Roses (Rosa) are one of the most valuable ornamental flowering shrubs around the globe. They are susceptible to numerous pathogens that require management, increasing the cost of cultivation. Rose rosette virus (RRV; genus Emaravirus) is a devastating virus that has been spreading since the 1940s in the United States and Canada. It is an emerging risk to European and worldwide rose cultivation, causing symptoms such as witches' broom, malformations, excessive thorn production, and eventually plant death. RRV is transmitted by the eriophyid mite Phyllocoptes fructiphilus and by grafting. Research is being undertaken to understand RRV and to find control measures and resistant cultivars, as they are not currently available. Early detection of the disease is the key to prevent the establishment and spread of RRV and its vector. Different molecular and serological diagnostic methods have been designed and implemented, including ELISA, RT-PCR, RT-qPCR, LAMP, and high-throughput sequencing. RRV infected plants can remain symptomless for long periods, so these diagnostic assays are necessary in conjunction with visual assessment to facilitate early detection. Significant social, economic, and environmental impacts are expected if RRV and its vector establish and spread in Europe. Rose trade between countries is the most likely pathway of introduction of RRV into Europe. In this review we describe current knowledge about RRV, the molecular and serological methods available for the detection of this virus, pathways to entry, and the possible impact if it establishes and spreads in Europe.

1 INTRODUCTION

Roses (Rosa spp.) are one of the most important ornamental species worldwide (Boskabady et al., 2011), not only for their industrial properties (Dobhal et al., 2016), but for their fragrance, beauty, and aesthetics. They are considered the national flower of several countries in Europe, including England. Repeat flowering varieties were introduced into Europe from China in the 18th century (Joyaux, 2003) transforming the concept of roses, showing a broader range of colours, growth types, flower sizes, and scents. From that time, extensive rose breeding has taken place across the world, creating a massive industry (Debener and Byrne, 2014).

Cultivation of roses is economically important around the globe. The estimated annual production of cut flowers is around 18 billion stems, 60–80 million potted plants (miniature roses and bare-root grafting plants), and 220 million plants for landscaping (Blom and Tsujita, 2003; Pemberton et al., 2003; Roberts et al., 2003). The world rose production was estimated to be valued at €24 billion (around £21 billion) in 2008 (Heinrichs, 2008). In the USA, total wholesale production of shrub roses was estimated to be worth $204 million in 2014 (less than £166 million), with 1,808 growers producing 36.6 million plants (United States Department of Agriculture, 2015). In terms of plants for planting, including bare-rooted plants, pot plants, cuttings/budwood, rootstock, and tissue culture, Serbia (36.34%) and China (30.81%) are the main countries from which the European Union (EU) imports roses (Table 1). Rosehips are also traded, used for different products such as rosehip jelly, water, or perfume (Leghari et al., 2016).

TABLE 1. Rose plants imported from non-EU countries to the EU from Jan 2014 to Dec 2018

Source country	Mean
Source country	kg	% of total
Serbia	281,740	36.34
China	238,880	30.81
South Africa	120,920	15.60
Uzbekistan	33,280	4.29
Kenya	20,920	2.70
Switzerland	20,560	2.65
Norway	13,040	1.68
Moldova	9,120	1.18
Ethiopia	6,120	0.79
South Korea	5,900	0.76
North Macedonia	5,880	0.76
Ukraine	5,540	0.71
Turkey	4,220	0.54
Morocco	3,860	0.50
United States	1,140	0.15
Sri Lanka	920	0.12
India	760	0.10
Belarus	620	0.08
Japan	620	0.08
Russian Federation	620	0.08
Ecuador	200	0.03
Lebanon	120	0.02
Israel	100	0.01
Colombia	60	0.01
Suriname	40	0.01
Thailand	40	0.01

Note

The table shows the percentage of the total imports originating from each country (Eurostat, 2019).

2 PEST AND PATHOGENS AFFECTING ROSES IN EUROPE

Roses are susceptible to numerous diseases that require management, increasing the cost of production. In the UK, the garden industry contributes £9 billion to the economy every year. Defra (Department for Environment, Food and Rural Affairs) valued general ornamental plant production at £1.1 billion in 2015, pointing out that diseases caused losses of £630 million annually in the UK to ornamental plant production, of which £40 million was due specifically to viral diseases (Department for Environment, Food and Rural Affairs, 2016; Little, 2016).

Roses are vulnerable to infections by bacteria, fungi, viruses, nematodes, and phytoplasmas, causing leaf and flower mosaics, distortion, spotting, discolouration, and necrosis, reducing growth or leading to death of the plant. Several fungal pathogens affect roses with a worldwide distribution. Black spot is the causal agent of the most serious fungal disease of roses grown outdoors in Europe and worldwide (Yasin et al., 2016). Rust is caused mainly by the fungi Phragmidium tuberculatum and Phragmidium mucronatum (Helfer, 2005), among other Phragmidium species, and is another common disease. Powdery mildew caused by Peronospora pannosa is the major fungal pathogen of roses grown in greenhouses, but can also be detected in the field (Schulz and Debener, 2010).

The management of pest and diseases in rose production is primarily achieved using agrochemicals. Restrictions imposed by plant protection legislation and the increasing ecological awareness of consumers have pushed breeders in line with plant pathologists to identify and characterize resistant cultivars (Schulz and Debener, 2010). Increasing disease resistance is especially necessary for garden roses, to inspire confidence amongst amateur rosarians, gardeners, and landscapers for their use in public areas (Leus et al., 2008).

The control of diseases in greenhouses is also important, because controlled environments enable a year-round supply of rose plants and cut flowers, even in seasons when outdoor temperatures or light conditions are not suitable for growth (Raviv et al., 2010). Rose varieties are commonly grown in greenhouses using rootstocks that favour a rapid economic multiplication of scions from desirable rose cultivars, which cannot be raised on their own roots (Tubbs, 1973). Rootstocks play an important role for economic aspects of propagation, flower production, flower quality, adaptation to different kinds of soil, and disease resistance (Fuchs, 1994). One of the most used rootstocks is Rosa multiflora.

3 ROSE VIRUSES REPORTED IN EUROPE

Several viruses have been reported affecting roses in Europe, including arabis mosaic virus (ArMV; genus Nepovirus), strawberry latent ringspot virus (SLRSV; family Secoviridae), apple mosaic virus (ApMV, genus Ilarvirus), and prunus necrotic ringspot virus (PNRSV; genus Ilarvirus; King et al., 2012). Rose mosaic disease (RMD) is one of the most common diseases of roses worldwide, and is caused by single or mixed infections of these viruses (Vazquez-Iglesias et al., 2019). Differences have been established between viruses involved in RMD occurring in North America and Europe, although PNRSV has been identified as the most frequent virus associated with this disease in both continents (Horst et al., 1983; Manners, 1997; Sertkaya, 2010). RMD is thought to have propagated in roses by grafting from infected rootstocks or scions, subsequently spreading among rose cultivars (Sertkaya, 2010). Viruses associated with RMD are considered to be transmitted by seeds, pollen, aphids, thrips, contaminated soil, or pruning tools, but no conclusive scientific evidence is available regarding transmission pathways (Horst and Cloyd, 2007). Golino et al. (2007) showed evidence of ApMV and PNRSV transmission via roots between roses growing close together in experimental fields.

Symptoms of RMD (Figure 1) vary depending on the variety, and include chlorotic line patterns, ring spots, mottles in leaves, yellow net, and mosaic. Infected plants are less vigorous and more likely to die over winter (Horst et al., 1983). PNRSV-infected plants have reduced quality with weaker shoots and fewer, smaller blooms, and are more likely to die after transplanting, generating losses in production. However, virus-infected plants can remain symptomless for much of the growing season, depending on the variety (Thomas, 1982).

Details are in the caption following the image — **FIGURE 1**
Open in figure viewer PowerPoint

Classic symptoms of rose mosaic disease include yellow netting and mosaic on leaves [Colour figure can be viewed at wileyonlinelibrary.com]

Rose cryptic virus-1 (RoCV1), also known as Rosa multiflora cryptic virus (Martin and Tzanetakis, 2008), is a partitivirus first reported in the USA (Sabanadzovic and Ghanem-Sabanadzovic, 2008) and subsequently in Canada (James et al., 2015), New Zealand (Milleza et al., 2013), and recently in the UK (Vazquez-Iglesias et al., 2019). Cryptic viruses escaped detection for many years because most cause no visible symptoms or, in a few cases, very mild symptoms (Milleza et al., 2013). Cryptic viruses occur in very low concentrations in infected plants (Hull, 2014). There are no known natural vectors, and no graft transmission or cell-to-cell movement. The reported mode of transmission is by cell division, pollen, or seed (Boccardo et al., 1987).

