2025 年 13 巻 4 号 p. 30-48
Roses (Rosa spp.) are among the most widely cultivated ornamental plants globally. However, there have been increasing threats from a wide range of plant viruses. These viral pathogens are taxonomically diverse and include representatives from multiple virus families, infecting roses through varied transmission pathways such as insect vectors, grafting, and propagation materials. Over 26 distinct viruses affecting rose production have been identified globally. These include rose rosette virus, apple mosaic virus, prunus necrotic ringspot virus, and rose cryptic virus 1. Infections result in a wide spectrum of symptoms, including leaf mottling, deformation, growth abnormalities, and floral disruption, which significantly reduce the aesthetic and commercial values of rose plants. Some viruses cause severe systemic effects that lead to plant decline or death, while others establish latent infections that are symptomless. Recent developments in molecular detection techniques, particularly sequencing technologies, have expanded the discovery and characterization of rose-infecting viruses, which reveal complex virus communities within single plants. Mixed infections are increasingly common and often intensify symptom severity. Despite these advances, substantial knowledge gaps regarding the biological behavior, epidemiology, and long-term management of many rose viruses. This review presents a global synthesis of the current understanding of rose-infecting viruses, including their taxonomic classification, method of transmission, geographical distribution, and symptomatic manifestations. It also discusses diagnostic challenges in virus detection, emerging threats linked to global trade, and the imperative for integrated disease management strategies.
Roses (Rosa spp.) are among the most economically and culturally significant ornamental plants worldwide. Their cultivation spans multiple industries, including floriculture, landscaping, and perfumery, contributing substantially to global and local economies. The diversity of roses has placed them as essential components in horticultural practices and ornamental breeding programs. Roses also hold cultural value and serve as national symbols. For instance, the United States officially designated the rose as its national flower in 1986 [1]. In Bulgaria, roses play a crucial role in the production of rose oil, which is a major export commodity [2]. Similarly, Iran is known as the world’s largest producer of rosewater [3].
Despite their value, rose cultivation has been increasingly infested by viral diseases that compromise plant health, productivity, and quality. These viral infections have emerged as critical concerns in both the commercial and private rose-growing industry.
1.2 Economic impactAccording to the commercial analysis by Grand View Research [4], the rose industry significantly contributes to the global economy, with the cut flower market valued at approximately USD 37.45 billion in 2023. In 2014, rose production in the US involved 1,808 growers who cultivated approximately 36.6 million plants, generating around USD 203.5 million [5]. Data from the Green Industry Research Consortium’s National Survey [6] revealed that roses made up 3% of total sales across 18 horticultural crop categories, which collectively contributed USD 25.9 billion. The rose sector alone was estimated to contribute nearly USD 777 million to the US economy. About 65% of roses were sold through retail channels, while the remaining 35% were distributed via landscape services [6]. According to Vineland Research and Innovation Centre [7], in terms of regional economic value, the rose landscape market in Canada was valued at USD 149 million, while in the US, it was valued at USD 41 million in 2015 [5].
However, viral diseases cause substantial economic challenges to the industry, which affects production, trade, and the aesthetic value of roses. Rose rosette disease (RRD) has led to revenue of up to 25% for US rose production businesses [8]. Annual losses are estimated at approximately USD 10 million due to decreased sales and increased management costs [9]. Aside from direct financial losses, it has severely affected landscape aesthetics and commercial nurseries, causing the removal and replacement of infected plants, which has escalated costs. The high labor expenses associated with RRD management impose additional economic burdens on growers [10].
On the other hand, a single symptomatic leaf of rose mosaic disease (RMD) infected rose can result in the rejection of entire shipments for wholesale or retail rose producers, which leads to increased costs due to the need for replanting with healthy roses [11, 12]. An economic analysis estimated that a 5% decline in sales due to RMD could result in a total economic impact of approximately USD 28.4 million, involving both direct financial losses and broader economic repercussions across associated sectors [13]. Similar economic challenges have been observed in other rose-producing regions, where losses from RMD-related reduced vigor and aesthetic defects in ornamental roses have led to lower marketability and increased production costs [9]. Infected propagation materials and grafting practices have also contributed to hidden economic losses, as affected plants often show symptoms only after distribution, leading to customer dissatisfaction and long-term reputational damage for producers [11]. In countries where roses contribute to the floral industry, outbreaks of viral diseases can disrupt supply chains, decrease export revenues, and necessitate stringent quarantine measures that further strain national economies [11].
Given the significant cultural, economic, and ecological importance of roses, addressing the emerging threats posed by viral diseases is essential. Understanding the epidemiology, transmission, and economic impact of these viruses is crucial for sustaining the global rose industry and mitigating their effects. This review provides a comprehensive overview of the current state of knowledge on rose viral diseases worldwide, including their symptoms and detection methods.
