence and geographical expansion and the translation of increasingly sophisticated molecular diagnostic technologies into reliable field applications. Addressing these challenges is becoming increasingly important as begomovirus epidemics continue to expand into new production regions.

This review synthesizes current understanding of cucurbit-infecting begomoviruses, with emphasis on their diversity, epidemiology, symptomatology, genome organization, infection biology, global distribution, detection, and management. Particular attention is given to the biological and ecological processes underlying viral emergence and spread, advances in molecular diagnostic technologies, and the opportunities and challenges associated with their deployment under field conditions. Finally, the review identifies key research priorities to strengthen disease surveillance, improve epidemic preparedness, and support sustainable management of begomovirus diseases in cucurbit production systems.

2 Symptomatology and disease impact

Begomovirus infection produces a broad spectrum of symptoms in cucurbits that reflect interactions among viral genotype, host susceptibility, environmental conditions and, in many cases, associated satellite molecules (2, 6, 11). Disease expression affects vegetative growth, reproductive development and fruit quality. Typical foliar symptoms include leaf curling, mosaic, chlorosis, vein thickening, vein clearing, blistering, leaf deformation, shortened internodes and plant stunting (Figure 1), whereas at the reproductive level infections commonly reduce flowering, impair fruit set and cause malformed fruits (2, 12, 13).

Symptom expression varies markedly among virus–host combinations. Cucurbit leaf crumple virus (CuLCrV) typically induces downward leaf curling in watermelon and squash, whereas Squash leaf curl virus (SLCV) more frequently causes upward leaf cupping and severe distortion (12). Vein hypertrophy, particularly on young leaves, is a characteristic feature of Tomato leaf curl New Delhi virus (ToLCNDV) infection in zucchini, melon and cucumber, although the severity of this trait varies with cultivar and environment (2). Comparable variation has been reported for other cucurbit-infecting begomoviruses across geographical regions and host species, underscoring the context-dependent nature of symptomatology (14, 15).

Mixed infections further complicate symptom development. Co-infection of Watermelon chlorotic stunt virus (WmCSV) and SLCV in Lebanon produced more intense yellowing, leaf deformation and plant dwarfing than either virus alone (16), indicating that disease severity often reflects interactions among co-infecting viruses, host plants and their associated satellites rather than the effect of a single pathogen. Similar multivirus disease complexes have recently been described in cucurbit crops in Saudi Arabia (17), where they are associated with severe yield and quality losses.

Beyond visual symptoms, the major economic impact of cucurbit-infecting begomoviruses arises from reductions in marketable yield (2, 3, 18). Early infections frequently suppress flowering, reduce fruit set, generate malformed fruits and, in severe cases, cause near-complete crop failure (2, 19). However, quantitative yield losses vary widely among pathosystems and production environments owing to differences in host genetic background, environmental conditions, cropping systems and disease assessment methods (6, 11).

Collectively, these observations indicate that while symptom assessment remains useful for rapid field recognition and for prioritizing samples, its diagnostic value is constrained by the high variability of symptom expression across virus–host combinations and the prevalence of mixed infections. Symptom-based diagnosis should therefore be complemented by molecular assays for accurate pathogen identification, robust epidemiological inference and evidence-based disease management (2, 20).

3 Genome organization

Genome organization provides the molecular framework for understanding the adaptability, pathogenicity and evolutionary success of begomoviruses (6, 21). Differences in genome architecture influence viral replication, systemic movement, host interactions and recombination potential, and ultimately shape the ability of these viruses to colonize new hosts and expand into new geographical regions (6, 11, 22). Consequently, comparative analyses of genome organization yield critical insights into disease development, viral evolution and the emergence of novel begomovirus variants (6, 23).