Rose yellow vein virus (RYVV) is a circular double-stranded (ds) DNA virus that has recently been reported in Turkey (Karanfil et al., 2018), but was first described in the USA and New Zealand (Perez-Egusquiza et al., 2013). RYVV belongs to family Caulimoviridae, genus Rosadnavirus (King et al., 2012), causing vein banding or central vein chlorosis in infected leaves (Milleza et al., 2013; Mollov et al., 2013).

4 ROSE ROSETTE VIRUS

Rose rosette virus (RRV) is a virus in the order Bunyavirales, genus Emaravirus, and is the causal agent of rose rosette disease (RRD; Laney et al., 2011), a damaging disease of roses in North America. RRV is a multipartite RNA virus consisting of seven single-stranded negative-sense RNA particles (RNA1–RNA7), encoding an RNA-dependent RNA polymerase (RdRp), a glycoprotein, a nucleocapsid, a movement protein, and p5, p6, and p7 proteins, respectively (Laney et al., 2011; Di Bello et al., 2015).

RRV was first described in the 1940s in Manitoba, Canada (Conners, 1941). At the same time, similar reports were made in Wyoming and California (Thomas and Scott, 1953). RRV is considered the most important viral disease of roses in the USA (Dobhal et al., 2016). Early studies suggested the cause of RRD could be related to phytoplasma (Gergerich and Kim, 1983), but the association of double-membrane-bound bodies and dsRNA (Doudrick and Millikan, 1983) with rosette-affected material indicated the involvement of a virus (Laney et al., 2011).

Numerous plant species have been assessed for the presence of RRV, but Rosa remains the only host genus identified (Laney et al., 2011). This occurrence may explain the small variation between RRV isolates (Laney et al., 2011), as host-driven diversity has not developed in RRV. Similarly, studies in European mountain ash ringspot-associated virus (EMARaV, the type species of Emaravirus) have also shown little sequence diversity (Kallinen et al., 2009; von Bargen et al., 2013). It may be hypothesized that the reported RRV low variability could be due to the virus replication in the vector, creating an evolutionary bottleneck where only variants replicating in both plant and mite are transmissible, such as the case of EMARaV and the mite Eriophyes pyri reported by Mielke-Ehret et al. (2010). However, further research is being undertaken to look for isolate variation in RRV (Byrne et al., 2019; Katsiani et al., 2020).

4.1 The beginning of RRD dissemination in North America

R. multiflora was introduced to North America from Japan during the early 1800s, as an ornamental for breeding proposes and as a rootstock (Rheder, 1936). Due to its hardiness and resistance to pests and diseases, it was used widely in amenity planting. For example, 14 million multiflora roses were planted in West Virginia alone between 1940 and 1960 (Dugan, 1960). R. multiflora was subsequently considered a weed (Dale et al., 1988) and in the early 2000s, the number of hectares covered by R. multiflora in the eastern USA reached 18 million (Loux et al., 2005).

RRV was considered an agent for the biological control of R. multiflora, on the assumption that rose plants would die within a period of 5 years (Epstein and Hill, 1999). Even though the US government was aware that the mite was a vector of the virus, they assessed the risk of spreading of RRD to other ornamental roses to be low (Amrine, 1996). However, as different types of roses grew in popularity, hundreds of thousands of RRV-susceptible plants were planted in private gardens and commercial beds, making it more likely that the virus would spread (Amrine, 1996).

4.2 RRV geographical distribution

RRV is currently present from the eastern coast of the USA to the Rocky Mountains and California (Center for Invasive Species and Ecosystem Health, 2019). It was thought to be endemic to North America until 2017, when it was reported for the first time in India (Chakraborty et al., 2017). R. multiflora is a widespread susceptible host, serving as a reservoir for both virus and vector. Beyond R. multiflora, RRD has been reported in different rose species such as R. arkansana, R. bracteate, R. canina, R. corymbifera, R. gallica, R. glauca, R. rubiginosa, R. spinossisima, R. villosa, R. woodsia, and in a multitude of types: climbers, hybrid teas, floribundas, miniatures, shrub, and antique roses (Martin, 2014).

4.3 Symptoms

Symptoms of RRV (Figure 2) are highly variable between rose cultivars, stage of the disease, and environmental factors (Epstein and Hill, 1995, 1999). Moreover, roses may harbour other viruses such as PNRSV and/or ApMV and their synergistic effect on symptom expression has not been determined. Symptoms of RRD include reddening on newly emerging shoots, excessive lateral shoot growth, excess thorn production, leaf mosaic, and mottling. Flowers tend to bunch together, forming witches' broom or rosetting, with malformed flowers (Laney et al., 2011; Dobhal et al., 2016). The virus moves throughout the plant affecting the roots, and plants show reduced growth and vigour compared to uninfected plants (Epstein and Hill, 1999). Other symptoms that may be expressed are darkening of canes, short internodal distances, blind shoots, rough leaf texture, and an increased susceptibility to infection, especially by fungal diseases (Hong et al., 2012). Infected plants die within 3–5 years of becoming infected (Di Bello et al., 2017).

Roses infected with RRV can show few or no symptoms during early stages of infection (Dobhal et al., 2016), and can remain symptomless for 30–146 days after transmission (Allington et al., 1968). Hence, by the time the first recognizable symptoms appear, the disease could have spread to nearby plants (Hong et al., 2012).

4.4 RRV transmission

Members of the genus Emaravirus are transmitted by eriophyid mites (Mielke-Ehret and Mühlbach, 2012). In early epidemiological studies, researchers theorized symptoms of RRV might be caused by eriophyid mite feeding toxicity (Slykhuis, 1980). Later experiments showed RRD was mite transmissible (Allington et al., 1968) and the pathogenicity of RRV was demonstrated by Di Bello et al. (2015). The eriophyid mite Phyllocoptes fructiphilus (Figure 3) is currently the only competent vector species identified (Keifer, 1966; Allington et al., 1968), although research has been undertaken with other Phyllocoptes species. The mite Phyllocoptes adalius is difficult to discriminate from P. fructiphilus morphologically because the prodorsal shield, which is used to distinguish them, is not visible with the naked eye (Druciarek et al., 2016). The identification of eriophyids is based on morphological observations, and sometimes ecological characteristics give important clues. Light and electron microscopy techniques are used to identify P. fructiphilus and differentiate it from other mite species. It is commonly found in the flowers, under stipules or vegetative bud scales (Otero-Colina et al., 2018). Whilst P. adalius is similar to P. fructiphilus, and a significant pest in its own right, causing serious damage due to feeding, it has been shown to not be an RRD vector (Amrine, 2002). Another mite species also considered for RRV transmission is Eriophyes eremus (Figure 3). This eriophyid mite is also found in roses, and was first described in Israel (Druciarek and Lewandowski, 2016). E. eremus was found in several states of the USA in 2018, colonizing native, naturalized, and ornamental rose cultivars (Otero-Colina et al., 2018), and like P. fructiphilus, it is also a microenvironment shelter seeking mite. Interest in E. eremus arose after being found in large numbers and as the only mite species feeding on a symptomatic, quantitative reverse transcription PCR (RT-qPCR)-positive plant (Solo, 2018). However, finding an E. eremus colony upon a rose specimen that tested positive to RRV may be circumstantial. Otero-Colina et al. (2018) have shown that no damage has been observed in association with this mite.

Eriophyids are small, typically between 140–170 µm, and unlike most mite species possess four, rather than eight legs. These mites are typically found in the angles formed between leaf petioles and axillary buds, feeding on plant tissues and overwintering on plants. Eriophyids are thought to survive for only 8 hr without a host. Eriophyids have a short life cycle of 8 days, and during that time can lay an egg a day (Kassar and Amrine, 1990). They do not have wings, but they can be transported by insects during pollination, dispersed by the wind, or by contact with clothing (Hong et al., 2012; Byrne et al., 2015). Jesse et al. (2006) showed roses with a higher density of leaves had a greater number of mites, because of a larger microhabitat availability, and they described a preference for sunny environments.

