Caleb Paslay
Akhtar Ali- Department of Biological Science, Oxley College of Health & Natural Science, The University of Tulsa, Tulsa, OK, United States
Roses have been cultivated by humans for centuries. They play an essential role in the horticulture industry by contributing economically, enhancing landscape aesthetics, supporting pollinators and other wildlife. However, roses are susceptible to viral diseases. More than thirty known and emerging plant viruses have been directly identified in rose plants worldwide. Emerging viruses pose a potential threat to the cultivation of roses. These viruses are taxonomically diverse, primarily belonging to the Bromoviridae, Betaflexiviridae, Secoviridae and Tospoviridae families, with the Ilarvirus, Nepovirus, and Orthotospovirus genera being most common. Most of these viruses are positive-sense single-stranded (+ssRNA) or negative-sense single-stranded (-ssRNA) and have segmented genomes, while only two DNA viruses have been reported in roses. Transmission of these viruses occurs via arthropod vectors (n=16), as well as through vegetative propagation, grafting, and nematodes. Current virus management strategies focus on early detection and removal of infected plants to prevent virus spread. This review provides a comprehensive overview of the geographical distribution, transmission mechanisms of viruses infecting roses, and molecular properties of virus genomes offering valuable insights for growers and researchers. This review may help in developing targeted strategies for virus management and emphasizes the importance of continued collaboration to improve viral disease management in roses.
1 Introduction
Roses are among the most important and morphologically diverse ornamental plants with wide-ranging applications in landscape design, the cut flower industry, and traditional medicine. The genus Rosa belongs to the subfamily Rosoideae within the large Rosaceae family, which also includes related genera such as Prunus (almond, apricot, cherry), Malus (apple), and Rubus (blackberry, raspberry). There are between 140 and 180 known rose species, along with >30,000 rose varieties (1). Roses have been cultivated since ancient times, with their original domestication linked to China and other regions of Asia (1). Common landscape roses include hybrid teas, Drift®, and Knock Out® roses. While cultivated roses typically feature greater than five petals, naturalized roses generally have five petals (2). Another distinguishing characteristic of cultivated roses is their ability to bloom repeatedly throughout the summer, whereas naturalized roses typically flower once a year, usually in late spring to early summer (Figure 1).
Figure 1. Different rose morphologies. (A) A rose that was photographed on 5/31/2024 of a non-cultivated rose species near Tulsa, OK. (B) A cultivated hybrid tea rose plant cv ‘Pink Peace’.
1.1 Significance and economic importance of roses
Roses are economically important because they contribute substantial monetary value to the global market. The total value of global rose trade was previously estimated at a staggering $3.12 billion, with nearly 10 billion rose stems sold annually (1). Globally, the top exporters of roses were the Netherlands and Ecuador in 2022 (according to BACI-CEPII, http://www.cepii.fr/CEPII/en/welcome.asp (3);, while the leading importers were the United States of America (USA) and the Netherlands in the same year.
While the garden, potted, and cut rose industries are significant and highly valued, roses are also used in various industrial applications. Fragrant roses are highly sought after for their use in producing essential oils (4). Fragrance has been selectively minimized in cut roses due to some evidence suggesting an inverse relationship between fragrance and petal longevity or vase life (1). However, in other cases, fragrance is deliberately selected for, as exemplified by the damask rose (Rosa damascena). Such roses are used to produce oils, waters, soaps, creams, and other products.
Rose oil is one of the most expensive oils by volume, as the flowers are hand-harvested, and a large quantity of petals is required to produce a small amount of oil (5). It takes approximately 3,000 kg of rose petals to yield just 1 kg of rose oil (6). For example, 15 kg of rose petals are needed to fill a 5-ml bottle of rose oil. The retail price for 5 ml of rose oil ranges from $140 to $366 according to several sources (https://www.revive-eo.com/product/rose-essential-oil/, https://www.youngliving.com/us/en/product/rose-essential-oil, https://www.doterra.com/US/en/p/rose-oil).
Beyond their fragrant appeal, rose oils possess a variety of biochemical and pharmacological properties, including antioxidant, antibacterial, antimicrobial, anticancerous, and other health benefits (6). Additionally, rose-based products contribute to agriculture by serving as valuable feed supplements (7). From an ecological perspective, roses play an important role by supporting beneficial insects (8) and provide habitats and resources for pollinators (9, 10).
1.2 Impediments to the production of healthy roses
Abiotic and biotic stressors limit the production of roses. Biotic stress can significantly impact the reproductive success, flower quality, and marketability of roses worldwide, leading to negative consequences for rose growers (11). Biotic stress in roses includes fungi (1), bacteria (12–14), phytoplasma (15–18) and viruses. Plant viruses, in general, are estimated to cause an economic loss of about $30 billion annually (19). Specifically, viral infection in roses can lead to reduced flower yields, lower bud quality, and poor rooting of cuttings (20).
Since the mid-1900s, numerous viruses have been identified from both cultivated and non-cultivated rose species. In 1962, four common disease phenotypes were recognized in the genus Rosa, including rose mosaic, rose yellow mosaic, rose streak, and rosette of roses (21). The causative agents of rose mosaic, rose yellow mosaic, and rose rosette will be discussed in more detail in the following sections. In contrast, the causative agent of rose streak disease remains unknown and is currently classified as a “phantom agent.” Other rose diseases associated with phantom agents include rose ring pattern, rose wilt, rose leaf curl (in the USA), rose flower proliferation, mottled rose mosaic virus, rose stunt, rose line pattern virus, and rose X disease (22). These phantom agents should no longer be considered, as they create unnecessary complications for plant certification processes and screening programs.
Nearly two decades ago, a compendium was published highlighting the growing number of viruses in roses (23). Several studies have identified numerous viruses that infect roses, though they often lack detailed information regarding the viruses’ distribution, transmission, or other characteristics (24, 25). In contrast, other authors offer more in-depth information but cover a smaller number of viruses (26–29). More recently the compendium of rose diseases and pests, third edition (30) includes an expanded and updated section on 34 viruses affecting roses, incorporating the most recent advances in rose virology and pathology. It documents a broad range of virus- and graft-transmissible diseases (e.g., Ilarvirus, Nepovirus, and Emaravirus species) known to infect roses worldwide, assisting diagnosticians and growers in distinguishing between molecularly confirmed pathogens and those identified primarily through symptomatology. Rose necrotic mosaic virus (RoNMV) and rose color break virus, which were described in the rose compendium, have been classified as tentative viruses within this review.
Therefore, this review builds upon previous work (30) and has updated the current list to 37 viruses known to infect roses providing comprehensive information on each known and emerging viruses. Additionally, tentative rose-infecting viruses were considered but not included as part of the list of 37 viruses. The insights offered will 1) scaffold future research on rose infecting viruses and 2) assist rose growers and researchers in developing highly specific and effective management practices.
2 Overview of viruses infecting roses
Through an extensive review of the literature, we identified 37 viruses that have been directly detected in roses using a range of diagnostic techniques (Table 1). With the emergence of high-throughput sequencing and other advanced molecular tools, molecular confirmation has become the gold standard for verifying viral presence and pathogenicity in plant hosts. However, several viruses lack molecular evidence supporting their occurrence in roses. This raises concern, as earlier detection methods often relied on symptomatology, virion morphology, or serological assays, which can lead to misidentification or cross-reactivity without molecular validation. Accurately defining host range, pathogenicity, and virus distribution remains challenging. Conversely, several viruses have been identified solely through molecular techniques, raising a different concern due to the limited understanding of their biological properties. To address these contrasting issues, Table 1 differentiates between viruses with molecular confirmation in roses and those without, providing essential context for interpreting their etiological significance. It is important to note that these distinctions do not undermine alternative diagnostic approaches; rather, they highlight the need for further investigation into viruses that (1) lack molecular confirmation or (2) have been detected only through molecular methods, with minimal biological characterization in roses.