In synthesizing existing research on rose viral diseases, this review aims to provide information and guidance to future studies focused on disease mitigation. Also, a deeper understanding of rose viral diseases will contribute to the development of sustainable and innovative solutions to ensure long-term health and productivity of the global rose industry.
To date, 26 viruses have been reported to infect roses. Among these, this review focuses on 14 well-characterized viruses that are consistently associated with infections in roses, supported by molecular or serological detection, and taxonomically validated. This section presents a systematic overview of rose-infecting viruses, including their taxonomic classification, method of transmission, global distribution, and symptomatic manifestations that define their impact on global rose health.
Figure 1 presents the distribution map of rose viruses discussed in this review. In addition, Table 1 provides a summary of each virus, detailing its name, genus/family, transmission method, affected rose species or cultivars, and associated symptoms.
2.1 Apple mosaic virus (ApMV)Apple mosaic virus (ApMV), a member of the genus Ilarvirus (Bromoviridae family), is widely distributed and infects over 65 woody plant species, including apple, pear, apricot, peach, plum, strawberry, hazelnut, and roses [14]. Its genome comprises three single-stranded RNA molecules: RNA 1 and RNA 2 each contain a single open reading frame (ORF) [15], while RNA 3 has two ORFs encoding the movement protein and coat protein [16, 17]. The coat protein is expressed from a subgenomic RNA 4 [17].
Symptom expression varies significantly among rose cultivars and is influenced by environmental conditions [18]. Common symptoms include chlorotic bands, ringspots, wavy lines, yellow vein banding, oak-leaf pattern, and general mosaic [18]. Infected plants exhibit reduced vigor, lower flower production on shorter stems, poor transplant survival, and increased susceptibility to frost [19].
ApMV is primarily transmitted through root grafting and infected vegetative propagation material [19]. While mechanical inoculation can experimentally transmit the virus to herbaceous plants, there is no evidence of transmission via seeds, pollen, or insect vectors [19].
In Poland and Belarus, molecular characterization of ApMV isolates from roses revealed considerable genetic variability, suggesting frequent mutations that enhance adaptability to diverse hosts and environments [18]. In Turkey, ApMV was detected in R. damascena, often co-infecting with Prunus necrotic ringspot virus (PNRSV) and Arabis mosaic virus (ArMV), posing challenges for virus management in commercial rose production [20]. In the UK, ApMV was identified as a major cause of RMD, with its widespread distribution linked to infected propagation materials used in nurseries [21]. ApMV was detected in roses in New York, causing chlorotic patches, puckering, and leaf distortion [22]. Further studies confirmed that the virus spreads predominantly through vegetative propagation and infected pollen [23, 24]. In a study by Ortega-Acosta et. al [25], ApMV was detected in Mexico, co-infected with another rose virus under genus Carlavirus.
2.2 Arabis mosaic virus (ArMV)ArMV, a member of the Secoviridae family and the Nepovirus genus, affects a wide range of plants, including strawberries, hops, grapevines, raspberries, rhubarb, and elderberry [26]. It comprises two single-stranded, positive-sense RNAs, designated RNA-1 and RNA-2. The RNA-1-encoded polyprotein (P1) undergoes proteolytic processing to generate six proteins: X1 (a protein of unknown function), X2 (a putative protease cofactor), NTB (a nucleotide triphosphate-binding protein), VPg, Pro (a 3C-like protease), and Pol (an RNA-dependent RNA polymerase) [24]. The RNA-2-encoded polyprotein (P2) is cleaved in trans by the RNA-1 protease, producing three functional proteins: the homing protein (2A), the movement protein, and the coat protein, all of which play essential roles in viral replication and systemic infection [27].
Transmission of ArMV occurs through multiple routes, including nematode vectors, particularly Xiphinema diversicaudatum, as well as mechanical means such as pruning tools, grafting, and, to a lesser extent, seed transmission [28].
In Turkey, studies on R. damascena revealed symptoms such as ring spots, mosaic chlorosis, and weakened root systems, which pose a significant threat to the rose oil industry [20]. Similarly, in Florida, hybrid tea roses infected with ArMV exhibited poor flowering, premature leaf drop, and increased vulnerability to environmental stress [29]. In England, surveys have confirmed that ArMV induces severe leaf distortion and mosaic patterns, diminishing the commercial value of roses [30]. Additionally, studies in the UK have identified ArMV as a primary causal agent of RMD, further highlighting its detrimental effects on rose cultivation [31].
In Iran, ArMV has been found co-infecting roses alongside PNRSV and Cucumber mosaic virus (CMV), contributing to chlorotic mottling, leaf distortion, and stunted plant growth in rose plantations [32]. Further investigations have reported severe leaf discoloration, necrotic lesions, and weakened root systems, significantly impacting the economic viability of infected plants [33]. Efforts to mitigate ArMV infections in roses have focused on chemo-thermotherapy and microshoot tip tissue culture, both of which have demonstrated promise in eliminating the virus from plantlets [33].