Currently, P. fructiphilus has only been described in North America, and is thought to be widely distributed in the USA on wild and commercial roses (Amrine, 2002). Although RRV has been reported in India, P. fructiphilus has not been detected and it is unknown if there is a vector present (Chakraborty et al., 2017; EPPO, 2019). Although mite transmission is the primary mechanism for spread in the field, RRV can also be transmitted by grafting (Amrine et al., 1988) and potentially by pollen (Babu et al., 2017a).

4.5 Early detection and biocontrol

The diagnosis of RRD in the early stages of infection is difficult. Symptoms are often confused with other pest problems, herbicide damage, nutrient deficiencies, or fungal infections. When glyphosate, a broad-spectrum systemic herbicide, contacts green tissue during autumn treatments, it is translocated to the buds and witches' broom symptoms with yellow leaves may appear during the following spring; this is easily confused with the rosetting caused by RRV (Hong et al., 2012). Also, manure contaminated with picloram + 2,4-dichlorophenoxyacetic acid, a systemic herbicide, can also cause the same symptoms when applied around roses (Davis et al., 2015).

Nevertheless, early detection is crucial, and identification and eradication of infected plants are necessary for effective control of RRD (Hong et al., 2012). Pruning out parts of plants with symptoms does not eliminate the virus and should be avoided to minimize the persistence of the virus after overwintering in the root system (Di Bello et al., 2017). Ideally, all multiflora roses in a 100 m radius should be removed, because they serve as a source of inoculum for RRV (Department for Environment, Food and Rural Affairs, 2016). The use of acaricides could decrease mite populations, reducing the risk of RRV dissemination. Acaricides may be useful to treat rose plants surrounding areas where RRV-infected plants have been removed (Hong et al., 2012). However, it is difficult to completely eliminate mites, because eriophyids hide in inaccessible areas of the plant (Otero-Colina et al., 2018).

There is no complete resistance or immunity reported in rose cultivars for RRD. Resistance to any pathogen depends on host genotype, the RRV isolate, the environment, the vector biology, and seasonality. The development of new resistant varieties is a long process that takes years. The stability of the prospective resistance is not known until later phases of testing, in which varieties are assessed in different locations within a range of environmental conditions and diversity of pathogens (Debener and Byrne, 2014). Amrine (2002) observed that rose species or varieties differ in RRV symptom expression and that there are likely to be differences in susceptibility or resistance to the virus. When a rose genotype shows resistance and robustness in a field with high RRV infestation, the molecular mechanism that makes this phenotype resistant can be studied to enable the use of resistant genetic material in breeding programmes (Byrne et al., 2015, 2019). Other rose species including R. acicularis, R. arkansana, R. blanda, R. californica, R. carolina, R. palustris, R. pisocarpa, R. setigera, and R. spinossisima have shown elevated levels of resistance to RRV infection. R. bracteata and Rosa ‘Meizeli’ (the “McCartney rose”) are resistant to feeding by the mite vector, although both are susceptible to the virus (Hong et al., 2012). Because the RRV genome is known, there are possibilities of applying gene-editing technology in the future. Research groups in the USA are making efforts to develop RRD-resistant roses: identifying genes linked to resistance, discriminating susceptible and resistant plants to the virus and to the mite, aiming to incorporate traits into elite rose germplasm (Byrne et al., 2015; Dobhal et al., 2016; Roundey et al., 2016).

4.6 Diagnostic techniques

Several techniques have been developed in the last few years for detection and diagnosis of RRV. Jordan et al. (2018) are developing polyclonal, monoclonal and/or single-chain antibodies and associated serology-based protocols, that is, ELISA (enzyme-linked immunosorbent assay), immunodip-stick (lateral flow), and immunocapture reverse transcription (RT)-PCR, for specific, reliable, and sensitive detection of RRV. ELISA is a versatile technique, widely used for routine virus testing in phytosanitary, quarantine, or virus certification applications (Boonham et al., 2014). However, ELISA requires the costly production of high-quality antisera with lack of cross reactivity to diverse pathogens and plant proteins, which may be seen as a disadvantage (Boonham et al., 2014) compared to nucleic acid-based methods, which are less costly to develop, more sensitive, and easier to manipulate to achieve the desired specificity (Schaad and Frederick, 2002; Arif and Ochoa-Corona, 2013; Arif et al., 2014). However, in the long run, once antisera are developed, it allows more throughput processing of samples and lower costs than nucleic acid-based methods.

RT-PCR is considered a sensitive and relatively rapid method for detection of RNA viruses. The first reported RRV detection method consists of an end-point RT-PCR with primers designed to amplify a fragment of RNA1 of the RRV genome (Table S1; Laney et al., 2011). Subsequent work showed the initial method to be inconsistent compared to other assays (Babu et al., 2016), which has led to the development of additional methods.

Di Bello et al. (2017) developed an RT-PCR assay designed in a highly conserved region of RNA3 of the RRV genome (Table S1). They proposed that RNA3 would be a better target because it codes for a nucleoprotein, so this gene would be transcribed at higher levels than the virus polymerase (RNA1). They used previously published sequences of 23 isolates available in GenBank for primer design and additional sequences from 107 isolates collected in different US states, thereby incorporating intravirus variation into the primer design. This assay was used in conjunction with primers designed to amplify the NADH dehydrogenase gene as an internal positive control in a multiplex PCR. Evaluation of the sensitivity was performed in comparison to the RT-PCR developed by Laney et al. (2011), and it was found to have higher sensitivity.

A different end-point RT-PCR was developed by Dobhal et al. (2016). The primers were designed to be compatible with two quantitative RT-PCR chemistries: TaqMan RT-PCR and SYBR Green combined with high-resolution melting (HRM) analysis, aimed at providing flexibility to diagnosticians with different resources or diagnostic preferences, because these techniques can be used with a single set of primers (Table S1). These proposed primers were designed using the nucleocapsid protein gene fragment (RNA3) of RRV as a template. The sequences of all RRV isolates available in NCBI GenBank at that time were considered. To verify the specificity of the primers, an in silico analysis was performed. Moreover, a panel of 11 reference control viruses was used for exclusivity assessment of the three techniques, and the limit of detection was determined to be 1 fg. Positive amplification was obtained with RRV-infected samples, and sequencing of the amplicon confirmed RRV was specifically amplified. The presence of phenolic compounds, carbohydrates, pigments, and other putative compounds in rose tissue were found to interfere during nucleic acid extraction (Dobhal et al., 2016). The use of PCR amplification facilitators bovine serum albumin (BSA) and polyvinylpyrrolidone (PVP) in the PCR mix improved amplification and helped avoid false negatives. BSA and PVP did not cross react or influence the specificity of the primer or the negative control.

Quantitative PCR (qPCR) based on TaqMan chemistry provides a greater specificity and speed compared to conventional end-point PCR for the detection of a pathogen, or a group of pathogens (Jenkins et al., 2002; Metzgar, 2011). In the case of RRV, both techniques have a comparable limit of detection. Babu et al. (2016) developed multiple primer/probe sets (Table S1) targeting three different regions of the RRV genome. Four primer/probe sets (RRV_2-1, RRV_2-2, RRV_3-2, RRV_3-5) and their corresponding product were tested in silico. Then the sensitivity (1 fg) was determined for the different assays. The specificity of the primer/probe sets in the presence/absence of other common rose-infecting viruses, and their reproducibility, was tested three times within a 30-day interval. By comparison with end-point RT-PCR, the RT-qPCR was more sensitive, detecting positive infected samples that gave negative results when using RT-PCR (Laney et al., 2011). In addition, positive detection of samples from different states of the USA indicated that the primer/probe sets had broad specificity.

Another TaqMan RT-qPCR assay for RRV detection was developed in 2017 at the Plant Health and Environment Laboratory (PHEL), New Zealand (author's unpublished data; Table S1). The primers and probe were designed based on the alignment of 27 RRV sequences of the nucleocapsid gene of RNA3 sourced from GenBank; the product size of the assay is 103 bp. An in silico assessment of this assay indicates that it is likely to detect all reported RRV isolates, and this is supported by results obtained showing two RRV isolates were successfully detected while samples of nontarget emaraviruses (fig mosaic virus and raspberry leaf blotch virus) and healthy rose plant tested negative. The described TaqMan RT-qPCR assay is currently the assay implemented by PHEL for RRV routine testing. Since 2018, a total of 214 rose samples have been tested for the presence of RRV, including postentry quarantine and domestic growers. RRV is not reported in New Zealand to date.