Table 1. List of 37 viruses infecting roses and their molecular and distribution-related characteristics.
Among the observable disease phenotypes, one of the more prominent is rose mosaic disease (RMD, Figures 2A–C). Previous studies suggest that RMD may be caused by at least six different viruses including apple mosaic virus (ApMV), arabis mosaic virus (ArMV), prunus necrotic ringspot virus (PNRSV), strawberry latent ringspot virus (SLRSV), TSV, and tomato ringspot virus (ToRSV, 23, 31). Other viruses exhibit more distinct symptoms in roses. For instance, rose rosette virus (RRV) causes severe rosette of the leaves and increased diameter of auxiliary stems compared to the main stems (32, Figures 2D–F). In our observations, we have noted flower abortion and bud necrosis on infected rose plants (Paslay C. and Ali A., unpublished). Rose leaf rosette-associated virus (RLRaV) appears to cause conspicuous severe rosette-like symptoms in its rose host (33).
Figure 2. Common symptoms of virus infection observed in roses: (A) mosaic, (B) yellow mosaic, and (C) leaf splotching. Typical symptoms of rose rosette disease (RRD) include (D) excessive thorniness, (E) rosette formation or witches’ broom, and (F) reddening and malformed leaves.
2.1 Taxonomic distribution
Most viruses infecting roses (Table 1) are classified within the families Bromoviridae (n=7) and Betaflexiviridae (n=7), followed by Secoviridae (n=6), Tospoviridae (n=4), Rhabdoviridae (n=3), Partitiviridae (n=2), Potyviridae (n=2), and Tombusviridae (n=2). Additionally, four other virus families (Caulimoviridae, Closteroviridae, Fimoviridae, and Geminiviridae) each contain one virus known to infect roses. In terms of genera, there are six members of the genus Ilarvirus known to infect roses. Nepoviruses and orthotospoviruses each have four virus members detected in roses. These findings are consistent with previous studies, such as Mitrofanova et al., which also identified nepoviruses and ilarviruses among the most common rose-infecting viruses (20). Overall, viruses detected in roses belong to 12 different families and 21 distinct genera.
2.2 Genomic distribution
When examining the distribution of the virus genomes infecting roses, there is a clear predominance of positive sense RNA viruses (+ssRNA; n=25) compared to other genomic types. Additionally, two viruses, rose leaf curl virus (RoLCuV) and rose yellow vein virus (RYVV), have DNA genomes. Eighteen of the virus genomes are monopartite, with tripartite genomes being the next most common type (n=12). Overall, there are nineteen virus species known to infect roses which are segmented. In terms of genome size, the largest genomes are found in viruses from the Closteroviridae, Fimoviridae, and Tospoviridae families, whereas the smallest genomes belong to viruses in the Geminiviridae, Partitiviridae, and Tombusviridae families.
2.3 Virion properties
The majority of viruses infecting roses have either icosahedral or filamentous virion morphologies (n=26). Geminate morphology is the least common, with only one geminivirus (RoLCuV) infecting roses. Regarding enveloped virions, eight viruses possess a nucleocapsid protein shell surrounded by an envelope. Notably, all enveloped viruses (Table 1) possess negative-sense RNA genomes, and likewise, all negative-sense RNA viruses are enveloped.
2.4 Transmission diversity
An analysis of transmission modes revealed that fourteen viruses are either known or presumed to be transmitted by insect vectors (Table 1). Among insect vectors, aphids (n=9), thrips (n=4), and whiteflies (n=1) are represented. Nematodes (n=5) and mites (n=3) are responsible for a lesser proportion of transmitted viruses. Additionally, many viruses in roses can also be transmitted via pollen and seed. Although not always the primary pathways, vegetative propagation and grafting are the most frequently reported methods of virus transmission between infected and healthy plants. As shown in Table 1, many of these viruses can be transmitted by multiple mechanisms which can complicate disease management. Some modes of transmission are of a tentative nature, lacking empirical evidence (indicated by # in Table 1). Importantly, the values provided here include both recognized and tentative modes. In some cases, the exact transmission pathways for these viruses are not yet fully understood, but it is likely that these viruses share similar transmission strategies with other members of their respective genera. Generally, viruses within the same genus tend to exhibit similar biological characteristics, including modes of transmission (Table 1).
2.5 Reported occurrences of viruses detected in roses from different countries
Analysis of the reported occurrence of rose-infecting viruses showed that sixteen viruses have a localized range, while seven are considered widespread (Figure 3). Widespread viruses include ApMV, PNRSV, rose cryptic virus 1 (RCV-1), Rose partitivirus (RoPV), Arabis mosaic virus (ArMV), strawberry latent ringspot virus (SLRSV) and rose spring dwarf-associated virus (RSDaV). A closer look at virus presence in the world indicates that nineteen of the identified rose viruses have been reported in the New World. In contrast, fourteen have been detected in both the New World and the Old World (Figure 3). Concerning the USA, eighteen viruses detected in roses have been reported from at least one USA region. For further details on the geographical distribution of specific viruses, resources such as CABI (https://www.cabidigitallibrary.org/) and the European and Mediterranean Plant Protection Organization (EPPO, https://gd.eppo.int/) offer useful information. Additionally, a specialized website like Rose Rosette (https://roserosette.org/) provides valuable insights on rose rosette disease (RRD) and its distribution across the USA.
Figure 3. Worldwide occurrence of known viruses infecting roses (specifically detected from roses). Countries where rose viruses have been reported are colored magenta.
3 Characteristics of each virus species in roses
3.1 Betaflexiviridae
Seven viruses identified in roses belong to the family Betaflexiviridae. These viruses are molecularly characterized by monopartite, +ssRNA genomes ranging from 6.5 to 8.8 kb in length. Biologically, they form non-enveloped, flexuous filamentous particles measuring between 600 and 1,000 nm (34). In general, betaflexiviruses are transmitted mechanically or via vectors such as aphids, though transmission mechanisms can vary depending on the genus (34).
3.1.1 Apple chlorotic leaf spot virus
Apple chlorotic leaf spot virus (ACLSV) is classified within the genus Trichovirus (species binomial: Trichovirus mali). To date, there is no molecular evidence of this virus in roses according to nucleotide submissions on NCBI. While ACLSV is widespread in other hosts, its potential to infect roses had not been reported until recently. In 2013, ACLSV was detected from Greece in roses (Rosa canina and Rosa acicularis) by serology and reverse transcription polymerase chain reaction (RT-PCR, 35). Although this initial detection is promising, further molecular and biological characterization of ACLSV in roses is essential to more fully establish Rosa as a new biological host. The exact route of virus transmission remains unclear, though previous studies suggest that vegetative propagation and grafting are the main mechanisms for virus dissemination (35).
3.1.2 Apple stem grooving virus
Apple stem grooving virus (ASGV) is classified within the genus Capillovirus (species binomial: Capillovirus mali). This virus has been described since the 1960s in apple (36). ASGV is globally widespread in a variety of woody stemmed plants such as citrus, apple, and pear. However, there are limited reports of ASGV in roses and no known cases of the virus infecting roses from the USA. In 2015, ASGV was reported from China in wild roses using deep sequencing (33). Additionally, ASGV was found during a virome study from Taiwan (25). Since the surveyed rose was co-infected, it is challenging to correlate symptoms with the causative virus. In other hosts, ASGV may be asymptomatic or cause yellowing, vein banding, and mosaic on the leaves. ASGV is also commonly associated with stem grooving and graft union necrosis in apple and citrus (37, 38). There is some evidence of seed (37, 39) and pollen transmission (40) in apple, but no known vectors have been identified.