2.3 Cucumber mosaic virus (CMV)CMV belongs to genus Cucumovirus (family Bromoviridae) and is composed of three single-stranded, positive-sense RNAs [34]. Each RNA segment is encapsidated separately within icosahedral virions, which are approximately 29 nm in diameter and consist of 180 identical coat protein subunits [34].
CMV is well-known for its broad host range, infecting over 1,000 plant species across more than 85 plant families including cucumber, squash, pepper, spinach, lettuce, celery, tomato, and bean [34, 35]. The virus is transmitted in a nonpersistent manner by at least 75 species of aphids [36]. While certain mutations in the coat protein have been identified that inhibit aphid-mediated transmission [37], CMV exhibits minimal vector specificity. Beyond aphid transmission, CMV can also spread via seed dispersal and through the parasitic plant Cuscuta spp., where the virus is capable of replication [38].
A study by Vazquez-Iglesias et al. [30] reported the first detection of CMV in roses in the UK. This survey revealed that CMV coexisted with tomato spotted wilt virus (TSWV) and Ilarviruses, resulting in stunted growth, delayed blooming, and reduced flower size. PCR-based detection methods and electron microscopy were employed to confirm the presence of CMV in rose tissues.
2.4 Prunus necrotic ringspot virus (PNRSV)PNRSV is a tripartite, single-stranded, positive-sense RNA genome belonging to genus Ilarvirus and family Bromoviridae [39]. RNA1 and RNA2 are monocistronic, encoding replication-associated proteins, while RNA3 is bicistronic, encoding the movement and coat protein via a subgenomic RNA4. The 5’ ends of these RNAs are capped, and the 3’ ends form conserved secondary structures essential for replication [39, 40]. PNRSV exhibits a broad host range, affecting species within the genus Prunus, such as cherries, peaches, plums, and almonds, as well as ornamental plants like roses [41, 42].
Some rose cultivars grown in the field do not exhibit symptoms of PNRSV infection, while others display symptoms like line patterns, ringspots, or leaf yellowing [19, 43, 44, 45]. Infected roses tend to flower earlier than healthy plants but produce malformed flowers. The virus leads to significant reductions in flower number and size, as well as in shoot number, size, and length [46, 47, 48].
One of the primary methods of transmission of PNRSV in roses is mechanical transmission, occurring when infected plant materials, such as cuttings or grafts, are handled, leading to the transfer of the virus to healthy plants. Studies have shown that PNRSV can be mechanically transmitted to herbaceous hosts, which can then serve as reservoirs for the virus, complicating control efforts in rose cultivation [49]. This method is particularly relevant in commercial rose production, where propagation techniques often involve the use of tools that can inadvertently carry the virus from one plant to another [50].
PNRSV was first reported in roses in Europe, causing symptoms such as leaf mottling, ring spots, and yellow netting. Subsequent studies confirmed the virus’s widespread presence in Europe, with isolates from France being classified into the PNRSV-PV32 group based on sequence analysis [51, 52, 53]. In Poland, PNRSV isolates were found to share genetic similarities with other European strains [51].
Studies in New York indicated that PNRSV was one of the most prevalent viruses affecting roses [22]. This finding was supported by a survey that explored the virus’s variability across different rose cultivars and geographical locations [49]. In 2011, a biological and molecular characterization of PNRSV isolates from three distinct rose cultivars confirmed its presence in the US [51]. In South America, PNRSV was molecularly characterized in Brazil, revealing significant genetic diversity within the virus [54, 55].
In the Middle East, PNRSV has been detected in Lebanon, where it causes RMD symptoms [56], and in Iran, where mixed infections with ArMV have been reported and were predominantly found in red rose varieties such as Rosa damascena, R. chinensis, R. canina, and R. multiflora [32]. Additionally, Turkey has confirmed the presence of PNRSV, as have studies in Jordan [57, 58].
In Asia, PNRSV has been reported in India [59] and Japan [60], while in China, a study on China roses (R. chinensis) found that PNRSV was the only virus consistently detected in symptomatic plants [61].
PNRSV is also found in New Zealand, where a comprehensive nationwide survey revealed that 22% of the 89 rose samples tested were infected with the virus [62].
2.5 Rose cryptic virus 1 (RCV-1)Rose cryptic virus 1 (RCV-1) is a tripartite double-stranded RNA (dsRNA) virus that belongs to genus Deltapartitivirus and family Partitiviridae [63]. Members of this genus are characterized by their infection of plants and possess a bipartite genome structure. However, RCV-1 is notable for its tripartite genome, comprising three monocistronic dsRNA segments [63].