Recombinase-polymerase amplification (RPA) and loop-mediated isothermal amplification (LAMP) are simplified isothermal amplification techniques (Notomi et al., 2000; Piepenburg et al., 2006). Their advantages compared to other PCR methods are: (a) the reduction of reaction time to around 20 min; (b) the reaction runs at a constant low temperature (37–42°C for RPA, 65°C for LAMP), so there is no need for thermal cycler investment, enabling the use of simpler equipment; and (c) the potential to be transferable to the field for use as a simplified screening assay (Sen and Ashbolt, 2011).

Babu et al. (2017b) developed a basic gel-based RT-RPA assay. The method uses three different primer sets (RPA-131, RPA-267, RPA-321) designed to detect different regions of the RRV genomic RNA (Table S1). The specificity of the three sets of primers was assessed beforehand in silico against other common rose-infecting viruses, and was found to be 1 fg/µl. The method worked well with different tissue sources (leaves, petals, and stems), and with samples from different states of the USA.

A probe-based RT-recombinase-polymerase amplification (RT-exoRPA) assay for RRV was also described by Babu et al. (2017a). Primers were designed in the conserved regions of RRV genomic RNA3 (Table S1; RPA-267). Analysis in silico, assessment of the specificity, and limit of detection (1 fg/µl) were undertaken to assess this primer set. The developers of this technique envisioned commercial growers and nursery personnel performing the method on-site. Thus a quick viral RNA extraction method, named direct antigen-capture, was developed, which can be completed in around 5 min and allows the use of different types of plant tissues (Babu et al., 2017a).

RRV was detected in pollen (anthers) of RRV-infected roses with the RT-exoRPA analysis (Babu et al., 2017a). This finding suggested a new potential transmission pathway of the virus; however, further research is needed to confirm the finding and its significance. Sample collection still poses questions regarding which plant parts are best for sampling. The detection of RRV from the primary and secondary roots suggests they can be a good matrix for RRV detection, where the virus could overwinter, and allows the testing of plants even in the absence of leaves, green stems, and petals (Babu et al., 2017a). Roots can be tested in winter, and petals and leaves with symptoms during the rest of the year. This type of sampling proved to work well at the Oklahoma State University, Microbial Forensic Laboratory (Francisco Ochoa-Corona, personal communication). However, a statistically tested sampling technique for symptomless plants is yet to be demonstrated.

LAMP primers for RRV were designed after analysis of RRV P3 and P4 gene sequences using Primer Explorer software (https://primerexplorer.jp/e/; Salazar-Aguirre et al., 2016; Table S1). Alignment of the P3 and P4 RRV genes allowed precise LAMP primer design for broad detection of most reported isolates up to 2016 (Salazar-Aguirre et al., 2016). RRV-LAMP primers do not cross-react with cDNA reverse transcribed from 10 reference isolates of frequently coinfecting viruses in rose or RRV-related viruses: high plains wheat mosaic virus, maize stripe virus, impatiens necrotic spot virus, tomato spotted wilt virus, groundnut ringspot virus, ApMV, ArMV, PNRSV, tobacco ringspot virus, and tobacco mosaic virus. LAMP for RRV was tested successfully using tissue samples of RRD-infected roses with and without symptoms from Oklahoma. Healthy tissue and nontemplate controls were included in all reactions.

High-throughput sequencing (HTS) has revolutionized diagnostics since 2009 (Adams et al., 2009; Al Rwahnih et al., 2009; Kreuze et al., 2009). HTS offers the possibility of generic detection of viruses and other pathogens (Boonham et al., 2014), and allows a generic approach to virus identification that does not require previous knowledge of the targeted pathogens. HTS can deliver a species/strain-specific result (Adams and Fox, 2016). HTS continues to evolve, and different platforms and sample preparation methods have been developed (Pecman et al., 2017). A novel bioinformatic pipeline called electronic diagnostic nucleic acid analysis (EDNA) is being developed for the detection and diagnosis of 24 reported viruses infecting rose worldwide (Peña-Zuñiga et al., 2017). This computational tool combines HTS and bioinformatics, minimizes and ignores nonrelevant sequence data, and focuses on predetermined specific pathogen-associated sequences. It enables the detection of multiple viruses in a single sample or run (Figure 4) of either Illumina or Oxford Nanopore MinION raw metagenomic outputs.

4.7 Potential entry pathways to Europe

There are several potential entry pathways into the EU for RRV and its vector. Roses for planting are imported from different countries (as dormant plants free from leaves), including India and the USA. Although the percentage of imported plants from these countries is not high, the risk is elevated because 2,000 kg of roses are imported to Europe yearly from countries where this virus is present. Details about the rose species and varieties imported are unknown. R. multiflora is a regulated plant species in 13 US states, where its importation, distribution, trade, and sale have been banned (New York Invasive Species, 2019). Only dormant Rosa plants free from leaves, flowers, and fruit can be imported into the EU from non-European countries. However, the risk of RRV introduction and its vector persist because both can survive on dormant plants (EPPO, 2018). Thus, RRV has been regulated in the EU since November 2019, and roses imported from the USA, Canada, and India need to follow specific measures to avoid the introduction of RRV and P. fructiphilus (Andriukaitis, 2019). Moreover, roses may be imported illegally through internet trading or smuggling (Tuffen, 2016).

If RRV-infected plants were imported without the vector, the virus would be limited to that plant, except if used for propagation. Nevertheless, as reported, all plants showing symptoms of RRD are generally infested by P. fructiphilus (Otero-Colina et al., 2018) if imported from North America. The presence of just one female will be enough to initiate a population. In the case of introduction of nymph and adult stages of the vector, adults could be dispersed by wind or by other media, spreading the infection (Tuffen, 2016).

Other possible but less likely pathways are by natural spread or by the rosehip trade. The countries with the presence of RRV and P. fructiphilus are far from Europe, so vector transmission by wind is unlikely. Rosehips are generally used for domestic consumption therefore are unlikely to act as a pathway to the wider environment. The spreading of RRV by pollen needs to be further assessed by research (Babu et al., 2017a).

4.8 Cut flowers: a risk?

Rose rosette virus has not been reported infecting cut rose varieties yet, though it is highly probable they are susceptible. There are no-commercially available resistant or tolerant species. The possibility of finding flowers with symptoms in the market is low, because they would probably be graded out due to quality issues. Nevertheless, flowers could be taken from symptomless parts of an infected plant. The quality standards are high for cut roses, and under controlled conditions the use of agrochemicals could reduce the mite population.

The EU is a significant importer of fresh cut roses. This fact increases the risk of entrance of any exotic pathogen if phytosanitary measures are not effective. During the first 10 months of 2017, rose imports into the EU were valued at €624 million (£507 million), 10 times more than the value of exported roses to non-EU countries. According to Eurostat (2019), the Netherlands was the top EU exporter of cut flowers (70% of the total extra-EU exports of roses), as it is a major producer in Europe and receives cut flowers from other producer countries to redistribute them to the European market. After the Netherlands, other key exporters in Europe are Lithuania (11%), Germany (8%), and Latvia (7%). The Netherlands was also the top importer of fresh cut roses from outside the EU (77% of the total EU imports of roses). Other major importers were the UK (10%), Germany (6%), and Spain (5%). There is a minor trade of cut flowers with the USA (200 kg in 2016; Eurostat, 2019), and there is no trade with Canada. The trade with India increased from 300,000 to 900,000 kg in 2012–2016, mainly exported to the Netherlands and the UK (EPPO, 2018).

The possibility of RRV being introduced by cut flowers is unlikely, though not impossible if infected plants and vectors were found in an exporters production site. Cut flower shelf-life is around 2 weeks. Cut flowers are mostly used indoors, which reduces the risk of mites moving outdoors to transmit the virus in gardens. However, when the cut flowers are disposed of outdoors, for example in compost, mites may still be able to reach garden roses and transmit the virus.

4.9 RRV impact on the US industry and environment

Rose rosette virus has led to a significant decline of garden roses and urban landscapes of cities in the USA (Laney et al., 2011). The outbreak of RRV has been particularly evident in Tulsa and Oklahoma City (Oklahoma) and has affected the rose industry in other states (authors' personal observations). RRV infects randomly in the field with other viruses, creating new combinations of mixed infections in a large number of rose varieties and hybrids (Peña-Zuñiga et al., 2017), and threatens to decimate the US rose industry (Byrne et al., 2015).