3.1.3 Cherry necrotic rusty mottle virus
Cherry necrotic rusty mottle virus (CNRMV) is classified within the genus Robigovirus (species binomial: Robigovirus necroavii). The first complete genome of CNRMV was published in 2001 (41). CNRMV has been reported from various regions, including the USA (42–44), China (45), South America (46), Korea (47), Japan (48), and Europe (49). The primary hosts of CNRMV include sweet cherry (Prunus avium), peach (Prunus persica), and sour cherry (Prunus cerasus). More recently, CNRMV has been detected in several rose species from India, including Rosa brunonii, Rosa multiflora, Rosa cathayensis, and Rosa alba (50). This is the only known report of CNRMV in roses with the authors suggesting that these wild rose species could serve as reservoirs for the virus during dormant periods (50). CNMRV is primarily transmitted through infected plant material via grafting or propagation (50, 51), and there is currently no known vector for its transmission (52).
3.1.4 Grapevine pinot gris virus
Grapevine pinot gris virus (GPGV) is classified within the genus Trichovirus (species binomial: Trichovirus pinovitis). GPGV was first discovered in grapevine in 2012 via deep sequencing (53). The primary host of GPGV is grapevine and the presence of GPGV has been reported from Algeria, Argentina, Australia, Canada, France, Greece, Russia, Slovakia, Spain, Switzerland, USA, and others (54–60). In relation to roses, GPGV has only been detected from Hungary (56). Symptoms of GPGV in roses have not been clearly defined, as strains from non-Vitis hosts tend to cluster within the asymptomatic clade (56). GPGV is transmitted by grafting (61) and eriophyid mites (62). Additionally, given the virus’s asymptomatic nature, correlating virus presence with symptom expression is challenging.
3.1.5 Rose virus A
Rose virus A (RVA) is classified within the genus Carlavirus (species binomial: Carlavirus alpharosae). This virus was first characterized in roses from the USA which remains the only report of RVA to date (63). The associated symptoms include leaf deformation and mosaic, as initially described (63). The transmission mechanisms are currently unknown, but many carlaviruses are naturally transmitted by aphids in a nonpersistent manner (34). While it is not yet confirmed that RVA is aphid-transmitted, this remains a likely mode of dissemination. Further studies are needed to better understand the transmission mechanisms of RVA.
3.1.6 Rose virus B
Rose virus B (RVB) is classified within the genus Carlavirus (species binomial: Carlavirus betarosae). RVB has been characterized in roses from both the USA (64) and Mexico (65). During a study conducted in the USA, high throughput sequencing (HTS) was used to assess roses in a virus collection, revealing an asymptomatic ‘Out of Yesteryear’ rose with sequences homologous to members of the Carlavirus genus. These partial sequences were confirmed by additional RT-PCR assays and were given the provisional name “Rose virus B” (64). In a 2022 study from Taiwan, RVB was annotated from HTS data, but a low read count was observed and RVB was not detectable by RT-PCR (25). This suggests that RVB may be present in Taiwan, but further studies will be valuable to confirm its occurrence. Recently, RVB was also characterized in Mexico (65). The symptoms associated with RVB on roses remain unresolved due to mixed infections, though potential symptoms such as mosaic, vein yellowing, chlorotic line patterns, and interveinal chlorosis have been documented (65). Transmission mechanisms for RVB are currently unknown, as for RVA, aphid vectors are likely involved. Further studies are needed to better understand additional transmission pathways for RVB.
3.1.7 Rose virus C
Rose virus C (RVC) is a proposed species within the genus Carlavirus. Molecular data from NCBI indicates that RVC has been detected from roses in China. RVC was first recognized from transcriptome data in 2021 (66) with symptoms including yellow mosaic of the leaves (67). The virus mode of transmission is still unknown, but like other rose carlaviruses (RVA and RVB), RVC is likely transmitted by aphids, though this requires further experimental validation.
3.2 Bromoviridae
Seven viruses which belong to the family Bromoviridae have been identified in roses. These viruses are molecularly characterized by their tripartite, +ssRNA genomes, which range in size from 7.9 to 8.8 kb. The virions themselves are non-enveloped, spherical or quasi-spherical in shape, with diameters ranging from 26 to 35 nm (68). Typically, viruses within the family Bromoviridae are spread through pollen, insect vectors, or mechanical mechanisms (68).
3.2.1 Apple mosaic virus
Apple mosaic virus (ApMV) is classified within the genus Ilarvirus (species binomial: Ilarvirus ApMV). ApMV has been studied since the 19th century when the disease was visually characterized (69). In the mid-20th century, experiments demonstrated the mechanical transmissibility of ApMV to tobacco (70). The earliest report of ApMV in the USA from the plant genus Rosa was in 1928 (71). In 1993, ApMV was purified from roses in the USA (72). ApMV has since been detected in roses from Australia, Ecuador, Mexico, New Zealand, Turkey, and the USA (20, 65, 73, 74). ApMV is associated with RMD, which is characterized by symptoms such as mosaic, chlorotic bands, yellow vein banding, and oak-leaf patterns (75). ApMV is important because it can infect both economically and ecologically important hosts (76). The virus is transmissible through grafting and propagation, but there is no evidence for seed or pollen transmission in roses. Additionally, natural root graft transmission has been demonstrated (77). While no natural vector has been identified, some evidence suggests that ApMV may be transmissible by thrips and/or aphids (76).
3.2.2 Blackberry chlorotic ringspot virus
Blackberry chlorotic ringspot virus (BCRV) is classified within the genus Ilarvirus (species binomial: Ilarvirus BCRV). BCRV was first described as a novel virus from the UK in Rubus (78) and later reported in Rubus for the first time from the USA in 2007 (79). In relation to roses, BCRV was first documented in 2006 and initially named rose virus 1 (RsV-1, 80). The virus was later considered to be an isolate of BCRV and renamed accordingly. In the USA, BCRV has been detected in roses from various regions, including Arkansas, Missouri, and Washington, D.C. (accession number: OK338424.1, 81). BCRV has also been detected in China from Rosa multiflora (33). To date, molecular data on NCBI shows that most BCRV sequences in roses have been submitted by USA research groups/individuals. A single infection typically results in mild symptoms in roses. The virus has been found to have a seed transmission rate of 58% in Rosa multiflora (82). BCRV is likely transmitted by pollen and pollen-carrying insects such as thrips (81).
3.2.3 Cucumber mosaic virus
Cucumber mosaic virus (CMV) is classified within the genus Cucumovirus (species binomial: Cucumovirus CMV). In 2006, a survey of rose viruses was conducted in Iran whereby the authors screened for PNRSV, ArMV, and CMV using DAS-ELISA (83). The results showed that CMV was not detected in any of the rose samples. Later, several researchers detected CMV during surveys conducted between 2017 and 2020 in the UK, marking the first detection of CMV in roses in the UK (84). Descriptions of symptoms on roses are limited. CMV is one of the most widely distributed plant viruses with a host range of ~1,200 species and is primarily transmitted by aphid vectors, notably Myzus persicae (85).
3.2.4 Prunus necrotic ringspot virus
Prunus necrotic ringspot virus (PNRSV) is classified within the genus Ilarvirus (species binomial: Ilarvirus PNRSV). PNRSV is known to be distributed globally in the Rosaceae family particularly within the genus Prunus, but also in the genus Rosa. Unlike many other viruses that infect roses, which are limited in their geographical distribution, PNRSV has a widespread geographical distribution in roses. It has been reported and characterized from regions across the globe, including India, Turkey (86), Lebanon, Bulgaria, Brazil, China (31), Poland (87), France, Ecuador, New Zealand, Saudi Arabia (88), Iran, Jordan (89), Egypt (90), Tasmania (91), UK (92), Spain (93) and other countries (94).