Begomoviruses possess circular single-stranded DNA (ssDNA) genomes that occur either as a single genomic component (monopartite) or as two components (bipartite), designated DNA-A and DNA-B, each approximately 2.5–2.8 kb in size (24, 25). Bipartite genomes predominate among New World begomoviruses, whereas both monopartite and bipartite species occur in the Old World (5). DNA-A encodes proteins required for viral replication and host interaction, including the replication-associated protein (Rep/AC1), the transcriptional activator protein (TrAP/AC2), the replication enhancer protein (REn/AC3) and the multifunctional C4 protein, which contributes to symptom development and suppression of host defense responses. The coat protein (CP/AV1) mediates encapsidation and vector-mediated transmission, while the pre-coat protein (V2/AV2), present in many Old World begomoviruses, facilitates viral movement and suppression of host RNA silencing (6, 25). DNA-B encodes two movement-associated proteins: the nuclear shuttle protein (NSP/BV1), which transports viral DNA between the nucleus and cytoplasm, and the movement protein (MP/BC1), which mediates cell-to-cell spread through plasmodesmata. Functional coordination between DNA-A and DNA-B is therefore essential for successful systemic infection in bipartite begomoviruses (Figure 2).

Although this overall genomic layout is broadly conserved across the genus, frequent mutation, recombination and pseudorecombination continually reshape begomovirus genomes, generating variants with altered virulence, host range and geographical distribution (6, 14, 23). These evolutionary processes have contributed directly to the emergence and global spread of economically important cucurbit-infecting viruses such as Tomato leaf curl New Delhi virus (ToLCNDV), for which multiple recombination breakpoints have been identified and linked to host-range expansion and intercontinental dissemination (2, 15, 26, 27). Understanding how canonical genome architecture constrains and enables such evolutionary change is therefore central to predicting the future trajectories of cucurbit-infecting begomoviruses.

4 Mechanisms of infection and pathogenesis

Infection begins when viruliferous whiteflies (Bemisia tabaci) introduce viral particles into plant tissues during feeding. Following entry, the viral genome is transported to the nucleus and replicated using host DNA replication machinery, primarily via rolling-circle and recombination-dependent mechanisms (11). However, most detailed molecular studies have been conducted in model hosts such as Nicotiana benthamiana, and their relevance under field conditions in cucurbit crops still needs to be validated (11).

The vector B. tabaci is not a passive carrier but an active participant in the infection process (28). Different B. tabaci biotypes, such as MEAM1 (Middle East–Asia Minor 1) and MED (Mediterranean), differ in transmission efficiency, host preferences and insecticide susceptibility, which strongly influence begomovirus epidemiology and disease spread (3, 5). Whitefly feeding also triggers plant defense responses, including activation of jasmonic acid and salicylic acid pathways, which can either facilitate or restrict viral infection depending on the virus–host combination (22). The ability of whiteflies to acquire and transmit multiple begomoviruses simultaneously promotes mixed infections and disease complexes, particularly in regions with high whitefly pressure, as reported for cucurbit crops in the Middle East (17). In addition, whitefly endosymbionts such as Hamiltonella, Rickettsia and Portiera have been implicated in modulating transmission efficiency, although their specific roles in cucurbit-infecting begomoviruses remain poorly characterized (5). Understanding these vector-mediated interactions is therefore critical for designing effective management strategies, because vector behavior and population dynamics directly shape patterns of viral spread and disease severity.

4.1 Satellite molecules and their role in pathogenicity

In addition to their genomic components, many Old World begomoviruses are associated with subviral satellite molecules that significantly modulate pathogenicity, symptom expression, and host range (23, 29). These satellites are circular single-stranded DNA molecules of approximately 1.3 kb that depend on a helper begomovirus for replication, encapsidation, insect transmission, and systemic movement (30, 31).

Betasatellites are the most extensively characterized satellite molecules associated with begomoviruses. They encode a single multifunctional protein, βC1, which acts as a potent suppressor of host RNA silencing and transcriptional gene silencing, thereby enhancing viral pathogenicity (22). βC1 also interferes with host developmental pathways, leading to the severe leaf curling, enations, and stunting characteristic of betasatellite-associated diseases (29). In cucurbits, betasatellites have been identified in association with several Old World begomoviruses, including ToLCNDV and WmCSV, and their presence has been correlated with increased symptom severity and higher viral DNA accumulation (17, 23). In the Middle East, WmCSV frequently occurs in complexes with betasatellites that intensify disease symptoms in watermelon and melon, complicating disease management (17).