In the USA about 35% of the rose sales are specifically used by the landscape industry. Recently, this market has reduced the use of roses by about 10% per year due to RRV and associated virus complexes. There are approximately 2,000 businesses that produce garden roses to sell in the USA. These growers produced 36.6 million garden-rose bushes in 2014 generating sales worth $203.5 million (£165.5 million), creating approximately $777 million (£632 million) for the US economy (Pemberton et al., 2018). The overall losses caused by RRV to present are being estimated and the official magnitude of the economic loss caused by the RRD is yet to be determined (communication with rose stakeholders at technical meetings).

4.10 Potential impact in Europe

For RRV introduction and establishment in Europe, it will require the introduction of its vector P. fructiphilus. The economic impact is expected to be high. Breeders, nurseries, retailers of garden and pot roses, and landscapes would be affected. Rose plants with symptoms would be unmarketable and eradication measures, which include destruction of plants in a range of 100 m even if they remain symptomless, will damage the economy of this sector (EPPO, 2018). The cost associated with replacement of rose plants in private and public landscaping will be high and the rose industry will be seriously affected by the introduction of alternative ornamentals into both the garden and landscape industry.

Bulgaria and Turkey are the largest producers of rose oil worldwide, which relies primarily on species like R. damascena, which is reported to be an RRV host (EPPO, 2018). In Bulgaria, the rose oil industry provides labour for c. 65,000 people, mostly seasonal workers (Kovacheva et al., 2010). In Turkey, 8,200 families grew oil roses in 2005 (Gunes, 2005).

The environment is also expected to be affected by RRV. In Europe there are several wild species known to be susceptible to the virus, for example R. canina and R. rubiginosa (EPPO, 2018). Roses are used for hedges, game cover, slope stabilization, and erosion control. Invertebrates that rely on Rosa spp. would also be affected, for example the gall-forming wasp Diplolepis spinosissimae. This insect causes the so-called robin's pincushion. A negative impact on pollinators is expected, as there are species that feed on roses. Pollinators have alternative sources available, but some have a specific relationship with these plants (Tuffen, 2016).

The introduction of RRV to Europe would also cause serious social impact, from affecting the mental and physical health benefits associated with gardening (Soga et al., 2017) to the loss of employment and income in the nursery industry and other associated sectors such as tourism, which rely heavily on public gardens and attractive urban landscapes. The availability of rose products with cultural importance like jam, rosehips, rose water, rose petals, or flower buds is likely to be reduced.

Rose germplasm repositories and unique European rose germplasm collections will be threatened, such as the “Europa-Rosarium Sangerhausen” (Germany), which is the largest rose collection in the world and plays an important role as a source of budwood and support for research.

5 CONCLUSIONS

Roses have a significant cultural value for a number of European countries (EPPO, 2018), and is a valuable flower crop worldwide affected by a range of pathogens. RRV is a devastating mite-transmitted virus that could potentially be introduced into Europe. The first finding of RRV outside North America has triggered interest and raised concern. The introduction pathway for RRV to India remains unknown. In view of the intercontinental distance between RRV-infected countries and Europe, the virus or the vector is unlikely to be introduced by natural spread, but other pathways of entry are possible.

Creating awareness plays a critical role in preventing RRV establishment. Thus, European governments should inform stakeholders and interested parties, including members of the public, about this virus, the disease that it causes, and the economic consequences. Simple tips to follow include spacing of plants to prevent mites crawling from plant to plant or implementing good hygiene measures to avoid spread (e.g., clean equipment before pruning, cleaning clothes). Breeders, nurseries, and botanic gardens should be informed and made aware about RRV and routine checks should be performed during the year. In the event of an outbreak, a prompt notification to the authorities to allow a regulatory response must be quick.

Controls within rose trading countries are key to prevent the introduction of RRV. Early detection and surveillance programmes are necessary, because plants can have long latent periods, during which the mite vector can spread the virus. Regular inspection throughout the growing season with destruction of plants with symptoms appears to be the most effective control measure for RRV at present. Visual diagnosis of RRV requires serological or molecular confirmation during the early stages of infection (Figure 5). Several diagnostic methods have been developed and incorporating these into early detection strategies is essential to intercept the virus and vector before it is able to establish. The different diagnostic methods available enable techniques to be chosen depending on the resources available for each laboratory (Babu et al., 2018). All the techniques available are useful for detecting an outbreak, within the limit of detection and capacities of the assay. RT-qPCR is a good option, due to its high sensitivity compared with RT-PCR or ELISA. HTS has a potential as a front-line diagnostic tool, in particular for screening multiple virus infections in propagation material, but further research work is in process. RRV testing must be rapid to target symptomless infections because these are common. In the case of an outbreak, an eradication and tracing programme should be followed. First, suspect plants are to be tested to confirm the presence of RRV, and if positive, infested and adjacent plants (including the roots) are to be destroyed. Inspect for presence of the vector and forbid movement of rose plants from the site of the RRV outbreak. Precautions should be taken to avoid spreading the vector during the response (e.g., bagging plants before any manipulation to avoid dispersing the vector). In addition, nearby host plants must be treated with acaricides. If occurring in a glasshouse, the whole glasshouse should be disinfested (EPPO, 2018).

Following an outbreak, delimiting surveys of the area surrounding the infected plants are needed, including visual surveys. Trace-forward and -back analysis should be conducted to identify possible areas where infected plants might be present. Surveys of Rosa plants in late spring and summer should be performed each year and for at least 2 years after the outbreak of the first infection due to the long incubation period of RRV. Similar surveys should be carried out for vector infestations before declaring the outbreak eradicated. No Rosa spp. should be moved out of risk demarcated areas until the eradication is declared successful (EPPO, 2018).

Another measure to limit the spread of RRV is to import roses from an RRV and P. fructiphilus pest-free area (PFA), as England and Wales (UK) have now declared (Department for Environment, Food and Rural Affairs, 2019). Other considerations should be taken, for example the packing conditions to prevent infestation by P. fructiphilus during transport, and pre- or postentry quarantine period for at least one growing season. This should include visual inspection for RRV and P. fructiphilus and molecular testing for RRV.

5.1 Future directions

Further research is needed to identify other possible RRV vectors or transmission pathways, as well as to improve understanding of RRV variability and diversity. The susceptibility of cut rose varieties needs to be assessed, as they could play an important role in the spread of RRV and its vector if infection can occur. Resistant varieties adapted to European hardiness zones need to be developed and released to reduce the impact and spread of RRV in advance. An effective educational programme is required to inform the general public and create awareness regarding RRV, all of which will help to develop a quick response in case of an RRV outbreak.

ACKNOWLEDGEMENTS

We thank Dr Gary R. Bauchan for sharing the scanning electron microscopy images of Phyllocoptes fructiphilus and Eriophyes eremus, and Dr Alan McLeod and Dr Melanie Tuffen for their help with the use of Eurostat.

Open Research

DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were created or analysed in this study.