The largest segment, dsRNA1, encodes the RdRP, essential for viral replication. The second segment, dsRNA2, encodes the major capsid protein, which forms the viral capsid [64]. The third segment, dsRNA3, also encodes a protein similar in size to the capsid protein, but its exact function remains undetermined [64]. This tripartite genome organization distinguishes RCV-1 from other deltapartitiviruses, which typically have only two genomic segments [63]. Phylogenetic analyses indicate that RCV-1 is closely related to other plant-infecting partitiviruses, forming a distinct clade within the family Partitiviridae [63].
RCV-1 is primarily known to infect roses and is often asymptomatic [63]. However, some studies have reported associations between RCV-1 and symptomatic conditions. For instance, RCV-1 has been detected in roses exhibiting spring dwarf symptoms [64] and in plants affected by RRD [65]. In these cases, RCV-1 was found alongside other viruses, suggesting that while RCV-1 alone may not induce symptoms, it could play a role in disease complexes when co-infecting with other pathogens [65].
RCV-1 is primarily transmitted vertically in roses through seeds and pollen. This mode of transmission ensures the virus persists within rose populations as it passes from parent plants to their progeny [64].
RCV-1 was first reported in the US in R. multiflora [65]. Subsequent research in Canada identified RCV-1 in cultivated roses, including ‘Goldener Olymp’ and ‘What a Peach’ [66]. In New Zealand, a comprehensive survey revealed a high prevalence of RCV-1, with approximately 48% of tested rose samples found to be infected [62]. Similarly, in the United Kingdom, high-throughput sequencing (HTS) techniques confirmed the presence of RCV-1 in rose samples [30]. Studies in Turkey further documented the occurrence of RCV-1 across multiple regions [57]. In Asia, it was detected in R. hybrida plants in Taiwan, particularly those exhibiting mosaic symptoms [28].
2.6 Rose leaf curl virus (RoLCuV)Rose leaf curl virus (RoLCuV), a member of the family Geminiviridae [67] and genus Begomovirus, affects various plant species such as pomegranate [68] and particularly those within the Rosa genus. Genome analyses have confirmed its monopartite structure and revealed a high nucleotide sequence identity with other isolates, reinforcing its classification as RoLCuV [69].
RoLCuV was first identified in India, where R. indica exhibited symptoms such as leaf curling, distortion, and dwarfing [69]. The virus has also been reported in R. chinensis in Pakistan, where infected plants displayed severe stunting and leaf curling [70].
RoLCuV has a broad host range and can interact with betasatellites, small DNA molecules that enhance viral pathogenicity, potentially influencing symptom severity and promoting disease synergy [71]. Furthermore, RoLCuV is transmitted by whiteflies, a key vector responsible for its spread.
2.7 Rose rosette virus (RRV)Rose rosette virus (RRV) is a negative-sense, single-stranded RNA virus classified under the genus Emaravirus within the family Fimoviridae [72]. RRV possesses a multipartite genome composed of seven distinct RNA segments, each encoding proteins essential for replication, movement, and pathogenicity [73]. RNA1 encodes the RNA-dependent RNA polymerase (RdRp), which facilitates viral genome replication, while RNA2 encodes a glycoprotein precursor involved in virion assembly and vector transmission. RNA3 encodes the nucleocapsid (N) protein, responsible for encapsidating viral RNA, whereas RNA4 encodes a putative movement protein that enables systemic infection within the host [73]. The functions of RNA5, RNA6, and RNA7 are hypothesized to play roles in host-virus interactions and pathogenicity, although the high plains wheat mosaic virus (HPWMoV) RNA7 and RNA8 are suggested to be silencing suppressor proteins [74].
RRV has only been detected in roses. It triggers a range of symptoms in infected roses, which can differ depending on the cultivar and environmental factors. Early signs of infection include the rapid growth of new shoots, often accompanied by red pigmentation. While certain rose cultivars naturally exhibit red hues in young growth, RRV-infected plants maintain this discoloration as the leaves mature, unlike healthy plants, where the redness fades to green [75, 76, 77]. One of the most prominent symptoms of RRV is the development of “witches’ brooms,” where small, malformed branches cluster densely at a single point. The leaves within these clusters tend to be stunted and deformed [73, 78]. Infected stems can show abnormal proliferation of thorns, which start out soft and flexible but harden as the infection progresses and serve as a distinguishing feature of RRV infection [76, 77]. Another symptom commonly observed in infected roses is floral deformities, where flowers may appear misshapen, discolored, or fail to open entirely. In severe cases, the plant’s ability to flower can be drastically reduced or completely absent [76, 77].
As the disease advances, roses experience leaf drop, dieback of stems, and a general loss of vigor, leading to death within two to four years. Additionally, infected plants tend to have lower cold tolerance, making them more susceptible to frost damage [76, 77]. In the early stages of infection, RRV may not display visible symptoms or may show only minimal signs [77], with an asymptomatic period lasting from 30 to 146 days after transmission [79]. By the time the symptoms become apparent, the virus may have already spread to nearby plants [78].