Alphasatellites represent another class of satellite molecules (~1.4 kb) that encode a replication-associated protein but depend on the helper begomovirus for encapsidation, movement, and transmission (23). Unlike betasatellites, alphasatellites do not generally enhance symptom severity, though their precise role in begomovirus disease complexes remains incompletely understood. Recent evidence suggests that alphasatellites may modulate vector transmission efficiency or influence viral replication dynamics (23, 29).

Deltasatellites represent a recently characterized and distinct class of begomovirus-associated satellites, approximately 0.7–1.4 kb in size, that are derived from defective recombinant molecules of the helper virus genome (8, 32). Unlike betasatellites, deltasatellites do not encode any functional protein and rely entirely on the helper begomovirus for replication, encapsidation, and transmission (33). Their biological significance has been most extensively studied in association with sweepoviruses (begomoviruses infecting sweet potato), where they have been shown to modulate symptom severity in a helper-virus-dependent manner — sometimes attenuating and other times exacerbating symptoms (32). Deltasatellites can also influence viral DNA accumulation and, in some cases, interfere with whitefly transmission efficiency, suggesting a complex interplay between the satellite and its helper virus (8).

In cucurbit-infecting begomovirus systems, the occurrence and functional relevance of deltasatellites remain largely unexplored. To date, no deltasatellite has been definitively characterized in association with ToLCNDV, SLCV, CuLCrV, or other major cucurbit-infecting begomoviruses. However, given the widespread distribution of deltasatellites in other begomovirus-host systems and the increasing detection of mixed begomovirus infections in cucurbits (17), systematic surveys are warranted to determine whether deltasatellites contribute to symptom modulation, host adaptation, or epidemiological dynamics in cucurbit crops. The discovery of such associations would have important implications for disease diagnosis and management, as deltasatellites could serve as additional targets for molecular detection or RNAi-based control strategies (34).

The association of satellites with cucurbit-infecting begomoviruses has important epidemiological and management implications. Satellites can expand host ranges and increase viral fitness, facilitating the emergence of new disease complexes with altered symptom phenotypes (30, 31). Moreover, the presence of satellites increases the genetic complexity of begomovirus populations and provides additional targets for RNA interference-based management strategies (35). However, significant uncertainties persist regarding the distribution, diversity, and functional roles of satellites in cucurbit-infecting begomoviruses, particularly in New World contexts where satellites are less common (21). Addressing these gaps through systematic surveys and functional studies will be essential for understanding the full pathogenic potential of cucurbit begomovirus complexes and for designing effective disease management strategies.

4.2 Histological and histopathological insights into begomovirus infection in cucurbits

Histological and histopathological investigations provide a critical tissue-level perspective on begomovirus biology in cucurbits, clarifying the structural basis of viral movement, symptom expression, and host resistance (36–39). Cucurbit-infecting begomoviruses are strongly phloem-limited, and their interactions with vascular tissues underpin both pathology and resistance (2, 36, 39). Classical ultrastructural work on Squash leaf curl virus (SLCV) in zucchini squash revealed abundant virions and large nuclear inclusion bodies in vascular parenchyma nuclei and maturing sieve elements, often occupying much of the nuclear volume, with virus particles present even in immature sieve elements indicating early colonization of differentiating vascular tissues (36). Severe sieve element necrosis occurred within days of infection, highlighting rapid disruption of phloem function, while fibrous ring structures typical of some geminiviruses were rare in SLCV-infected tissues, suggesting a potentially useful ultrastructural diagnostic trait (36). Comparable observations have been made for Cucurbit leaf crumple virus (CuLCrV), an emergent bipartite begomovirus infecting squash, watermelon, cantaloupe, and honeydew, with immunolocalization and in situ hybridization confirming that CuLCrV is strictly phloem-limited and not sap-transmissible, in contrast to many mechanically transmissible cucurbit RNA viruses (37, 40). These histological findings align with epidemiological data for begomoviruses such as SLCV and Tomato leaf curl New Delhi virus (ToLCNDV), which are acquired and inoculated by phloem-feeding Bemisia tabaci and are not efficiently transmitted by mechanical means (38, 39).

