Next Article in Journal
Genetic Identity and Diversity of Apple Accessions within a Candidate Collection for the Norwegian National Clonal Germplasm Repository
Next Article in Special Issue
The Apple Lipoxygenase MdLOX3 Regulates Salt Tolerance and ABA Sensitivity
Previous Article in Journal
Fusarium Dry Rot of Garlic Bulbs Caused by Fusarium proliferatum: A Review
Previous Article in Special Issue
Exogenous Melatonin Improves Cold Tolerance of Strawberry (Fragaria × ananassa Duch.) through Modulation of DREB/CBF-COR Pathway and Antioxidant Defense System
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 8
Issue 7
10.3390/horticulturae8070629
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Viral Infection Control in the Essential Oil-Bearing Rose Nursery: Collection Maintenance and Monitoring

by
Sevilia Seitadzhieva
1,*,
Alexander A. Gulevich
2,*,
Natalya Yegorova
1,
Natalya Nevkrytaya
1,
Suleiman Abdurashytov
1,
Lyudmila Radchenko
1,
Vladimir Pashtetskiy
1 and
Ekaterina N. Baranova
2,3
1
Research Institute of Agriculture of Crimea, Kievskaya St., 150, 295453 Simferopol, Russia
2
All-Russia Research Institute of Agricultural Biotechnology, Timiryazevskaya St., 42, 127550 Moscow, Russia
3
N.V. Tsitsin Main Botanical Garden of Russian Academy of Sciences, Botanicheskaya St., 4, 127276 Moscow, Russia
*
Authors to whom correspondence should be addressed.
Horticulturae 2022, 8(7), 629; https://doi.org/10.3390/horticulturae8070629
Submission received: 28 June 2022 / Revised: 7 July 2022 / Accepted: 9 July 2022 / Published: 12 July 2022
(This article belongs to the Special Issue Horticultural Crop Physiology under Biotic and Abiotic Stresses)
Browse Figures
Review Reports Versions Notes

Abstract

:
Viral diseases affecting the essential oil rose, which is a valuable object of agricultural production, may have a significant negative impact on the economic value of this crop. Hence, the study and control of potentially dangerous viruses is essential to improving the quality of cultivars of this raw plant material, to enable production of valuable derivatives. The diversity of viruses affecting Rosa L. plants manifests itself in their conditional division into those that are specific to this crop, and those that are hosted by other plants. Representatives of both groups are found in different countries, however, a low number of viruses identified have been thoroughly studied through the use of experimental methods. In particular, with regard to many viruses, the issue of their spread remains open. The viruses infecting Rosa L. plants along with other crops are described in the literature in detail, as the range of hosts they affect is rather wide and well-studied. It is also possible to single out the three most significant viruses affecting this host—Prunus necrotic ringspot virus, Apple mosaic virus and Arabis mosaic virus which individually, or collectively, cause viral diseases that manifest themselves in mosaic symptoms. The most likely mechanisms for the spread of the Rosa L. species viruses are vegetative propagation procedures and transmission by various pests. These presumptions underlie viral infection control methods, including a well-thought-out planting scheme and provision of accurate plant care, which considers plant disinfection, disease monitoring associated with diagnostics and obtaining virus-free material through biotechnology techniques.

1. Introduction

Essential oil roses belong to the family Rosaceae, genus Rosa. The essential oil rose plant is an important agricultural crop due to its high economic value. Essential oil is obtained mainly from four types of roses: R. damascena Mill., R. alba L., R. gallica L. and R. centifolia L. The highest quality oil is extracted from the Bulgarian rose R. kazanlika (Rosa damascena Mill. f. trigintipetala Dieck) which is a form of Rosa damascena Mill. [1,2].
The rose petals account for the main content of essential oil in the essential oil rose plant (about 93% of the total content in the flower). The rose flower derivatives include rose water (hydrolate), absolute oil (absolute), concrete and extract used in the perfume and toiletry industry and medicine [3,4]. The origin of the essential oil rose is associated with Iran and Syria [5,6]. Currently, the centres of cultivation of this crop are Bulgaria [7] and Turkey [8], it is also grown commercially in Saudi Arabia [9], Egypt [10], India [11], Russia [12], Georgia, China, Algeria, Spain, France, Italy and Morocco [2,13].
The essential oil rose derivatives of domestic production can claim competitiveness vis-à-vis the global reference producers, provided that the international standards of processing practice are observed. Hence, the need arises for breeding new high-performance cultivars [14,15]. This is the challenge facing the Research Institute of Agriculture of Crimea, the owner of a unique gene pool collection of essential-oil, spicy, aromatic and medicinal plants [16]. The collection specimens are a source material for the studies carried out by the Essential-Oil and Medicinal Crops Selection Division. The Institute is the owner and originator of five essential oil rose cultivars included in the State Register of Selection Achievements Authorized for Use of the Russian Federation [17].
Apart from the agro-technical crop care measures, essential-oil rose cultivation involves pest and pathogen control [18,19]. The rose-specific viral diseases are widely spread in the countries where this crop is grown. They impair the rose habit, its decorative and economic value, affect the vegetative and generative parts of plants and blunt the plant health and viability, even to the point of its death [20,21]. Detection of viral diseases, developing means and techniques for their prevention and control, as well as cultivation of new cultivars most resistant to infections are the important challenges facing the plant material growing process.
This article reviews the studies focused on the viral diseases of plants falling under genus Rosa L., including essential oil roses.