Despite its global spread, there are only several reports of PNRSV infecting roses from the USA. For example, PNRSV was previously detected using ELISA (95, 96). Additional investigations of non-Rosa hosts have found PNRSV from New York in cherry orchards (97), and from South Carolina and Georgia in wild Prunus sp (98). PNRSV is considered one of the most common viruses affecting roses (20, 99). The virus is primarily transmitted via pollen and can also spread indirectly by insect vectors such as bees and thrips (100).
3.2.5 Rosa Ilarvirus-1
Rosa ilarvirus-1 (RIV-1) is a newly classified species in the genus Ilarvirus (species binomial: Ilarvirus RIV1). According to NCBI, reports of RIV-1 have been localized to the UK in the genus Rosa. Although the virus was detected from the UK, the infected rose was an import from India (101). Since the virus was identified as part of a surveillance program, biological characterization was not conducted (101). The primary literature shows that RIV-1 has not been reported from any other countries, which aligns with the molecular data. Symptoms associated with RIV-1 include mottling, yellow veining, distortion, and ringspots. Like other ilarviruses, RIV-1 is presumed to be transmitted via seed and infected pollen grains, although further research is needed to confirm this.
3.2.6 Rose Ilarvirus 2
Rose ilarvirus 2 (RIV-2) is a newly classified species in the genus Ilarvirus (species binomial: Ilarvirus RIV2). RIV-2 has been detected from Taiwan and Ecuador in Rosa sp. (accession number: ON843765.1) and Rubus sp. (accession number: PP555255.1), respectively. Phylogenetic analysis has shown that RIV-1 and RIV-2 are closely related species (25). To date, only one published report of RIV-2 in roses exists. While the mode of transmission for RIV-2 remains unknown, it is presumed to be transmitted by seed and/or infected pollen grains, though this requires further investigation.
3.2.7 Tobacco streak virus
Tobacco streak virus (TSV) is classified within the genus Ilarvirus (species binomial: Ilarvirus TSV). According to NCBI, there are no molecular records of TSV in roses. TSV was first detected from roses in Wisconsin, USA (102). TSV has been detected from Oregon, USA (103) and Colombia (104) in roses. Although several studies have hypothesized TSV as a virus associated with observed symptoms, TSV was not detected in those investigations (79, 105). The symptoms of TSV infection in roses vary widely. In some cases, severe symptoms have been reported (94), while in other instances, TSV was present without any apparent symptoms (106). Symptoms may include stunting, vein chlorosis, twisting, and chlorotic regions (102). Generally, ilarviruses are transmitted via infected pollen grains (in or on, 68). Early studies on Rubus sp. suggested that TSV may spread through mechanisms other than associations with flowers (103). Further research demonstrated that TSV could be seed and sap transmissible in sweet clover (Melilotus alba) and cowpea (Vigna unguiculata, 106). TSV is transmissible by sap inoculation from infected leaves (102), but further details about TSV transmission in roses are unclear and requires additional investigation.
3.3 Caulimoviridae
A single virus identified in roses belongs to the family Caulimoviridae. Caulimoviruses are characterized molecularly by circular double-stranded DNA (dsDNA) genomes ranging from 7.1 to 9.8 kb in length (107). The virions are non-enveloped and isometric, measuring between 45 and 52 nm in diameter, although some may exhibit a bacilliform shape. These viruses are generally transmitted by insect vectors and grafting (107).
3.3.1 Rose yellow vein virus
Rose yellow vein virus (RYVV) is classified within the genus Rosadnavirus (species binomial: Rosadnavirus venarosae). RYVV has been detected from the USA, Turkey, and New Zealand in roses. Initially, RYVV was given the provisional name rose chlorotic ringspot virus (RoCRSV) when it was first described from the USA in the early 2000s (108), with its complete genome characterized later (109). RYVV was subsequently reported from Turkey in 2018 (110), with further studies indicating an expanded geographic range within the country (99, 111). In New Zealand, RYVV was first detected in 2013 (112) and later confirmed through field surveys (113). Given the isolation of RYVV throughout different studies, various symptoms have been observed on roses, which include vein yellowing and chlorotic mottling (112), vein banding and central vein chlorosis (113), chlorotic patterns, mosaic, and mottling (99). The variation in symptoms observed is influenced by a combination of factors including virus and host genotypes, mixed infections, and abiotic factors. Caulimoviruses are typically spread by vegetative propagation (107). Mollov et al., 2013, concluded that RYVV can be transmitted by grafting but mechanical or aphid-vectored mechanisms, which were tested, did not demonstrate transmissibility (109).
3.4 Closteroviridae
One virus detected in roses is classified within the family Closteroviridae. Closteroviruses are characterized molecularly by one to three molecules of +ssRNA, with genome sizes ranging from 13 to 19 kb (114). The virions are non-enveloped, helical-filamentous in structure, and vary in length from 650 to 2200 nm (114). These viruses are typically transmitted by insect vectors, but not through seeds or pollen (114).
3.4.1 Rose leaf rosette-associated virus
Rose leaf rosette-associated virus (RLRaV) is classified within the genus Closterovirus (species binomial: Closterovirus rosafolium). The virus was first described from a wild rose species from China (33) and later from California, USA in cultivated roses grown by a private breeder (115). It is unclear whether RLRaV is more prevalent in the USA, China, or other countries. Due to limited research, no explicit study has been conducted to assess the impact of RLRaV on rose performance or potential to reduce the quality of roses (115). Nevertheless, symptoms of RLRaV include mosaic patterns (31), small dense leaves, decline, dieback, and plant death, suggesting that RLRaV impacts rose performance and quality (33). Like other closteroviruses, RLRaV is likely transmitted by aphids in a semi-persistent manner. While less likely, it is also possible that RLRaV could be transmitted via sap. However, there is no evidence to suggest that closteroviruses are transmitted through seeds (114), making seed transmission an unlikely route for RLRaV.
3.5 Fimoviridae
A single virus species detected in roses has been classified within the family Fimoviridae. Members of this family, known as fimoviruses, possess multipartite genomes consisting of 4 to 10 segments of negative-sense single-stranded RNA (-ssRNA), with a total genome length ranging from 12.3 to 18.5 kb (116). Fimovirus particles are enveloped, quasi-spherical in shape, and measure approximately 80 to 150 nm in diameter (116). These viruses are primarily transmitted by eriophyid mites, although some are also capable of mechanical transmission (116).
3.5.1 Rose rosette virus
Rose rosette virus (RRV) is classified within the genus Emaravirus (species binomial: Emaravirus rosae). RRV has been characterized in the USA and detected in India from roses. It is widespread across the USA and has been considered endemic, infamous for causing RRD. However, a report of RRV from India suggests that its distribution may be expanding (117). According to the distribution map on Rose Rosette, (https://roserosette.org/distribution-map/), most USA states have reported RRD, with many confirmed cases of RRV. RRD has been recognized since the 1940s in the Western United States and Canada (118), but the virus was not identified as the causative agent until 2011 (119). RRV causes distinctive symptoms including rosette, excessive thorniness, prolonged reddening, and plant death (32, 120). Symptoms typically appear 1–6 months after initial infection. RRV is primarily transmitted by the eriophyid mite Phyllocoptes fructiphilus which does not cause direct damage to the host plant (121) and is often found associated with floral tissues such as sepals and petals (122). Other potential transmission routes, including seed, graft, mechanical, and root transmission have been explored (123). In experimental settings, graft transmission has been the most effective method (124, 125), though the other modes have limitations that hinder successful transmission. For instance, seed transmission is possible, but occurs at a low rate, and the virus is often not detectable after several months (123).