Histological comparisons with other cucurbit viruses underscore distinctive diagnostic features of begomovirus infections. Squash yellow leaf curl virus (SYLCV), a whitefly-transmitted poty-like virus, induces pinwheel-like cytoplasmic inclusion bodies in vascular parenchyma cells and is easily mechanically transmitted, contrasting with the predominantly nuclear inclusions and non-mechanical transmission of cucurbit-infecting begomoviruses (41, 42). Such contrasts in inclusion type, subcellular localization (nuclear versus cytoplasmic), and associated structures provide important ultrastructural criteria for distinguishing begomoviruses from other whitefly-borne viruses when symptoms overlap (41). Although detailed ultrastructural studies exist for SLCV and CuLCrV, comparable histopathological investigations across other cucurbit species, regions, and begomovirus complexes remain limited (2). In many contexts, molecular diagnostics such as PCR, sequencing, and phylogenetics dominate, often without parallel tissue-level analyses, despite the global importance of begomoviruses such as ToLCNDV and SLCV-related strains (2, 38). Expanding histological work across diverse host–virus combinations would help elucidate tissue-level resistance mechanisms and complement molecular epidemiology (2).

The strict phloem limitation of cucurbit-infecting begomoviruses and their reliance on phloem-feeding whiteflies support the use of systemic insecticides and other tactics that target vascular feeding stages of Bemisia rather than solely contact approaches (38, 39). Moreover, histological screening has aided identification of cucurbit cultivars with reduced virus accumulation or limited vascular pathology, illustrating the value of tissue-level phenotyping in breeding programs (37). Future research should prioritize comparative histopathology of resistant and susceptible genotypes, linking traits such as restricted viral movement or rapid vascular cell responses to field-level resistance and informing durable, globally relevant management strategies (2).

5 Epidemiology and global distribution

The global distribution of begomoviruses infecting cucurbits is characterized by distinct geographical patterns that are increasingly being disrupted by the international movement of plant material and insect vectors. Historically, specific virus complexes were confined to particular continents: New World (NW) begomoviruses, such as Squash leaf curl virus (SLCV) and Cucurbit leaf crumple virus (CuLCrV), were prevalent in the Americas (43), while Old World (OW) viruses like Watermelon chlorotic stunt virus (WmCSV) and various squash leaf curl viruses dominated Asia, the Middle East, and Africa (44). This dichotomy has been increasingly diminished in the 21st century, primarily due to the pandemic spread of Tomato leaf curl New Delhi virus (ToLCNDV). Initially identified in tomatoes in the Indian subcontinent, ToLCNDV has undergone a remarkable geographical and host-range expansion. Distinct strains have now been reported across Southeast Asia, the Middle East, North Africa, and, critically, have become established in the Mediterranean Basin (15). Its introduction and spread into Europe, first confirmed in Spain in 2013, exemplify the biosecurity risks posed by global trade in plant material and the ubiquity of its Bemisia tabaci vector (45). The global distribution of these viruses, including their inferred centers of origin and documented geographical expansion pathways, is illustrated in Figure 3. The map highlights the emergence of ToLCNDV from the Indian subcontinent and its subsequent spread to Europe, the Middle East, and Africa, as well as the regional importance of CuLCrV in the Americas, SqLCPhV in Southeast Asia, and WmCSV in the Middle East. The epidemiological success of ToLCNDV is underpinned by its bipartite genome, which facilitates genetic reassortment and recombination. These processes generate novel viral lineages with altered virulence and an expanded host range, enabling the virus to infect over 11 cucurbit species as well as key solanaceous crops like tomato and potato, alongside numerous weed hosts (27). Beyond the major viruses associated with cucurbits, several other begomoviruses contribute to regional disease burdens. For instance, Tomato leaf curl Palampur virus (ToLCPMV) is increasingly reported infecting cucurbits in India and the Middle East, often in mixed infections with ToLCNDV (46). In Central America, Melon chlorotic leaf curl virus (MCLCuV) affects melon production, while in Southeast Asia, Squash yellow mild mottle virus (SYMMoV) and Loofa yellow mosaic virus (LYMV) pose threats to pumpkin and luffa cultivation, respectively (47).