Phyllocoptes fructiphilus, an eriophyid mite, is the primary vector responsible for the transmission of RRV [79]. Early studies established that this transmits the virus through its feeding behavior, which involves piercing plant tissues to access the phloem [80, 81]. The ability of RRV to persist and potentially replicate within the mite vector complicates control strategies, as infected mites can spread the virus to healthy plants during feeding [80, 82]. Advancements in research have further clarified the role of P. fructiphilus in RRV transmission, confirming both its high efficiency as a vector and the environmental conditions that influence its activity [80, 81]. Over the years, increasing attention has been given to the impact of environmental factors on the virus’s transmission dynamics. Studies indicate that variables such as temperature, humidity, and overall plant health significantly affect mite behavior and the likelihood of virus spread [80]. For instance, elevated humidity levels have been associated with increased mite activity, thereby enhancing virus transmission rates; P. fructiphilus populations were highest at a moderate relative humidity (60%), symptom expression and severity of RRD were significantly greater under high humidity (95%) compared to low humidity (20%) [83].
RRV was first identified in the 1940s in Canada [84]. By the 1960s, the virus began spreading across the US and has since been confirmed in 36 states [77, 85, 86, 87]. Since its emergence, RRV has infected a wide range of roses across North America. The invasive multiflora rose (Rosa multiflora), highly susceptible to RRV, has played a crucial role in virus transmission by serving as a reservoir. Additionally, cultivated roses, including hybrid teas, floribundas, climbers, miniatures, and heritage varieties, have also been affected [88]. In 2017, RRV was detected in two ornamental gardens in India. Infected plants exhibited characteristic symptoms such as leaf curling and crumpling, flower deformation, leaf distortion, and persistent red pigmentation on mature leaves. While the specific rose species were not documented, the introduction is suspected to have occurred through the importation of a R. multiflora hybrid breeding line from the US [89].
2.8 Rose spring dwarf-associated virus (RSDaV)Rose spring dwarf-associated virus (RSDaV) is classified within the genus Luteovirus and family Luteoviridae. The virus genome is composed of dsRNA approximately 5,808 nucleotides [90, 91]. Phylogenetic analysis places RSDaV in close proximity to other members of the Luteovirus genus, showing considerable sequence similarity in both the RNA-dependent RNA polymerase and coat protein regions [90].
RSDaV exhibits a limited range of hosts, notably various species within the Rosa genus. Infected plants exhibit distinct symptoms, including yellow vein chlorosis, stunted growth, and leaf curling, all of which align with the characteristics described in previous studies of rose spring dwarf disease [90, 91, 92]. The yellow vein chlorosis is particularly indicative of a disruption in the plant’s vascular system, a common feature of luteovirus infections [91, 92]. In addition, plants may experience dwarfing, accompanied by leaf curling and distortion, which can significantly affect the aesthetic value of the roses and their commercial viability [90, 91, 92]. Mottling and necrotic spots have also been noted in some cases, particularly when RSDaV co-infects with other viruses such as RCV-1. The interaction between multiple viral infections can exacerbate disease symptoms, leading to more severe manifestations [93]. RSDaV is transmitted by rose-grass aphid (Metapolophium dirhodum) and yellow rose aphid (Rhodobium porosum), with a host range that spans both monocotyledonous and dicotyledonous plants [90].
RSDaV was first identified in the US in cultivated roses exhibiting symptoms typical of rose spring dwarf disease, including rosetting of new growth and vein clearing [90]. In Chile, RSDaV was detected in roses exhibiting yellow vein chlorosis, and the virus was also found in aphids collected from infected plants, suggesting that aphids may act as potential vectors [92]. In the UK, RSDaV was found in Rosa spp. samples exhibiting mottling, yellow or white patching, and thin-textured leaves [94]. In China, the virus was detected in R. chinensis [95]. Similarly, in Taiwan, RSDaV was identified in Rosa spp. plants showing symptoms characteristic of RMD, such as mosaic patterns, line patterns, and ringspots on leaves [28]. RSDaV was also found in Turkey along with other viruses infecting rose [57].
2.9 Rose virus A, B and C (RVA, RVB, RVC)The Carlavirus genus encompasses several species, including Rose Virus A (RVA), Rose Virus B (RVB), and Rose Virus C (RVC), which are distinguished by their genomic characteristics and exhibit host specificity towards roses.
RVA, the first Carlavirus reported to infect Rosa wichuraiana, was initially identified in the US. Its complete genome, spanning 8,849 nucleotides, comprises six ORFs encoding the replicase, triple gene block proteins, coat proteins, and nucleic acid-binding protein [38]. Phylogenetic analysis places RVA within the Carlavirus genus, family Betaflexiviridae. RVA was detected in ‘Queen Elizabeth’, and ‘Double Delight’ rose cultivars that exhibited no visible symptoms [96]. This finding suggests that RVA can establish asymptomatic infections in roses and has the potential for undetected viral presence.