RRV is considered one of the most important viruses infecting roses (126). As a result, recent studies have focused on virus diagnostics (120, 126, 127), resistance breeding (128–130), and exploring the genetic diversity of the RRV population (131, 132). Additionally, the first reverse genetic system for RRV was developed, which will be essential for understanding the virus’s complex molecular machinery (133). It is vital that RRV be maintained within the USA to prevent the introduction of RRV to other regions of the world. For more detailed information on RRV, we recommend a recent review by Vazquez-Iglesias et al. (134).
3.6 Geminiviridae
There is one virus species identified in roses which has been classified within the family Geminiviridae. Geminiviruses are molecularly characterized by circular single-stranded DNA (ssDNA) genomes ranging from 2.5 to 5.2 kb in length (135). Structurally, the virions are non-enveloped, twinned (geminate) in morphology, and measure between 22 and 38 nm in diameter (135). These viruses are primarily transmitted by insect vectors, with whiteflies being the most notable (135).
3.6.1 Rose leaf curl virus
Rose leaf curl virus (RoLCuV), which causes rose stunt disease (RSD, 136), is classified within the genus Begomovirus (species binomial: Begomovirus rosae). RoLCuV was first characterized from Pakistan in roses (136). RoLCuV continues to be primarily limited to the Indian subcontinent where it has been molecularly characterized from Pakistan and India in roses. Rose leaf curl (RLC) was reported in California during the 1970s, but its etiology remains unknown (137). It is possible that RoLCuV caused RLC, but this remains unsubstantiated and highlights why RLC is currently classified as a phantom agent in the USA (22). In the initial study, researchers demonstrated that the RoLCuV DNA-A alone did not induce typical symptoms in Nicotiana benthamiana and required the Digera arvensis yellow vein betasatellite (DiAYVB) for symptom development and DNA accumulation (136). Symptoms of RoLCuV include downward leaf curling, vein yellowing, and stunted growth in N. benthamiana plants (136). RoLCuV is transmitted by whiteflies in a persistent manner (138).
3.7 Partitiviridae
Two viruses detected in roses have been classified within the family Partitiviridae. Partitiviruses are molecularly characterized by linear, bipartite, double-stranded RNA (dsRNA) genomes ranging from 3.0 to 4.8 kb in length (139). The virions are non-enveloped, isometric, and measure between 25 and 43 nm in diameter (139). These viruses exhibit limited modes of transmission, occurring via seed transmission and intracellular cell division (139). Notably, no vectors are currently known to be involved in the transmission of partitiviruses.
3.7.1 Rose cryptic virus 1
Rose cryptic virus 1 (RCV-1) is classified within the family Partitiviridae, though it is not yet fully classified within a specified genus. Unlike most partitiviruses, RCV-1 is comprised of three linear segments of dsRNA rather than two (140). RCV-1 has been detected from Canada (141), New Zealand (113), Taiwan (25), Turkey (99), UK (142), and the USA (140) exclusively in the genus Rosa. RCV-1 has several synonymous names due to its characterization by different research groups. In addition to rose cryptic virus 1 (RCV-1), it was also referred to as rosa multiflora cryptic virus (143) and rose transient mosaic virus (108). RCV-1 is often asymptomatic, but in some cases, it has been associated with leaf yellowing, leaf mosaic, and mottling (108, 113). In our own surveys, we observed a range of symptoms on roses, from mild to severe, including mottling, leaf spotting, and mosaic patterns (Figure 4). These symptoms associated with RCV-1 may be due to the presence of an undetected virus, given that cryptic viruses are not associated with causing symptoms in their host. Like other partitiviruses, RCV-1 lacks known vectors and cannot move between cells via movement proteins. RCV-1 is likely transmitted through the ovules or pollen grains to the seed embryo. Additionally, these viruses are known to spread from cell-to-cell during cellular division (144).
Figure 4. Mosaic symptoms of RCV-1 on a rose sample collected from a field in Oklahoma. Virus presence was confirmed by RT-PCR and HTS analysis (C. Paslay and A. Ali, unpublished).
3.7.2 Rose partitivirus
Rose partitivirus (RoPV) is a species classified within the family Partitiviridae. The virus was first reported in Canada (145), found using HTS in USA (115), and more recently, it has been described from roses in Taiwan (25). Like other partitiviruses, RoPV is likely transmitted intracellularly during cell division and via seeds (139). No known vectors are capable of transmitting RoPV. Symptoms associated with RoPV in roses were not described in the initial report (145).
3.8 Potyviridae
Two viruses identified in roses have been classified within the family Potyviridae. Potyviruses are molecularly characterized by monopartite, +ssRNA genomes ranging from 8.2 to 11.5 kb in length (146). The virions are non-enveloped, flexuous filamentous particles measuring between 650 and 950 nm in length (146). Transmission occurs by arthropods, seeds, pollen, and Polymyxa graminis (genus: Bymovirus, 146), although in some cases, the specific vectors involved remain to be identified.
3.8.1 Bean yellow mosaic virus
Bean yellow mosaic virus (BYMV) is classified within the genus Potyvirus (species binomial: Potyvirus phaseoluteum). There are no molecular records of BYMV in roses according to NCBI. The only report of BYMV in roses (Rosa damascena) came from a study in Saudi Arabia where they found up to 10% virus detection via indirect-ELISA (147). The study also reported that the developed antibody exhibited cross-reactivity with other serologically related viruses such as pea mosaic virus (PMV) and clover yellow vein virus (CIYVV). The symptoms of BYMV in roses included yellow mosaic on leaf and moderate flower breaking on petals (147–149). The findings presented here are promising, however, it is essential that further biological and molecular studies of BYMV be conducted to fully establish its etiological role in roses.
3.8.2 Rose yellow mosaic virus
Rose yellow mosaic virus (RoYMV) is classified within the genus Roymovirus (species binomial: Roymovirus rosae). In the USA, RoYMV was first detected in the early 2000s (108). In Japan, RoYMV was isolated from the rose cultivar ‘Irish Mint’ (150). The complete genome sequence was later determined, and RoYMV was classified within the family Potyviridae, making it the first known potyvirus to infect roses (151). While BLASTP analysis initially suggested RoYMV as a member of the genus Potyvirus, phylogenetic analysis indicated otherwise, and RoYMV was eventually classified as part of a new genus within the family Potyviridae (151). Symptoms include yellow mosaic, premature leaf senescence, and necrotic stem lesions. In relation to transmission, RoYMV is lacking HC-Pro motifs and a DAG motif of the coat protein associated with aphid transmission. Additionally, a C-2x-C motif associated with eriophyid mite transmission suggests that RoYMV may be transmitted by eriophyid mites (151). It has been hypothesized that aphid transmission may have been lost through continuous vegetative propagations (151). Further research is needed to fully understand the specific vectors involved in RoYMV transmission.
3.9 Rhabdoviridae
Three viruses identified in roses have been classified within the family Rhabdoviridae. Rhabdoviruses are molecularly characterized by monopartite, bipartite, or tripartite -ssRNA genomes ranging from 10 to 16 kb in length (152). The virions are enveloped, bacilliform in shape, and range from 100 to 430 nm in length (152). Plant-infecting rhabdoviruses are primarily transmitted by arthropod vectors but may be transmitted by propagation (152).
3.9.1 Rose virus R
Rose virus R (RVR) is classified in the genus Betacytorhabdovirus (species binomial: Betacytorhabdovirus alpharosae) based on the full genome sequence (153). RVR has been documented in roses based on molecular evidence, and was first described from Maryland, USA in Rosa ‘Hugh Dickson’ in 2016 (154). Symptoms include leaf deformation and yellowing. Though aphids, leafhoppers, planthoppers, or whiteflies are typical vectors for the subfamily Betarhabdovirinae (plant-infecting rhabdoviruses), the specific vector for RVR remains unidentified and requires further study.