Although ToLCNDV has received considerable attention in recent years, other regionally important begomoviruses continue to cause significant yield losses. In the Americas, SLCV and CuLCrV remain endemic pathogens of squash, melon, and pumpkin, whereas in the Middle East, WmCSV is a major constraint to watermelon and melon production, often occurring in complexes with other begomoviruses or betasatellites, which intensify symptom severity (17). In Asia, viruses such as SLCCNV and SLCuPV continue to threaten pumpkin and other cucurbit production (13, 48). The phylogenetic relationships among these major cucurbit-infecting begomoviruses are illustrated schematically in Figure 4, which highlights the three primary evolutionary lineages: Old World begomoviruses (including the ToLCNDV and SLCV clades) and two New World clades.

5.1 Evolutionary and recombination dynamics in cucurbit-infecting begomoviruses

The remarkable adaptability and global emergence of cucurbit-infecting begomoviruses are underpinned by high mutation and recombination rates that continually generate novel genetic variants with altered virulence, host range and geographical distribution (6, 7, 14). Understanding these evolutionary processes is essential for predicting future emergence events and designing durable disease-management strategies.

Recombination is particularly important in begomovirus evolution because circular ssDNA genomes readily undergo template switching between related, and even distantly related, viruses (49–51). In cucurbits, recombination has played a pivotal role in the emergence of several economically significant begomoviruses. For example, the bipartite genome of ToLCNDV shows multiple recombination breakpoints in both Rep (AC1) and CP (AV1) genes, which have been linked to host-range expansion and spread from the Indian subcontinent into the Middle East and Mediterranean Basin (26, 27). Similarly, the emergence of SLCV in the Americas has been associated with recombination between ancestral New World begomoviruses, yielding variants with enhanced adaptation to cucurbit hosts (44).

Pseudorecombination, the exchange of genomic components between compatible DNA-A and DNA-B segments of bipartite viruses, represents another important mechanism driving genetic diversity and host adaptation (6, 22). In cucurbits, pseudorecombination events between ToLCNDV and other begomoviruses have generated novel lineages with altered symptom severity and host range (27). The frequent co-infection of multiple begomoviruses in cucurbit fields—particularly in regions with high B. tabaci pressure—provides abundant opportunities for both recombination and pseudorecombination (14, 17). These processes, together with the modulatory effects of satellites, create a highly dynamic virus population in which new variants can rapidly arise and spread.

Despite these well-documented examples, detailed breakpoint analyses and population-level studies of cucurbit-infecting begomoviruses remain limited compared with those conducted for tomato-infecting begomoviruses. This disparity reflects the relatively recent recognition of many cucurbit-infecting species as major pathogens, the limited availability of full-genome sequences from diverse regions and hosts, and the computational complexity of robustly detecting recombination signals in circular ssDNA genomes (14, 48). Addressing these gaps through coordinated international sequencing and comparative-genomics efforts is essential for clarifying the evolutionary trajectories of these viruses and anticipating future emergence events. The dynamic threat landscape summarized in Figures 3, 4 underscores the need for ongoing genomic surveillance to track the appearance and movement of new lineages, particularly given the genetic flexibility conferred by high mutation rates, recombination and synergistic interactions with satellite molecules (14).

6 Detection methods: comparative evaluation

Accurate and timely detection of cucurbit-infecting begomoviruses is essential for disease surveillance, epidemiological investigations, seed-health testing and integrated disease management. A wide range of molecular diagnostic methods has been developed for major cucurbit-infecting begomoviruses, including conventional and quantitative PCR, isothermal amplification techniques such as loop-mediated isothermal amplification (LAMP) and recombinase polymerase amplification (RPA), next-generation sequencing (NGS) and, more recently, CRISPR-based assays. These approaches differ substantially in analytical sensitivity, turnaround time, cost, technical requirements and suitability for field deployment, and no single method is optimal in all contexts.