RVB was identified in the ‘Out of Yesteryear’ rose cultivar, also in the US. Its genome, consisting of 8,825 nucleotides, encodes six predicted proteins, including the replicase, triple gene block proteins, coat proteins, and nucleic acid-binding protein [97]. Comparative sequence analysis reveals that RVB shares 75% and 78% amino acid identity with RVA in the replicase and coat protein, respectively, supporting its classification as a distinct species within the Carlavirus genus [97]. Additionally, an 8,842-nucleotide contig with 90.6% identity to a US RVB isolate was reported in Mexico, where it was detected in mixed infections with ApMV [25]. Infected rose plants exhibited symptoms such as mosaic patterns, vein yellowing, chlorotic line patterns, and interveinal chlorosis, suggesting a potential role for RVB in symptom expression in coinfected hosts.
Further studies led to the characterization of RVC in specific strains of R. chinensis. RVC exhibits a relatively low incidence rate in surveyed rose populations [98]. Its complete genome, 8,386 nucleotides in length, contains five ORFs. Phylogenetic analysis clusters RVC within the Carlavirus genus yet displays notably low nucleotide sequence identity with other Carlavirus members (ranging from 48.8–52.1% in the replicase gene and 40.4–45.9% in the coat protein gene), suggesting that RVC represents a distinct and atypical species [98]. The low detection frequency of RVC (5.4%) in surveyed roses may indicate a restricted distribution or recent emergence of this virus [98].
2.10 Rose yellow mosaic virus (RoYMV)Rose yellow mosaic virus (RoYMV) belongs to the Roymovirus genus within the Potyviridae family, primarily infecting roses. Its genome comprises 9,508 nucleotides, excluding the 3′ poly(A) tail, and contains a single ORF that encodes a polyprotein of 3,067 amino acids.
Infected roses exhibit symptoms such as yellow mosaic patterns, premature leaf senescence, severe necrotic cane lesions and dark-brown rings on canes [99, 100]. RoYMV has been experimentally transmitted via grafting from infected to virus-free rose cultivars [99]. Symptoms typically emerge in new growth within 4–6 weeks post-inoculation, and the presence of RoYMV in symptomatic plants has been confirmed through molecular detection techniques [99].
In the US, RoYMV has been identified in several rose cultivars, including ‘Ballerina’, ‘Buff Beauty’, ‘Mozart’, ‘Cornelia’, ‘Nastarana’, ‘Dorothy Perkins’, and ‘Sir Thomas Lipton’ in New York, as well as ‘June Bride’ and ‘Captain Harry Stebbings’ in Minnesota [99, 100]. In 2016, RoYMV was isolated from the ‘Irish Mist’ rose cultivar in Tokyo. The Japanese isolate exhibited high similarity to a strain previously identified in Minnesota; however, it contained the 6K1 protein region, which was absent in the Minnesota strain [101]. The 6K1 protein is essential for replication in potyviruses, but its function in RoYMV is unclear. The widespread occurrence of the Minnesota strain, which lacks the 6K1 cistron, suggests that 6K1 is not required for replication or pathogenicity in RoYMV. Its presence in the Japanese strain will be further studied.
2.11 Rose yellow vein virus (RYVV)Rose yellow vein virus (RYVV) belongs to the genus Rosadnavirus and family Caulimoviridae and is known to predominantly infect roses. The viral genome consists of a non-covalently closed, circular, dsDNA molecule spanning 9,314 base pairs, making it one of the largest genomes within the Caulimoviridae family [102]. RYVV harbors eight ORFs, with ORFs 1, 2, and 3 exhibiting 22–33% amino acid sequence similarity to known Caulimoviridae members. The remaining ORFs lack significant homology to any known viruses, suggesting potential novel functional elements [102, 103]. RYVV virions are non-enveloped and possess icosahedral symmetry, with diameters ranging from approximately 42–45 nm which aligns with other Caulimoviridae members characterized by isometric virions [102].
First identified in the US, RYVV was associated with vein yellowing symptoms in cultivated roses, and transmission studies revealed that the virus is graft transmissible [100]. Subsequent reports confirmed RYVV presence in New Zealand, where it was detected in two rose cultivars, ‘Leda’ and ‘Zephirine Drouhin’ [104]. The ‘Leda’ cultivar, co-infected with PNRSV, exhibited vein yellowing and chlorotic mottling at the leaf apex, symptoms not typically associated with PNRSV alone, suggesting a potential role of RYVV in symptom development. In contrast, ‘Zephirine Drouhin’ displayed leaf curling and mottling, but as these symptoms were observed in both RYVV-positive and -negative samples, a direct association with RYVV remains uncertain [105].