Supporting Information

REFERENCES

Adams, I. and Fox, A. (2016) Diagnosis of plant viruses using next-generation sequencing and metagenomic analysis. In: A. Wang and X. Zhou (Eds.) Current Research Topics in Plant Virology. Cham: Springer International Publishing. 323–335.
10.1007/978-3-319-32919-2_14
Google Scholar
Adams, I.P., Glover, R.H., Monger, W.A., Mumford, R., Jackeviciene, E., Navalinskiene, M. et al. (2009) Next-generation sequencing and metagenomic analysis: a universal diagnostic tool in plant virology. Molecular Plant Pathology, 10, 537–545.
10.1111/j.1364-3703.2009.00545.x
CASPubMedWeb of Science®Google Scholar
Al Rwahnih, M., Daubert, S., Golino, D. and Rowhani, A. (2009) Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology, 387, 395–401.
10.1016/j.virol.2009.02.028
CASPubMedWeb of Science®Google Scholar
Allington, W.B., Staples, R. and Viehmeyer, G. (1968) Transmission of rose rosette by the eriophyid mite, Phyllocoptes fructiphilus. Journal of Economic Entomology, 61, 1137–1140.
10.1093/jee/61.5.1137
Web of Science®Google Scholar
Amrine, J. (1996) 4.1.2 Phyllocoptes fructiphilus and biological control of multiflora rose. World Crop Pests, 6, 741–749.
10.1016/S1572-4379(96)80050-9
Google Scholar
Amrine, J.J. (2002) Multiflora rose. In: F. Driesche, B. Blossey, M. Hoodle, S. Lyon and R. Reardon (Eds.) Biological Control of Invasive Plants in the Eastern United States. Morgantown, WV: USDA. 741–749.
Google Scholar
Amrine, J., Hindal, D., Stasny, T., Williams, R. and Coffman, C. (1988) Transmission of the rose rosette disease agent to Rosa multiflora by Phyllocoptes fructiphilus (Acari: Eriophyidae). Entomological News, 99, 239–252.
Web of Science®Google Scholar
Andriukaitis, V. (2019) Commission implementing decision (EU) 2019/1739 of 16 October 2019 establishing emergency measures to prevent the introduction into and the spread within the Union of rose rosette virus (notified under document C (2019) 7328). Official Journal of the European Union, 62, L 265/12.
Google Scholar
Arif, M. and Ochoa-Corona, F.M. (2013) Comparative assessment of 5′ A/T-rich overhang sequences with optimal and sub-optimal primers to increase PCR yields and sensitivity. Molecular Biotechnology, 55, 17–26.
10.1007/s12033-012-9617-5
CASPubMedWeb of Science®Google Scholar
Arif, M., Aguilar-Moreno, G., Wayadande, A., Fletcher, J. and Ochoa-Corona, F.M. (2014) Primer modification improves rapid and sensitive in vitro and field-deployable assays for detection of high plains virus variants. Applied and Environmental Microbiology, 80, 320–327.
10.1128/AEM.02340-13
CASPubMedWeb of Science®Google Scholar
Babu, B., Jeyaprakash, A., Jones, D., Schubert, T.S., Baker, C., Washburn, B.K. et al. (2016) Development of a rapid, sensitive TaqMan real-time RT-PCR assay for the detection of rose rosette virus using multiple gene targets. Journal of Virological Methods, 235, 41–50.
10.1016/j.jviromet.2016.05.010
CASPubMedWeb of Science®Google Scholar
Babu, B., Washburn, B.K., Ertek, T.S., Miller, S.H., Riddle, C.B., Knox, G.W. et al. (2017a) A field-based detection method for rose rosette virus using isothermal probe-based reverse transcription-recombinase polymerase amplification assay. Journal of Virological Methods, 247, 81–90.
10.1016/j.jviromet.2017.05.019
CASPubMedWeb of Science®Google Scholar
Babu, B., Washburn, B.K., Miller, S.H., Poduch, K., Sarigul, T., Knox, G.W. et al. (2017b) A rapid assay for detection of rose rosette virus using reverse transcription-recombinase polymerase amplification using multiple gene targets. Journal of Virological Methods, 240, 78–84.
10.1016/j.jviromet.2016.11.014
CASPubMedWeb of Science®Google Scholar
Babu, B., Knox, G., Paret, M.L. and Ochoa-Corona, F.M. (2018) Rose rosette disease: recent advances on molecular diagnostic tools. HortScience, 53, 596–600.
10.21273/HORTSCI12551-17
CASWeb of Science®Google Scholar
von Bargen, S., Arndt, N., Robel, J., Jalkanen, R. and Büttner, C. (2013) Detection and genetic variability of European mountain ash ringspot-associated virus (EMARaV) in Sweden. Forest Pathology, 43, 429–432.
10.1111/efp.12046
Web of Science®Google Scholar
Blom, T. and Tsujita, M. (2003) Cut rose production. In: A. Roberts, T. Debener and S. Gudin (Eds.) Encyclopedia of Rose Science. Amsterdam: Elsevier Academic Press, pp. 594–600.
10.1016/B0-12-227620-5/00178-6
Google Scholar
Boccardo, G., Lisa, V., Luisoni, E. and Milne, R. (1987) Cryptic plant viruses. Advances in Virus Research, 32, 171–214.
10.1016/S0065-3527(08)60477-7
CASPubMedWeb of Science®Google Scholar
Boonham, N., Kreuze, J., Winter, S., van der Vlugt, R., Bergervoet, J., Tomlinson, J. et al. (2014) Methods in virus diagnostics: from ELISA to next generation sequencing. Virus Research, 186, 20–31.
10.1016/j.virusres.2013.12.007
CASPubMedWeb of Science®Google Scholar
Boskabady, M.H., Shafei, M.N., Saberi, Z. and Amini, S. (2011) Pharmacological effects of Rosa damascena. Iranian Journal of Basic Medical Sciences, 14, 295–307.
CASPubMedWeb of Science®Google Scholar
Byrne, D.H., Roundey, E., Klein, P. and Yan, M. (2015) Combating rose rosette disease: are there resistant roses?.American Rose, 78–83. https://neilsperry.com/wp-content/uploads/2016/05/SeptOct15_RRD.pdf.
Google Scholar
Byrne, D.H., Klein, P., Hall, C., Windham, M., Ochoa-Corona, F., Olson, J. et al. (2019) Combating rose rosette disease US national project. Acta Horticulturae, 1232, 203–212.
10.17660/ActaHortic.2019.1232.30
Google Scholar
Center for Invasive Species and Ecosystem Health. (2019) Rose rosette. Athens, GA, USA: University of Georgia. Available at: https://roserosette.org/ [Accessed 16 January 2019]
Google Scholar
Chakraborty, P., Das, S., Saha, B., Karmakar, A., Saha, D. and Saha, A. (2017) Rose rosette virus: an emerging pathogen of garden roses in India. Australasian Plant Pathology, 46, 223–226.
10.1007/s13313-017-0479-y
CASWeb of Science®Google Scholar
Conners, L. (1941). Twentieth Annual Report of the Canadian Plant Report Survey, 1940. Ottawa: Domain of Canada Department of Agriculture Science Service, Division of Botany and Plant Pathology.
Google Scholar
Dale, F.H., Amrine, J.W., Williams, R.L. and Terry, A.S. (1988) Rose rosette disease on multiflora rose (Rosa multiflora) in Indiana and Kentucky. Weed Technology, 2, 442–444.
10.1017/S0890037X00032243
Web of Science®Google Scholar
Davis, J., Johnson, S.E. and Jennings, K. (2015) Herbicide Carryover in Hay, Manure, Compost, and Grass Clippings. Raleigh, NC: North Carolina Cooperative Extension.
Google Scholar
Debener, T. and Byrne, D.H. (2014) Disease resistance breeding in rose: current status and potential of biotechnological tools. Plant Science, 228, 107–117.
10.1016/j.plantsci.2014.04.005
CASPubMedWeb of Science®Google Scholar
Department for Environment, Food and Rural Affairs. (2016) National Statistics. Agriculture in the United Kingdom 2015. London: Department for Environment, Food and Rural Affairs.
Google Scholar
Department for Environment, Food and Rural Affairs. (2019) Explanatory Memorandum to the Plant Health (England) Order 2019 No. 1070. London: Department for Environment, Food and Rural Affairs.
Google Scholar
Di Bello, P.L., Ho, T. and Tzanetakis, I.E. (2015) The evolution of emaraviruses is becoming more complex: seven segments identified in the causal agent of rose rosette disease. Virus Research, 210, 241–244.
10.1016/j.virusres.2015.08.009
CASPubMedWeb of Science®Google Scholar
Di Bello, P.L., Thekke-Veetil, T., Druciarek, T. and Tzanetakis, I.E. (2017) Transmission attributes and resistance to rose rosette virus. Plant Pathology, 67, 499–504.
10.1111/ppa.12738
Web of Science®Google Scholar