Laboratory-based PCR and qPCR remain the benchmark for specific, high-confidence diagnosis, particularly in seed-health laboratories and reference centers, but they require thermocyclers, reliable power and trained personnel. Isothermal methods such as LAMP and RPA can achieve sensitivities approaching those of PCR while using simpler equipment, making them attractive for decentralized or field-adjacent testing (48, 52). Portable NGS platforms (e.g. MinION) and emerging CRISPR-based assays offer unparalleled resolution and flexibility but are currently constrained by cost, infrastructure and the need for robust bioinformatics pipelines (20, 53). Table 1 summarizes representative examples of these methods for cucurbit-infecting begomoviruses, including target genes, limits of detection (LoD), assay duration, relative cost and field-deployability.

Table 1. Comparative performance of diagnostic methods for cucurbit-infecting begomoviruses: virus-specific targets, analytical sensitivity, and field applicability, LoD units – fg/µL and pg/µL: nucleic acid concentration for PCR-based and isothermal assays; ng/mL: antigen concentration for ELISA.

7 Management strategies and host resistance

Effective management of begomoviruses requires an integrated approach combining host resistance, vector control, and cultural practices. Host resistance remains the most sustainable strategy, yet most identified resistance sources are based on single genes, raising concerns about durability. Genetic resistance to ToLCNDV has been found in several cucurbit species, offering valuable resources for breeding. In melon (Cucumis melo), sources of resistance show reduced symptom severity and lower viral DNA accumulation (57). Similarly, cucumber (Cucumis sativus), pumpkin (Cucurbita moschata), and sponge gourd (Luffa cylindrica) genotypes with tolerance or resistance to ToLCNDV have been identified. Sáez et al. (58) evaluated a diverse collection of melon accessions for resistance to the Spanish isolate of ToLCNDV, identifying several with reduced symptom severity and lower viral DNA accumulation compared to susceptible controls.

Natural resistance to begomoviruses has been identified in both pumpkin and cucumber, and several loci and candidate genes have now been mapped and, in some cases, functionally validated (Verma et al., 2025; 57, 59). A summary of these host resistance sources, their genetic control, and candidate genes is presented in Table 2. In pumpkin (Cucurbita moschata), whitefly-mediated screening of twenty-five genotypes identified ‘Punjab Nawab’ (PVR-1343) as a resistant source against mixed infections of Squash leaf curl China virus (SLCCNV) and Tomato leaf curl New Delhi virus (ToLCNDV) (Verma et al., 2025). Resistance in ‘Punjab Nawab’ is digenic and recessive, controlled by two loci, qMI-sq/To7.1 on chromosome 7 and qMI-sq/To17.1 on chromosome 17, with qMI-sq/To7.1 explaining a major proportion of phenotypic variation (Verma et al., 2025; 60). Fine-mapping delimited qMI-sq/To7.1 to a 103-kb interval and led to the development of nine KASP markers, including Cmo4018182, which show high predictive power for resistance and are associated with a SYNTAXIN-121 candidate gene (Verma et al., 2025; 60).

Table 2. Host resistance sources and candidate genes for begomovirus resistance in cucurbits.

Gene-action analyses in intervarietal crosses (Punjab Nawab × MVSR-6711 and Punjab Nawab × P-135) revealed significant non-allelic (epistatic) interactions for percent disease index under SLCCNV, ToLCNDV and mixed infections, suggesting that recurrent selection in biparental progenies is suitable for accumulating additive resistance alleles (60). These findings support a polygenic, largely recessive inheritance model and emphasize the need for structured selection schemes to efficiently capture and pyramid begomovirus resistance in pumpkin breeding programs (60; Verma et al., 2025).