In 2018, RYVV was reported in Turkey, its first detection in Europe and Asia [105]. Infected roses exhibited characteristic symptoms, including vein banding and central vein chlorosis. Molecular analyses confirmed the presence of RYVV, with Turkish isolates displaying 96–97% nucleotide identity to those from the US and New Zealand [100, 104, 105].
2.12 Strawberry latent ringspot virus (SLRSV)Strawberry latent ringspot virus (SLRSV) belongs to genus Stralarivirus (family Secoviridae) and is a positive-sense single-stranded RNA virus with a bipartite genome consisting of two linear RNA molecules [106]. Originally identified in Scotland over fifty years ago, SLRSV has since been detected in strawberry, raspberry, cherry, plum, grapes, peaches, asparagus, and celery [107]. In addition, it was detected in various rose cultivars, causing symptoms such as chlorotic mosaics and leaf flecking [31, 107, 108]. The severity of these symptoms varies from asymptomatic infections to severe manifestations, highlighting the virus’s variable pathogenicity depending on host species and environmental conditions [30, 31]. Research indicates that SLRSV transmission is primarily mediated by the nematode vector Xiphinema diversicaudatum. Numerous studies have confirmed this association, underscoring the role of nematode populations in influencing the prevalence of the virus in rose plantations [109, 110, 111].
Geographically, SLRSV is prevalent in the UK, where it is frequently associated with rose cultivation in glasshouses [30]. Recent investigations utilizing HTS techniques have detected SLRSV in more localized regions, confirming its presence in both standard garden roses and protected environments such as nurseries [112]. Moreover, the occurrence of SLRSV in roses is part of a broader agricultural concern, as the virus is often found co-infecting plants alongside other pathogens like PNRSV and ArMV, which can exacerbate plant health issues [30].
2.13 Mixed viral infectionsMixed infections involving multiple viruses are increasingly recognized as a common phenomenon in roses. One of the most frequently observed combinations is PNRSV and ApMV, often associated with RMD complexes [19, 49, 113]. ArMV has also been detected alongside ApMV, CMV, and PNRSV, particularly in R. damascena cultivated in Iran [32] and Turkey [20], where mixed infections were shown to reduce plant vigor and flower production. RCV-1, although largely asymptomatic, has been found co-infecting with RSDaV [64, 93]. Additionally, RVA has been identified in mixed infections with ApMV in the US [25].
These co-infections are biologically significant as they can intensify disease symptoms, alter the expected symptoms of single-virus infections, and interfere with accurate diagnosis. In some cases, asymptomatic viruses like RCV-1 may modulate the host response, making disease expression more severe or inconsistent. Furthermore, mixed infections can complicate disease management, as infected propagation materials may carry multiple viruses, some of which remain asymptomatic but are still transmissible.
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Enzyme-linked immunosorbent assay (ELISA) was introduced to plant virology in the 1970s and became a preferred diagnostic due to its affordability, high sensitivity, and quantitative capabilities [114]. By leveraging antigen-antibody interactions to detect viral coat proteins, ELISA offered a specific and high-throughput alternative for plant virus detection. Studies by Barbara [115] and Thomas [116] demonstrated its effectiveness in screening for PNRSV and SLRSV in rose cultivars. Even to this date, advances in ELISA-based techniques continue to arise. The double antibody sandwich ELISA (DAS-ELISA) has been widely employed in research on various rose-infecting viruses. Modarresi et al. [33] utilized DAS-ELISA to assess the efficacy of chemotherapy and thermotherapy treatments in eliminating viral infections in rose plantlets, demonstrating its reliability in evaluating eradication strategies. Another study employed DAS-ELISA to detect both single infections of PNRSV and ApMV, as well as mixed infections of ApMV+PNRSV [113].
3.1.2 Immunostrip testsThis method functions as a lateral flow assay (LFA), where virus-specific antibodies bind to viral antigens in plant sap, producing a visible test line. Al Rwahnih et al. [117] employed immunostrip tests using commercially available LFA kits to detect PNRSV and ApMV. However, this method was less effective in identifying newly emerging or low-concentration viruses, which were subsequently detected using HTS. Sensitivity was also lower compared to RT-PCR, particularly for early-stage infections. Consequently, while useful for rapid field screening, immunostrip tests do not serve as substitutes for advanced molecular methods.
3.2 Molecular diagnostic techniques 3.2.1 Reverse transcription polymerase chain reaction (RT-PCR)Reverse transcription polymerase chain reaction (RT-PCR) is a widely used molecular technique that involves reverse transcription of RNA into complementary DNA (cDNA), followed by PCR amplification. Babu et al. [118] developed a highly sensitive TaqMan real-time RT-PCR assay for RRV detection, significantly improving diagnostic precision in cultivated roses. Their study highlighted the importance of tailored primer sets in enhancing detection sensitivity and reliability. Similarly, Dobhal et al. [77] investigated various RT-PCR chemistries for RRV detection, emphasizing the role of primer specificity in ensuring consistent and accurate results across conventional RT-PCR and quantitative reverse transcription polymerase chain reaction (RT-qPCR) methodologies.