Dobhal, S., Olson, J.D., Arif, M., Garcia Suarez, J.A. and Ochoa-Corona, F.M. (2016) A simplified strategy for sensitive detection of rose rosette virus compatible with three RT-PCR chemistries. Journal of Virological Methods, 232, 47–56.
10.1016/j.jviromet.2016.01.013
CASPubMedWeb of Science®Google Scholar
Doudrick, R. and Millikan, D. (1983) Some etiological and symptomatological aspects of rose rosette. Phytopathology, 73, 840.
Web of Science®Google Scholar
Druciarek, T. and Lewandowski, M. (2016) A new species of eriophyoid mite (Acari: Eriophyoidea) on Rosa sp. from Israel. Zootaxa, 4066, 323–330.
10.11646/zootaxa.4066.3.8
PubMedWeb of Science®Google Scholar
Druciarek, T., Kozak, M., Maroufpoor, M. and Lewandowski, M. (2016) Morphological variability of Phyllocoptes adalius female forms (Acari: Eriophyoidea), with a supplementary description of the species. Systematic and Applied Acarology, 21, 181–194.
10.11158/saa.21.2.3
Web of Science®Google Scholar
Dugan, R. (1960) Multiflora rose in West Virginia. West Virginia University Agricultural Experiment Station Bulletin, 447, 1–32.
Google Scholar
EPPO. (2018) Pest risk analysis for Rose rosette virus and its vector Phyllocoptes fructiphilus. Paris: EPPO.
Google Scholar
EPPO. (2019) EPPO Global Database. Available at: https://gd.eppo.int. [Accessed 16 February 2019].
Google Scholar
Epstein, A. and Hill, J.H. (1995) The biology of rose rosette disease: a mite-associated disease of uncertain aetiology. Journal of Phytopathology, 143, 353–360.
10.1111/j.1439-0434.1995.tb00275.x
Web of Science®Google Scholar
Epstein, A. and Hill, J. (1999) Status of rose rosette disease as a biological control for multiflora rose. Plant Disease, 83, 92–101.
10.1094/PDIS.1999.83.2.92
CASPubMedWeb of Science®Google Scholar
Eurostat. (2019) European Commision Eurostat. Available at: https://ec.europa.eu/eurostat/web/main/home. [Accessed 30 April 2019].
Google Scholar
Fuchs, H. (1994) Scion-rootstock Relationships and Root Behaviour in Glasshouse Roses. PhD thesis, Wageningen: Wageningen University & Research.
Google Scholar
Gergerich, R.C. and Kim, K.S. (1983) A description of the causal agent of rose rosette disease. Arkansas Farm Research, 32, 7.
Web of Science®Google Scholar
Golino, D., Sim, S., Cunningham, M. and Rowhani, A. (2007) Transmission of rose mosaic viruses. Acta Horticulturae, 751, 217–224.
10.17660/ActaHortic.2007.751.26
Google Scholar
Gunes, E. (2005) Turkey rose oil production and marketing: a review on problem and opportunities. Journal of Applied Sciences, 10, 1871–1875.
Google Scholar
Heinrichs, F. (2008) International Statistics Flowers and Plants. Didcot, UK: AIPH, Union Fleurs.
Google Scholar
Helfer, S. (2005) Overview of the rust fungi (Uredinales) occurring on Rosaceae in Europe. Nova Hedwigia, 81, 325–370.
10.1127/0029-5035/2005/0081-0325
Web of Science®Google Scholar
Hong, C., Hansen, M.A. and Day, E. (2012) Rose rosette disease. Virginia State University Cooperative Extension, 450-620 1–4.
Google Scholar
Horst, R. and Cloyd, R. (2007) Compendium of Rose Diseases and Pests. St Paul, MN, USA: American Phytopathological Society.
Google Scholar
Horst, R.K., Society, A.P. and Cornell University. (1983). Compendium of Rose Diseases. St. Paul, MN, USA: American Phytopathological Society in cooperation with Dept. of Plant Pathology, Cornell University.
Google Scholar
Hull, R. (2014) Plant Virology. Norwich, UK: Elsevier.
Google Scholar
James, D., Phelan, J., Varga, A. and Rott, M. (2015) First report of rose cryptic virus-1 in Rosa plants in Canada. Plant Disease, 99, 558.
10.1094/PDIS-09-14-0921-PDN
Web of Science®Google Scholar
Jenkins, G.M., Rambaut, A., Pybus, O.G. and Holmes, E.C. (2002) Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. Journal of Molecular Evolution, 54, 156–165.
10.1007/s00239-001-0064-3
CASPubMedWeb of Science®Google Scholar
Jesse, L.C., Moloney, K.A. and Obrycki, J.J. (2006) Abundance of arthropods on the branch tips of the invasive plant, Rosa multiflora (Rosaceae). Weed Biology and Management, 6, 204–211.
10.1111/j.1445-6664.2006.00222.x
Web of Science®Google Scholar
Jordan, R., Guaragna, M.A. and Hammond, J. (2018) Development of polyclonal and monoclonal antibodies to rose rosette virus nucleoprotein. Acta Horticulture, 1193, 77–82.
10.17660/ActaHortic.2018.1193.11
Google Scholar
Joyaux, F. (2003) History of rose cultivation. European (pre-1800). In: A. Roberts, T. Debener and S. Gudin (Eds.) Encyclopedia of Rose Science. London: Elsevier Academic Press, pp. 395–402.
10.1016/B0-12-227620-5/00047-1
Google Scholar
Kallinen, A., Lindberg, I., Tugume, A. and Valkonen, J.P.T. (2009) Detection, distribution, and genetic variability of European mountain ash ringspot-associated virus. Phytopathology, 99, 344–352.
10.1094/PHYTO-99-4-0344
CASPubMedWeb of Science®Google Scholar
Karanfil, A., Randa-Zelyüt, F., Ertunç, F. and Korkmaz, S. (2018) First report of Rose yellow vein virus in Turkey. New Disease Reports, 38, 11.
10.5197/j.2044-0588.2018.038.011
Google Scholar
Kassar, A. and Amrine, J.J. (1990) Rearing and development of Phyllocoptes fructiphilus (Acari: Eriophyidae). Entomological News, 101, 276–282.
Web of Science®Google Scholar
Katsiani, A., Stainton, D., Lamour, K. and Tzanetakis, I.E. (2020) The population structure of Rose rosette virus in the USA. Journal of General Virology. 101, 676–684.
10.1099/jgv.0.001418
CASPubMedWeb of Science®Google Scholar
Keifer, H. (1966) Eriophyid Studies B-21. Sacramento, CA, USA: Bureau of Entomology, California Department of Agriculture.
Google Scholar
King, A., Lefkowitz, E., Adams, M. and Carstens, E. (2012) Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses, London: Elsevier.
Google Scholar
Kovacheva, N., Rusanov, K. and Atanassov, I. (2010) Industrial cultivation of oil bearing rose and rose oil production in Bulgaria during 21st century, directions and challenges. Biotechnology & Biotechnological Equipment, 24, 1793–1798.
10.2478/V10133-010-0032-4
Web of Science®Google Scholar
Kreuze, J.F., Perez, A., Untiveros, M., Quispe, D., Fuentes, S., Barker, I. et al. (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology, 388, 1–7.
10.1016/j.virol.2009.03.024
CASPubMedWeb of Science®Google Scholar
Laney, A.G., Keller, K.E., Martin, R.R. and Tzanetakis, I.E. (2011) A discovery 70 years in the making: characterization of the rose rosette virus. Journal of General Virology, 92, 1727–1732.
10.1099/vir.0.031146-0
CASPubMedWeb of Science®Google Scholar
Leghari, A., Ali Leghari, U., Abdul, H. and Ahmed, T. (2016) Cultivation of rose (Rosa indica L.). Journal of Floriculture and Landscaping, 2, 1–4.
Google Scholar
Leus, L., Van Hylenbroeck, J., Van Bockstaele, E. and Höfte, M. (2008) Early selection of garden rose seedling for powdery mildew resistance. European Journal of Horticultural Science, 73, 5–11.
Web of Science®Google Scholar
Little, E.L. (2016) Georgia Plant Disease Loss Estimates 2014. Athens, GA, USA: University of Georgia. UGA Extension AP 102-7.
Google Scholar
Loux, M., Underwood, J., Amrine, J., Bryan, W. and Chandran, R. (2005) Multiflora rose control. Columbus: The Ohio State University Bulletin.
Google Scholar
Manners, M. (1997) Effects of rose mosaic disease on performance of hybrid tea roses in Florida. Proceedings of the Florida State Horticultural Society, 110, 118–121.
Google Scholar
Martin, C. (2014) Rose rosette disease and the impacts on propagation. Acta Horticulturae, 1055, 319–321.
10.17660/ActaHortic.2014.1055.68
Google Scholar
Martin, R.R. and Tzanetakis, I.E. (2008) First report of rosa multiflora cryptic virus in Rosa multiflora in the eastern United States. Plant Disease, 92, 1706.
10.1094/PDIS-92-12-1706B