3.9.2 Rose-associated cytorhabdovirus
A novel negative-sense virus named rose-associated cytorhabdovirus (RaCV) is classified as a member of the genus Betacytorhabdovirus (species binomial: Betacytorhabdovirus betarosae) and was discovered to be closely related to another betacytorhabdovirus, Yerba mate virus A (155). RaCV was characterized from Rosa chinensis using high throughput sequencing (155). The annotated genome was deposited in the GenBank under the accession number ON762421. The complete sequence was found to be 16 kb in length with a GC content of 37.8%. No symptoms were observed on infected plants. Additionally, the authors speculated that the virus may have been transmitted to the infected rose within a relatively short period of time given that the virus did not spread to nearby roses (155). Further research is needed to investigate the biological role of RaCV in roses.
3.9.3 Rose alphacytorhabdovirus 1
Rose alphacytorhabdovirus 1 (RosACRV1), classified in the genus Alphacytorhabdovirus (species binomial: Alphacytorhabdovirus rosae, 153) was identified through a data mining study of Rosa rugosa cv. ‘Bao White’ (156). The virus was unintentionally sequenced during a study focused on flavonoid biosynthesis (157). Phylogenetic analysis indicates that RosACRV1 clusters within the Alphacytorhabdovirus clade (156). Further research is needed to understand the biological properties of RosACRV1, including the symptoms it may cause on infected plants.
3.10 Secoviridae
Six viruses identified in roses have been classified within the family Secoviridae. Secoviruses are molecularly characterized by mono- or bipartite +ssRNA genomes ranging from 9 to 13.7 kb in length (158). The virions are non-enveloped, icosahedral, and measure between 25 and 30 nm in diameter (158). These viruses are primarily transmitted through arthropods, nematodes, as well as via seed and pollen (158).
3.10.1 Arabis mosaic virus
Arabis mosaic virus (ArMV) is classified within the genus Nepovirus (species binomial: Nepovirus arabis). ArMV has been characterized from ornamentals in Iran (159), grapevine in Spain (160), and hostas (Hosta sp.) in the USA (161). ArMV has been characterized in the UK from roses with notable damage on field grown rose bushes cv. ‘Fragrant Cloud’ (162) and from New Zealand during a survey of viruses in roses (113). Furthermore, ArMV has been detected from roses in Iran and India (83, 163). Thus far, ArMV has not been reported in the USA infecting roses (96). According to molecular data, this virus is most frequently reported in Vitis vinifera. Virus infection may result in symptomless appearance or may lead to chlorotic flecks and mosaic. In severe cases, plant death may occur (162). ArMV is transmitted by soil-inhabiting nematodes (164) and through seed (165). ArMV has been detected from non-rose plants in Ohio, Maryland, Minnesota, and New York. These might be regions of concern if ArMV is transmitted to susceptible rose cultivars.
3.10.2 Raspberry ringspot virus
Raspberry ringspot virus (RpRSV) is classified within the genus Nepovirus (species binomial: Nepovirus rubi). Molecular evidence suggests that this virus is present in Canada, Germany, Lithuania, New Zealand, Switzerland, and the UK where it has been detected from a variety of hosts including Rosa spp. The only published report and molecular record of RpRSV in roses comes from Germany (166). Early research suggested that this virus was not known to be present in the USA (167) and was likely restricted to Europe (168). Furthermore, no current evidence exists regarding the presence of RpRSV in the USA. Symptoms associated with the virus include stunting, mosaic, and chlorotic vein netting. RpRSV is transmitted by seed, sap, and nematode vectors (169–171). RpRSV transmission in roses is likely to occur by seed and/or nematode vectors, though this has not been established experimentally to date.
3.10.3 Strawberry latent ringspot virus
Strawberry latent ringspot virus (SLRSV) is classified within the genus Stralarivirus (species binomial: Stralarivirus fragariae, 172). SLRSV has been detected from a wide range of plant species, including roses, from which it has been molecularly characterized. SLRSV was first reported in the mid-1960s when it was discovered infecting roses and other rosaceous plants in the UK (173, 174). Since the initial discovery, SLRSV has been identified several times from roses in the UK (162, 175). From the initial description, SLRSV has spread globally and has been reported in numerous countries such as New Zealand (176), India (177), Turkey (178), and Poland (179) infecting both roses and other host plants. SLRSV has not been reported in roses from New Zealand. In the USA, SLRSV was initially identified in parsley (180), mint (181), and strawberry (182), but it has not been reported in roses. SLRSV can cause notable damage and is considered one of the most significant viruses affecting roses in the UK (84, 162). The virus is transmitted by nematodes with Xiphinema diversicaudatum being the known vector of its transmission (173). Furthermore, X. diversicaudatum has been specifically noted to transmit SLRSV in roses (183). Symptoms of SLRSV infection in roses include strap-like leaves, yellow flecks, yellow netting, vein banding, and typical RMD symptoms (84, 184). Additional symptoms such as reduction in leaflet size, chlorotic ringspots, and stunting of the plant have been observed (178).
3.10.4 Sweetbriar rose curly-top associated virus
Sweetbriar rose curly-top associated virus (SRCTaV) is classified within the genus Waikavirus (species binomial: Waikavirus rosae). SRCTaV was first reported from New Zealand (185) infecting roses. Additionally, SRCTaV has been detected in the UK from roses (accession numbers: PP812665.1 and PP812666.1). There is currently no experimental evidence regarding the mode of transmission for SRCTaV, nor is there any indication that this virus infects hosts other than roses. Generally, waikaviruses are transmitted by aphids or leafhoppers and are not associated with sap transmission (158). Additionally, waikaviruses tend to have a restricted host range (158). The symptoms of SRCTaV infection include curling of the upper leaves and shortening of terminal internodes (185).
3.10.5 Tobacco ringspot virus
Tobacco ringspot virus (TRSV) is classified within the genus Nepovirus (species binomial: Nepovirus nicotianae). According to NCBI, there is no molecular evidence of TRSV in roses. However, TRSV was detected in roses using serological assays during the early 1970s from the USA (186). Though TRSV was considered as a potential causative agent in several studies, it was not detected (84, 187). While some studies have noted the presence of TRSV in roses, its distribution in roses appears to be limited compared to other host plants infected by TRSV (23, 113, 188). In roses, TRSV has been observed to cause chlorotic lines and rings (186). Interestingly, these symptoms are often transient, with new tissue emerging symptom-free. This has been referred to as the “recovery” phenomenon (158). Due to this phenomenon, infected plants may remain asymptomatic, leading to the possibility that TRSV is more widespread than reported. The transient nature of TRSV symptoms complicates virus detection and reporting. Transmission of nepoviruses, in general, is understood to occur through nematodes, seeds, and/or pollen (158). TRSV is graft transmissible in roses (186), but other transmission mechanisms for TRSV in roses are not well defined and warrant further investigation.
3.10.6 Tomato ringspot virus
Tomato ringspot virus (ToRSV) is classified within the genus Nepovirus (species binomial: Nepovirus lycopersici). There are no molecular records of ToRSV in roses, allowing for possible exploration of ToRSV isolates from roses. ToRSV was first reported in 1936 where it was detected in tobacco (28). The two nucleic acid segments were later investigated (189) and the complete nucleotide sequence of RNA1 for ToRSV was determined in the mid-1990s (190). While ToRSV has been detected in several countries in other host plants (28, 191), it is less common in roses. In 1962, ToRSV was described from the USA in roses, where it caused RMD-like symptoms (21). More recently, ToRSV has been detected from Iran in roses (192, 193) but was not found during surveys in England (84). Typical symptoms of ToRSV infection include yellow spots, mosaic, line patterns, leaf wrinkling, and malformation (28, 192). Like other nepoviruses, ToRSV may be transmitted by nematodes, mechanical inoculation, grafting, pollen, or seed (158). Early studies have shown that ToRSV can be transmitted by nematode vectors such as Xiphinema americanum and Xiphinema rivesi (194, 195). While similar transmission mechanisms are likely to occur for ToRSV in roses, this has not been thoroughly investigated.