3.2.2 Multiplex reverse transcription polymerase chain reaction (RT-PCR)Multiplex RT-PCR has emerged as an efficient method for the simultaneous detection and amplification of multiple viral targets in a single reaction tube, significantly reducing reagent consumption and processing time. It is particularly used in diagnosing mixed infections in roses. A study by Yang et al. [119] established a multiplex RT-PCR system capable of detecting rose viruses. The assay was designed using primers targeted to highly conserved regions of the coat protein and polyprotein genes, with optimization of primer and cDNA concentrations, as well as cycling conditions.
3.2.3 Quantitative reverse transcription polymerase chain reaction (RT-qPCR)Quantitative reverse transcription polymerase chain reaction (RT-qPCR) has further advanced diagnostic capabilities by enabling real-time quantification of viral loads, providing insights into infection severity. Babu et al. [120] successfully utilized qPCR to quantify viral loads in infected rose samples.
Additionally, recent advances in molecular diagnostics have introduced reverse transcription-recombinase polymerase amplification (RT-RPA) as an alternative approach for RRV detection. This technique allows for rapid and sensitive detection without the need for sophisticated thermal cycling equipment, making it a promising tool for field-based diagnostics [120].
3.2.4 Loop-mediated isothermal amplification (LAMP)Loop-mediated isothermal amplification (LAMP) is an isothermal amplification method known for its high specificity and efficiency. It employs a DNA polymerase and a set of 4–6 oligonucleotides designed to recognize multiple target regions [121]. The results can be visualized through colorimetric or fluorescence-based detection methods, such as Hydroxynaphthol Blue or SYBR Green I [121, 122]. Since LAMP alone detects only DNA, reverse transcription LAMP (RT-LAMP) is employed for RNA viruses by converting RNA into cDNA before amplification.
Salazar et al. [123] successfully detected RRV using RT-LAMP in both symptomatic and asymptomatic rose samples. Additionally, Wani et al. [59] employed RT-LAMP with specific primer sets for PNRSV and ApMV detection.
3.2.5 High-throughput sequencing (HTS)High-throughput sequencing (HTS) allows for the simultaneous sequencing of millions of DNA fragments, providing comprehensive genomic data [124]. A notable application of HTS in rose virus detection was the identification of RCV-1 in the UK, where 251 rose samples were analyzed using HTS, followed by the development of an RT-qPCR assay for targeted virus detection [93]. Further studies utilizing HTS have identified multiple viruses in rose plants, including well-known pathogens such as ApMV and PNRSV [113].
Moreover, HTS enhances the understanding of viral population structures and dynamics. Studies on RRV using sequencing techniques have revealed low genetic diversity among viral isolates, offering insights into virus evolution and epidemiology [73].
4. ConclusionThe rose industry is increasingly affected by a wide array of viral pathogens all over the world. These major viruses significantly impact plant health, quality, and productivity. The transmission of these viruses occurs through multiple vectors, including eriophyid mites, aphids and mechanical tools, with propagation materials being one of the most common causes for the spread of virus. The resulting viral infections lead to symptoms such as leaf chlorosis, distortion, and reduced flowering, which can drastically lower the value of roses.
The economic impact of these viral infections affects multiple sectors of the rose industry. Viral diseases lead to significant yield losses, reduced quality, and increased production costs due to the removal of infected plants, sanitation measures, and disease management interventions. The industries linked to roses, including nursery businesses, landscaping, and the global cut flower market, encounter disruptions in supply chains, increased quarantine and regulatory costs, and increased labor fees. Moreover, the presence of these viruses in major rose-producing regions can pose a risk to national economies, mainly in countries where roses are an export commodity.
There is a need for effective viral management strategies to mitigate the economic losses caused by these diseases. In order to limit the transmission of these viruses, it is critical to promote the advancement of early detection methods, including serological tests like ELISA, as well as molecular diagnostic methods like RT-PCR and HTS. In addition, disease management practices that include vector control, resistant cultivar breeding, and the use of pathogen-free propagation materials will be key components in reducing the viral infection.
The financial losses caused by viral diseases have given rise to the urgent need to invest in innovative research aimed at developing sustainable solutions for virus control. However, it might also be essential to build collaborations between researchers, breeders, and stakeholders to develop and implement effective disease management strategies that will protect the long-term sustainability of the rose industry. Future research should focus on understanding the virus-host interactions at the molecular level, exploring novel resistance mechanisms.
In conclusion, it is therefore necessary to address the growing threat of rose viral infections and mitigate their impacts. By integrating advanced molecular diagnostics, breeding innovations, and vigorous disease management frameworks, the rose industry can enhance the resilience of rose cultivation against pathogens, which will ensure the continued economic value of roses worldwide.