In cucumber (Cucumis sativus), the accession No.44 provides a well-characterized source of resistance to ToLCNDV isolates from the Mediterranean and Southeast Asia, including the aggressive isolate ToLCNDV-CsES (57, 59). This resistance is conferred by the Cy-1 locus on chromosome 1, which encodes CsRDR3, a DFDGD-class RNA-dependent RNA polymerase functioning in transcriptional gene silencing and orthologous to Ty-1/Ty-3 in tomato and Pepy-2 in capsicum (59). Map-based cloning narrowed Cy-1 to a 209-kb interval containing 24 predicted genes; virus-induced gene silencing of CsRDR3 abolished resistance, confirming its causal role (59). CsRDR3 from No.44 carries multiple amino acid substitutions and promoter deletions, and is expressed at higher levels than in susceptible cultivars, consistent with enhanced antiviral RNA silencing (59).

Additional QTLs contributing to ToLCNDV resistance have been identified on cucumber chromosomes 2, 6 and 7 (57, 59). A recessive QTL on chromosome 2 was first detected in Indian resistance sources and later associated with candidate genes including CsHSFA2 (heat shock factor A2), while QTL7 includes CsaV3_7G022160, encoding a CCCH-type zinc finger protein, as a leading candidate (57, 59). Together, these loci indicate that ToLCNDV resistance in cucumber is quantitatively controlled and involves RNA-silencing components (CsRDR3) alongside regulatory proteins such as zinc finger and heat shock factors, providing multiple targets for marker-assisted selection and pyramiding of resistance (57, 59).

7.1 Conventional and molecular breeding for resistance

Beyond the identification of natural resistance sources, significant progress has been made in understanding the genetic architecture and molecular mechanisms underlying begomovirus resistance in cucurbits. Conventional breeding approaches have historically relied on phenotypic screening of germplasm collections, followed by crossing and backcrossing to introgress resistance into elite cultivars (18, 58). However, the polygenic and often recessive nature of begomovirus resistance, as demonstrated in pumpkin (Verma et al., 2025) and cucumber (59), complicates phenotype-based selection and necessitates the use of molecular markers to accelerate breeding cycles.

Marker-assisted selection (MAS) has emerged as a powerful tool for introgressing resistance loci with greater precision and efficiency. In pumpkin, nine KASP markers developed from the fine-mapped qMI-sq/To7.1 locus, including Cmo4018182, now enable reliable selection of resistant progeny without time-consuming whitefly-mediated screening (Verma et al., 2025; 60). In cucumber, the Cy-1 locus and its causal gene CsRDR3 provide robust targets for MAS, with diagnostic markers already validated across diverse genetic backgrounds (59). Similarly, in melon, QTLs on chromosome 11 have been associated with reduced ToLCNDV accumulation, and linked markers are being refined for routine breeding application (58).

Looking ahead, gene pyramiding — the stacking of multiple resistance genes or QTLs into a single genotype — offers a promising strategy to enhance resistance durability. By combining Cy-1-mediated transcriptional gene silencing with additional QTLs on chromosomes 2, 6, and 7 in cucumber (57, 59), or by pyramiding qMI-sq/To7.1 and qMI-sq/To17.1 in pumpkin, breeders can reduce the probability of resistance breakdown by resistance-breaking virus strains. Genomic selection approaches, which use genome-wide marker data to predict breeding values, may further accelerate these efforts, particularly for quantitatively inherited resistance traits (Verma et al., 2025). Together, these advances are transforming cucurbit breeding from a phenotype-driven to a genomics-assisted discipline, enabling more rapid and durable deployment of begomovirus resistance.

Vector management is complicated by the rapid development of insecticide resistance in whitefly populations. Emerging technologies such as RNA interference and CRISPR/Cas systems show promise but face challenges related to field validation, regulatory approval, and public acceptance. A major gap in current research is the lack of region-specific management strategies that account for local virus–vector complexes. A summary of management strategies, their mechanisms, readiness levels, and references is presented in Table 3.

Table 3. Management strategies for cucurbit begomoviruses: mechanisms, examples, readiness level, and references.