3.11 Tombusviridae
Two viruses detected in roses have been classified within the family Tombusviridae. Tombusviruses are molecularly characterized by monopartite, +ssRNA genomes ranging from 3.7 to 4.8 kb in length (34). The virions are non-enveloped, icosahedral, and measure between 32 and 35 nm in diameter (34). These viruses are primarily transmitted through mechanical means and vegetative propagation (34). In addition, transmission can occur via seeds or biological vectors such as aphids (144).
3.11.1 Rosa rugosa leaf distortion virus
Rosa rugosa leaf distortion virus (RrLDV) is classified within the genus Pelarspovirus (species binomial: Pelarspovirus rosae). Molecular evidence suggests that RrLDV is primarily located in the USA, where it had been detected from two distinct regions, Washington, D.C. and Minnesota. In 2008, RrLDV was detected in roses from several US states (108). A few years later, the complete genome sequence for RrLDV was characterized (196, 197). Additionally, RrLDV has been detected from China in Rosa chinensis (accession number: MN447653.1) under the virus name rose yellow leaf virus (RYLV). Prior to 2015, RrLDV and RYLV were considered separate species, but with the creation of the genus Pelarspovirus, RYLV was classified as an isolate of RrLDV (198). The coat protein (CP) of the RYLV isolate shares a 95% amino acid identity with RrLDV (198). Symptoms of RrLDV infection include yellowing of the leaves and premature senescence. RrLDV can be transmitted via grafting (196, 197). Other mechanisms of virus transmission for RrLDV remain unexplored.
3.11.2 Rose spring dwarf-associated virus
Rose spring dwarf-associated virus (RSDaV) is classified within the genus Luteovirus (species binomial: Luteovirus rosae). RSDaV has been reported from roses and was first characterized in California, USA (199, 200). Following this initial discovery, RSDaV has been reported in several other countries, including Chile (201), China (202), New Zealand (113), Taiwan (25), Turkey (99), and the UK (203). The symptoms of RSDaV infection can vary but commonly include mosaic patterns, yellow vein chlorosis, and rosette or ball-like appearance (201, 202). There is evidence that RSDaV can infect the rose host without expressing symptoms (asymptomatic, 99). RSDaV is transmitted by several aphid species, including the rose grass aphid (Metopolophium dirhodum) and yellow rose aphid (Rhodobium porosum, 199). This mode of transmission was further substantiated as RSDaV was successfully detected from R. porosum using RT-PCR (201).
3.12 Tospoviridae
Four viruses identified in roses have been classified within the family Tospoviridae. Tospoviruses are molecularly characterized by tripartite -ssRNA genomes ranging from ~12.3 to 16.7 kb in length (144). Structurally, the virions are enveloped, spherical to pleomorphic in shape, and range from 80 to 120 nm in diameter (144). These viruses are primarily transmitted by thrips (144).
3.12.1 Impatiens necrotic spot virus
Impatiens necrotic spot virus (INSV) is classified within the genus Orthotospovirus (species binomial: Orthotospovirus impatiensnecromaculae). While INSV is widely distributed across the globe, its presence in roses appears to be more localized. INSV has been detected in over 50 different host plants, but there are no molecular records available regarding its detection from roses. INSV was reported from Iran in ornamentals plants during a 2002 study, where roses were found to be infected (204). Later studies also confirmed that INSV was responsible for infection in roses (205). INSV is transmitted by thrips, particularly Frankliniella species (206).
3.12.2 Iris yellow spot virus
Iris yellow spot virus (IYSV) is classified within the genus Orthotospovirus (species binomial: Orthotospovirus iridimaculaflavi). While IYSV has been reported in several regions globally, molecular evidence from NCBI does not indicate its presence in roses. Within the USA, IYSV has been detected in other hosts but there are no specific reports of IYSV detection from roses. In the early 2000s, IYSV was detected from roses by serological assays in Iran (205). Although IYSV has rarely been reported in roses, it could potentially become an increasing threat to rose cultivation. Most reports of IYSV in the primary literature involve Allium sp (207–209). IYSV is primarily transmitted by thrips, with Thrips tabaci as the main vector (210).
3.12.3 Tomato spotted wilt virus
Tomato spotted wilt virus (TSWV) is classified within the genus Orthotospovirus (species binomial: Orthotospovirus tomatomaculae). Overall, there is no data available concerning the molecular characterization of TSWV in roses. TSWV is one of the most important plant viruses globally due to its widespread distribution and cosmopolitan nature (28, 211). It was first detected in the early 1900s in Australia, but the virus is believed to have originated from the New World (211). TSWV has been reported from roses in several studies. One of the earliest is from a possible case where ring patterns were observed on roses in the USA (212), but these symptoms differed from ringspot symptoms in more recent observations (30). In Iran, inoculation of TSWV from symptomatic roses to other host plants was demonstrated, which resulted in necrotic local lesions after inoculation (213). More recently, TSWV was detected for the first time from the UK in roses (84). Additional studies have incorporated TSWV assays when screening for viruses in roses, but TSWV was not detected (113). Typical symptoms associated with TSWV include necrotic lesions, wilting, mosaic, mottling, vein yellowing, ringspots, veinal chlorosis, and vein banding. In some cases, the virus may remain asymptomatic (28, 84). TSWV is transmitted by thrips (both persistent and propagative), grafting, and mechanical inoculation (28, 214).
3.12.4 Tomato yellow ring virus
Tomato yellow (fruit) ring virus (TYRV) is classified within the genus Orthotospovirus (species binomial: Orthotospovirus tomatanuli). TYRV was first reported in 2002 from Iran in tomatoes, where it was initially given the tentative name tomato yellow fruit ring virus (215). A synonym for TYRV is tomato varamin virus (205). In 2013, the complete nucleotide sequence of TYRV was characterized and the virus was designated as tomato yellow ring virus (216). While there are limited reports of this virus overall, even fewer have been documented in roses. In addition to Iran, TYRV has been reported from Poland and Kenya (217). According to available nucleotide data, TYRV has primarily been detected from tomato (Solanum lycopersicum). In 2005, TYRV was detected from roses in Iran (205). To date, TYRV appears to be largely localized in Iran and has only been minimally associated with roses. Notably, observable virus symptoms include chlorotic spots, mottling, leaf curling, and color breaking of petals (30). As with other orthotospoviruses, effective transmission of TYRV is rendered by thrips (Thrips tabaci, 218).
4 Tentative viruses or virus-like organisms affecting the genus Rosa
As mentioned in a previous section, there are several disease agents that are considered “phantom agents”, which supposedly caused disease in roses, but current evidence is inadequate (22). The virus or virus-like organisms listed below have been described in roses but are lacking important experimental confirmation, other than characterization by electron microscopy (EM). They have not been omitted, given their potential role in rose pathology. It is important to carefully evaluate these agents and avoid overstating their potential impact.
Rose necrotic mosaic virus (RoNMV) is a tentative virus with no molecular evidence for its detection. There is only one report on this virus, which includes characterization via electron microscopy, followed by analysis of the virion properties (750–800 nm) and genomic sequences (30, 108). In a subsequent publication, the same group did not provide further molecular characterization of RoNMV (219). This provisional virus has not been investigated in recent years and is likely no longer being considered as a novel virus of roses. RoNMV could potentially be a legitimate virus, but further study is required to confirm this.