CASPubMedWeb of Science®Google Scholar
Metzgar, D. (2011) Adaptive evolution of diagnostic resistance. Journal of Clinical Microbiology, 49, 2774–2775.
10.1128/JCM.02334-10
PubMedWeb of Science®Google Scholar
Mielke-Ehret, N. and Mühlbach, H.-P. (2012) Emaravirus: a novel genus of multipartite, negative strand RNA plant viruses. Viruses, 4, 1515–1536.
10.3390/v4091515
CASPubMedWeb of Science®Google Scholar
Mielke-Ehret, N., Thoma, J., Schlatermund, N. and Muhlbach, H.P. (2010) Detection of European mountain ash ringspot-associated virus-specific RNA and protein P3 in the pear leaf blister mite Phytoptus pyri (Eriophyidae). Archives of Virology, 155, 987–991.
10.1007/s00705-010-0667-3
CASPubMedWeb of Science®Google Scholar
Milleza, E.J.M., Ward, L.I., Delmiglio, C., Tang, J.Z., Veerakone, S. and Perez-Egusquiza, Z. (2013) A survey of viruses infecting Rosa spp. in New Zealand. Australasian Plant Pathology, 42, 313–320.
10.1007/s13313-012-0191-x
Web of Science®Google Scholar
Mollov, D., Lockhart, B., Zlesak, D. and Olszewski, N. (2013) Complete nucleotide sequence of rose yellow vein virus, a member of the family Caulimoviridae having a novel genome organization. Archives of Virology, 158, 877–880.
10.1007/s00705-012-1547-9
CASPubMedWeb of Science®Google Scholar
New York Invasive Species. (2019) New York Invasive Species (IS) Information. Available at: http://nyis.info/invasive_species/multiflora-rose/ [Accessed 10 May 2019].
Google Scholar
Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N. et al. (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Research, 28, E63.
10.1093/nar/28.12.e63
CASPubMedWeb of Science®Google Scholar
Otero-Colina, G., Ochoa, R., Amrine, J.W. Jr, Hammond, J., Jordan, R. and Bauchan, G.R. (2018) Eriophyoid mites found on healthy and rose rosette diseased roses in the United States. Journal of Environmental Horticulture, 36, 146–153.
10.24266/0738-2898-36.4.146
Google Scholar
Pecman, A., Kutnjak, D., Gutiérrez-Aguirre, I., Adams, I., Fox, A., Boonham, N. et al. (2017) Next generation sequencing for detection and discovery of plant viruses and viroids: comparison of two approaches. Frontiers in Microbiology, 8, 1998.
10.3389/fmicb.2017.01998
PubMedWeb of Science®Google Scholar
Pemberton, H., Kelly, J. and Ferare, J. (2003) Pot rose production. In: A. Roberts, T. Debener and S. Gudin (Eds.) Encyclopedia of Rose Science. Amsterdam: Elsevier Academic Press, pp. 587–593.
10.1016/B0-12-227620-5/00074-4
Google Scholar
Pemberton, H.B., Ong, K., Windham, M., Olson, J. and Byrne, D.H. (2018) What is rose rosette disease? HortScience, 53, 592.
10.21273/HORTSCI12550-17
CASWeb of Science®Google Scholar
Peña-Zuñiga, L., Espindola, A.S., Klein, P., Debener, T., Rees, J., Byrne, D. et al. (2017) EDNA-Rose a novel approach for detecting rose viruses combining next generation sequencing and bioinformatics. Phytopathology, 107(S5), 58.
Google Scholar
Perez-Egusquiza, Z., Liefting, L. and Ward, L. (2013) First report of rose yellow vein virus in Rosa sp. in New Zealand. Plant Disease, 97, 1122.
10.1094/PDIS-10-12-0981-PDN
CASPubMedWeb of Science®Google Scholar
Piepenburg, O., Williams, C.H., Stemple, D.L. and Armes, N.A. (2006) DNA detection using recombination proteins. PLoS Biology, 4, e204.
10.1371/journal.pbio.0040204
CASPubMedWeb of Science®Google Scholar
Raviv, M., Medina, S., Wendin, C. and Lieth, J.H. (2010) Development of alternate cut-flower rose greenhouse temperature set-points based on calorimetric plant tissue evaluation. Scientia Horticulturae, 126, 454–461.
10.1016/j.scienta.2010.08.011
Web of Science®Google Scholar
Rheder, A. (1936) On the history of the introduction of woody plants into North America. Natural Horticultural Magazine, 15, 245–257.
Google Scholar
Roberts, A., Debener, T. and Gudin, S. (2003) Introduction. In: A. Roberts, T. Debener and S. Gudin (Eds.) Encyclopedia of Rose Science. Amsterdam: Elsevier Academic Press, pp. 1–2.
Google Scholar
Roundey, E., Anderson, N., Bedard, C., Scheiber, M. and Byrne, D.H. (2016) Evaluation of Rosa palustris as a parent for breeding rose rosette disease-resistant roses. In: Proceedings of ASHS Atlanta 2016. Available at https://ashs.confex.com/ashs/2016/webprogram/Paper23444.html. [Accessed 4 August 2020].
Google Scholar
Sabanadzovic, S. and Ghanem-Sabanadzovic, N.A. (2008) Molecular characterization and detection of a tripartite cryptic virus from rose. Journal of Plant Pathology, 90, 287–293.
CASWeb of Science®Google Scholar
Salazar-Aguirre, A., Molina-Cárdenas, S., Ochoa-Corona, F. and Olson, J. (2016) Rose rosette virus detection using loop-mediated isothermal amplification (LAMP). Phytopathology, 106, S4.117.
Web of Science®Google Scholar
Schaad, N.W. and Frederick, R.D. (2002) Real-time PCR and its application for rapid plant disease diagnostics. Canadian Journal of Plant Pathology, 24, 250–258.
10.1080/07060660209507006
CASWeb of Science®Google Scholar
Schulz, D. and Debener, T. (2010) Downy mildew in roses: strategies for control. Acta Horticulturae, 870, 163–170.
10.17660/ActaHortic.2010.870.21
Google Scholar
Sen, K. and Ashbolt, N. (2011) Environmental Microbiology: Current Technology and Water Application. Norfolk, UK: Caister Academic Press.
Google Scholar
Sertkaya, G. (2010) An investigation of rose mosaic disease of rose in Hatay-Turkey. Julius-Kühn-Archive, 427, 309–313.
Google Scholar
Slykhuis, J. (1980) Mites. In: K. Harris and K. Maramorosch (Eds.) Vectors of Plant Pathogens. New York: Academic Press, pp. 325–356.
10.1016/B978-0-12-326450-3.50018-8
Google Scholar
Soga, M., Gaston, K.J. and Yamaura, Y. (2017) Gardening is beneficial for health: a meta-analysis. Preventive Medicine Reports, 5, 92–99.
10.1016/j.pmedr.2016.11.007
PubMedGoogle Scholar
Solo, K.M. (2018) Rose Eriophyid Mites: An ecological study of Phyllocoptes fructiphilus Keifer (Acari: Eriophyidea), vector of Rose rosette virus, and its relationship with Rosa species. Master's thesis, Knoxville, TN; University of Tennessee.
Google Scholar
Thomas, B. (1982) The effect of prunus necrotic ringspot virus on field-grown roses. Annals of Applied Biology, 100, 129–134.
10.1111/j.1744-7348.1982.tb07199.x
Web of Science®Google Scholar
Thomas, E. and Scott, C. (1953) Rosette of rose. Phytopathology, 43, 218–219.
Web of Science®Google Scholar
Tubbs, F.R. (1973) Research fields in the interaction of rootstocks and scions in woody perennials. Parts 1 and 2. Horticultural Abstracts, 43, 247–253; 325–335.
Google Scholar
Tuffen, M. (2016) Rapid Pest Risk Analysis (PRA) for: Rose rosette virus and its vector Phyllocoptes fructiphilus. London: Department for Environment, Food and Rural Affairs (DEFRA).
Google Scholar
United States Department of Agriculture. (2015) 2012 Census of Agriculture: Census of Horticultural Specialties. Washington: United States Department of Agriculture.
Google Scholar
Vazquez-Iglesias, I., Adams, I.P., Hodgetts, J., Fowkes, A., Forde, S., Ward, R. et al. (2019) High throughput sequencing and RT-qPCR assay reveal the presence of rose cryptic virus-1 in the United Kingdom. Journal of Plant Pathology, 101, 1171–1175.
10.1007/s42161-019-00307-5
Web of Science®Google Scholar
Yasin, N., Ahmed, S., Khan, W. and Ashraf, Y. (2016) Survey and pathogenicity of black spot disease of rose in Pakistan. Journal of Horticulture, 3, 189–196.
Google Scholar

Citing Literature

Volume69, Issue9

December 2020

Pages 1603-1617

This article also appears in:

Plant Pathogen Impact Reviews

Facing Rose rosette virus: A risk to European rose cultivation

Abstract

1 INTRODUCTION

Note

2 PEST AND PATHOGENS AFFECTING ROSES IN EUROPE

3 ROSE VIRUSES REPORTED IN EUROPE

4 ROSE ROSETTE VIRUS