8 Future research priorities

Despite substantial progress in understanding cucurbit begomovirus diversity, epidemiology and management, durable and sustainable strategies remain constrained by rapid viral evolution and recombination, expanding Bemisia tabaci populations, and climate change, even as advances in genomics, molecular diagnostics, artificial intelligence (AI) and resistance breeding open new opportunities. Future work should prioritize stacking multiple resistance loci through marker-assisted selection to enhance durability and broaden the genetic base of resistance. Major genes such as Cy-1/CsRDR3 can be combined with additional QTLs on chromosomes 2, 6 and 7 in cucumber using validated KASP markers, while qMI-sq/To7.1 and qMI-sq/To17.1 can be pyramided in pumpkin using the KASP marker Cmo4018182, with multi-location evaluation across diverse agro-ecological zones (57, 59; Verma et al., 2025; 60). Resistance present in wild cucurbit relatives (Cucurbita spp., Cucumis spp., Luffa spp.) should be systematically characterized via association mapping in at least 200 accessions to discover additional loci, and breeding strategies should, wherever feasible, prioritize recessive resistance mechanisms, which tend to be more durable than dominant resistance, with the aim of releasing the first pyramided varieties within the next five years. In parallel, surveillance and diagnostics must be strengthened: diagnostic platforms based on LAMP, RPA and CRISPR should be validated across multiple cucurbit-producing regions over several growing seasons, benchmarked against qPCR as the current gold standard (20, 52), and embedded within standardized international seed-health protocols developed in collaboration with ISTA, EPPO and APHIS, including certification thresholds (for example, no more than five infected seeds per 10,000) in view of documented seed transmission of CuLCrV and ToLCNDV (52, 55). Multiplex LAMP or RPA assays capable of simultaneously detecting ToLCNDV, SLCV, CuLCrV, WmCSV, SLCCNV and associated betasatellites should be designed and validated on large field sample sets to address the growing prevalence of mixed infections (17).

AI-enabled genomic surveillance and climate-informed forecasting will be critical cross-cutting tools. AI-driven predictive models should be developed to link genomic changes in viruses with epidemiological outcomes, enabling early warning of high-risk variants (64–67), while also simulating viral evolution under selection pressure to identify gene combinations that are more likely to remain durable against resistance-breaking strains and thereby potentially reducing resistance-breakdown risk by about 50% relative to single-gene varieties (68). AI-assisted metagenomic pipelines for high-throughput sequencing data should be applied to accelerate the discovery of novel satellites and to clarify their associations with specific virus–host combinations (34). In tandem, AI- and machine-learning-based, climate-informed forecasting systems should be trained on long-term datasets of whitefly population dynamics, weather variables, cropping patterns and disease incidence to generate short-term risk forecasts that support proactive management, with these tools co-designed with farmers through participatory approaches and delivered via simple interfaces such as SMS alerts or paper-based guides to ensure usability in low-resource settings (10, 64). Future disease hotspots should be modelled under climate-change scenarios by coupling climate projections with whitefly population dynamics and virus distribution data to identify regions at highest risk of emergence and guide targeted deployment of resistant cultivars and vector-management interventions (10). Sustained investment in long-term, multidisciplinary programs that integrate virology, vector biology, host genetics, climate science and AI will be essential to translate these advances in surveillance, diagnostics, resistance breeding and forecasting into practical, durable solutions for managing cucurbit begomoviruses. A conceptual framework integrating these future priorities in resistance breeding, surveillance and diagnostics, AI-driven forecasting, and climate-adaptive vector management is presented in Figure 5.

9 Conclusions

Begomoviruses represent a major and evolving threat to cucurbit production worldwide. While significant progress has been made in understanding their biology and management, critical gaps remain in epidemiology, detection, and resistance durability. This review highlights the need for a shift from descriptive studies to integrative and data-driven approaches. Addressing these challenges will be essential for developing effective and sustainable strategies to mitigate the impact of begomoviruses on global agriculture.

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Footnotes

Edited by: Sayanta Bera, Sister Nivedita University, India

Reviewed by: Muhammad Nawaz-ul-Rehman, University of Agriculture, Pakistan

Barinder Kaur, Punjab Agricultural University, India

Marzieh Shamshiri, University of Torbat Heydarieh, Iran