Rose color break virus is a putative virus that has been previously described (29). To date, no molecular data is available to support its taxonomic classification, but biological evidence has been compiled since the late 1950s (220–222). Early investigations suggest that this disease agent may belong to the genus Tobamovirus (223). Further research is necessary to confirm its identity and clarify its etiological role in rose pathology.
5 Prospective management strategies and approaches
When assessing the impact of viral infections on plants, it is essential to consider both current management strategies and future preventative approaches. Unlike many other plant pathogens, viruses are difficult, if not impossible, to treat or eliminate once they have infected a host. Given the importance of roses as a highly desirable perennial plant, preventing and controlling viral infections in roses is paramount. The primary model for managing plant disease assumes the disease triangle, which involves the host, virus, vector, and environment (19). The goal is to disrupt one of these elements to prevent a virus from infecting another host. For example, if the vector responsible for transmitting a virus can be controlled, the virus may not be able to reach and infect a healthy host plant. To effectively manage viral diseases, it is essential to identify emerging viruses and ensure reliable detection of known viruses.
Virus discovery plays a crucial role in advancing virus detection methods and developing effective diagnostic strategies, especially as plant viruses continue to evolve. This knowledge is invaluable because interactions between different virus isolates (strains or species) within the same host may lead to higher recombination and reassortment potential. This may increase the severity of disease if a highly virulent strain or novel species emerges (128). In this way, virus discovery contributes to enhanced detection capabilities. For example, the discovery and characterization of RoPV in a 2016 study (145) paved the way for the identification of closely related viruses in other hosts by other researchers (224–227). This highlights the value of virus discovery in enhancing subsequent detection efforts. As new viruses and strains are identified, diagnostic assays become more robust, allowing for competent detection of all known strains of a particular virus or all viruses within a genus. In short, virus discovery contributes to reducing both economic loss and the risk of dynamic evolutionary events like recombination and reassortment of viruses, ultimately leading to improved outcomes.
Given the nature of viral infections and their persistence within the host, an imperative management strategy (if not the most important) is early virus detection followed by removal of the infected plant (228). This approach helps prevent the spread of the virus and minimizes economic losses. Several techniques have been used for early virus detection, including quantitative polymerase chain reaction (qPCR, 228), reverse transcription recombinase polymerase amplification (RT-RPA, 229), reverse transcription loop-mediated isothermal amplification (RT-LAMP, 127), and monoclonal and polyclonal antibodies (83, 95, 147, 230). It is essential that the chosen assay be highly sensitive, cost-effective, and time efficient. Early detection not only facilitates a prompt response but also provides opportunities for gaining further insights into plant viruses. However, it is important to consider that these viruses must first be detected before they can be managed.
Other key strategies for managing virus diseases in plants may include; 1) using novel technologies for more rapid virus detection, 2) educating growers and breeders on virus-like symptoms or other visual cues of infection, 3) developing resistant cultivars (either against the virus and/or vector), 4) exploring the use of antagonistic viruses to reduce the impacts of more virulent viruses (i.e. superinfection exclusion), 5) introducing predatory insects or other kinds of biocontrol, 6) applying insecticides to reduce insect vector populations, thereby reducing virus transmission, 7) certification programs that screen for economically important or harmful viruses, 8) elimination of viruses from infected plant materials using thermotherapy and meristem-tip culture, 9) planting virus-free germplasm, and 10) planting away from sources of infection. Overall, a combination of physical, chemical, and biological barriers can offer varying levels of protection against a viral pathogen.
In this review, we have provided information on the genomic content, distribution, and transmission mechanisms of each virus to help inform specific strategies for detecting and managing virus infection in roses. In terms of virus detection, DNA specific kits such as rolling circle amplification (RCA), would not be effective for identifying viruses that infect roses, as only two DNA viruses have been reported. Therefore, RNA-based detection assays are more appropriate for identifying these viruses. Regarding geographical distribution, we found that eighteen of the known viruses are present in the USA. This offers a foundation supporting the implementation of targeted screening programs that could help identify the virus responsible for a given disease. In terms of transmission, nine viruses discussed here are transmitted or potentially transmitted by aphids. If virus-like symptoms are observed in conjunction with aphids, researchers or landscapers can quickly narrow the possibilities of causation using the information provided in this review. The information provided here establishes a context-specific framework for the global management of viral diseases in roses. We hope that future management practices will be developed based on these insights, increasing the likelihood of interrupting the disease triangle as previously discussed.
6 Conclusions
Roses have shared a long and rich history with humans, dating back to antiquity. As highlighted in this review, roses are a valuable commodity in horticulture, contributing to the economy and enhancing the aesthetic appeal of landscape gardens. They also play a crucial role in supporting pollinating insects and animals. Like all plants, however, roses are vulnerable to disease caused by viruses. In this review, we described the characteristics of 37 viruses from roses. These viruses are taxonomically diverse, with the majority belonging to Bromoviridae, Betaflexiviridae, Secoviridae and Tospoviridae families. The Ilarvirus, Nepovirus, and Orthotospovirus genera are the most frequently represented among the known rose-infecting viruses. Additionally, several tentative viruses (RoNMV and rose color break virus) were discussed but require further experimental investigation. Genetically, most of these viruses are +ssRNA and have segmented genomes. Their distribution patterns vary, with some viruses being region-specific, whereas others have a more global presence. Notably, nearly half of the viruses reported in roses have been identified in the USA, while eighteen have not been reported in the New World. When examining virus transmission, we found that fourteen viruses are spread by insect vectors. Other common transmission methods include vegetative propagation and grafting. Lastly, we briefly reviewed current strategies for preventing the spread of viruses to other roses. Most available management options are preventative rather than curative, emphasizing the importance of virus discovery, early virus detection, and the removal of infected plants from the local environment. These approaches reduce the disease pressure and can potentially protect neighboring roses from infection. The response to a viral infection depends on the specific context, and the information presented here will aid in crafting informed, effective responses.
Plant viruses are fascinating acellular infectious entities that can significantly impact rose health, reducing yield, vigor, flower production, and the overall aesthetic appeal of roses. This review aims to provide a comprehensive overview of all the known viruses associated with roses, offering a valuable resource for growers, hobbyists, gardeners, and researchers. Collaborative efforts among rose cultivators and researchers will continue to expand our understanding of rose viruses and improve management strategies to protect our cherished roses from viral diseases.
Author contributions
CP: Formal analysis, Investigation, Methodology, Resources, Validation, Writing – original draft. AA: Conceptualization, Data curation, Funding acquisition, Project administration, Resources, Supervision, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research and/or publication of this article. We acknowledge the financial support provided by the USDA NIFA Specialty Crop Research Initiative Project: Developing Sustainable Rose Landscapes (2022-51181-38330).
Acknowledgments
The authors would like to express their gratitude to the University of Tulsa, the Graduate School, and the Department of Biological Sciences for their support. The authors would like to kindly thank the reviewers and editorial staff involved in enhancing the original manuscript.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords: roses, RNA viruses, DNA viruses, segmented viruses, transmission, disease management
Citation: Paslay C and Ali A (2025) A comprehensive review of known and emerging viruses infecting rose species. Front. Virol. 5:1669397. doi: 10.3389/fviro.2025.1669397
Received: 19 July 2025; Accepted: 03 November 2025;
Published: 24 November 2025.
Edited by:
Lev G. Nemchinov, United States Department of Agriculture (USDA), United StatesReviewed by:
John Hammond, United States Department of Agriculture, United StatesDimitre Mollov, United States Department of Agriculture (USDA), United States
Copyright © 2025 Paslay and Ali. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Akhtar Ali, YWtodGFyLWFsaUB1dHVsc2EuZWR1