2. Overview of the Rosa L. Species Viruses

Studies focused on the essential oil rose-specific viruses are rare in the literature while the information available addresses the viral pathologies specific to Rosa L. plants only in general. The basic reference source to be relied upon in this context is the European and Mediterranean Plant Protection Organization Global Database [22]. The documents of this organization provide the certification scheme for Rosa L. species and hybrids tested for pathogens [23]. A detailed list of the Rosa L.-specific viruses is given in the works by various authors. The data from these sources is presented in Table 1.
It should be noted that Tobacco ringspot nepovirus and Tomato ringspot nepovirus presented in Table 1 are included in the Uniform List of Quarantine Objects of the Eurasian Economic Union [28].
As seen from Table 1 a fairly large number of viruses infecting Rosa L. species are known; they may be divided into only the viruses hosted by Rosa L. plants and those whose host plants are represented by other crops. Table 2 presents the viruses hosted by Rosa L. plants.
The data presented in Table 2 suggests that the spread mechanism for many Rosa L.-specific viruses is not known while the symptoms of the plant viral diseases are common in certain cases.
Table 3 presents the viruses for which Rosa L. is one of the host plants.
More information is available on the transmission routes of the viruses that are not specific to Rosa L. plants, since these phytopathogens have been studied in more detail in other crops. Nevertheless, the data presented in Table 2 and Table 3 suggests that, in general, the viral infections affecting rose plants are superficialized, which is confirmed by the scarcity of data on symptomatic manifestations and transmission routes of these phytopathogens. The economic cost caused by viruses is assessed by the effect they produce on the normal growth and vital activity of plants. The effect produced by the virus on plants is studied based on the disease manifestations. In general, viruses are characterized as causing a systemic disease in plants, when a phytopathogen moves from the primary point of the infection entry to other parts of the plant (Figure 1).
Localized infection with viral diseases manifests itself as discoloration of the lamina. This type of symptom is not so significant for essential oil roses, but is important for the diagnostic detection of viruses. Examples of such symptoms include chlorosis (chlorophyll decay or deficiency), increased chlorophyll concentration in some areas of old leaves, necrotic lesions, ringspots. Systemic symptoms include stunted growth; mosaic (alternating light- and dark-green areas); yellowing (complete leaves yellowing); ringspots in leaves and fruits caused by the tissues yellowing or the surface cells destruction; necrotization of large groups of cells, organs or even the whole plant; malformation (distortion of various organs, overgrowth, tumours) [59,60].
For all the diversity of viral symptoms, many of them are similar to those caused by other pathogens which makes diagnosis difficult (Figure 2).
Based on the articles by various authors, it may be concluded that the most typical and common manifestation of the viral diseases affecting Rosa L. plants is viral mosaic caused by such pathogens as Prunus necrotic ringspot virus, Apple mosaic virus and Arabis mosaic virus [8,39,41,61,62,63,64,65]. Its hallmark is that the infection has a mono- or mixed nature, that is, it is triggered by a single virus or a group of viruses. Moreover, manifestations of one or several viruses may be different: chlorotic lines; ringspots; vein clearing and banding; leaf mottling during vegetation; yellow netting and yellow mosaic; oak leaf pattern; leaf distortion and curling; necrosis; flower distortion; flower size reduction; shrinkage in the plant stem at the grafting point [24,26,63,64].
Signs of a viral infection may also vary wildly, being subject to the air temperature and the time of year. They often manifest themselves in spring and early summer. For example, bands along the leaf veins may come up during lengthy hot periods. At times only a certain part of the plant may have lesions while in some cases infected parts of the plant manifest no symptoms. The disease results in reduced flowering, impaired winter survival, premature leaf fall and increased vulnerability to low temperatures. At the same time some infected plants do not manifest any symptoms at all [26,64].
Descriptions of the viruses causing mosaic in rose plants are presented in Table 4; details of their genetic structure are given in Appendix A.

3. Spread of Rosa L. Plants’ Viruses

Control of rose plant-affecting viral diseases involves, in the first instance, the study of the pathogen transmission routes. However, as mentioned above, there is only a conjectural concept of transmission mechanisms of viruses affecting Rosa L. plants as experimental studies focused on these issues are very few. For example, ArMV is spread by the nematode Xiphinema diversicaudatum Micol. but this data is related to the crops which are the main virus host plants, while no data on Rosa L. plant infection have been reported [76,77,78,79]. ApMV is presumably transmitted via grafting, including root grafting, and infected sap when pruning [74]. PNRSV can be transmitted via cuttings from an injured plant during vegetative propagation [62].
Moury et al. [25] reported that the progression of PNRSV-caused infections in greenhouse grown roses is very slow or non-existent since in this study only 1% of the plants manifested symptoms two years after they were planted (in the absence of special precautions such as the plant isolation or disinfection of the tools used for pruning). Therefore, it can be concluded that the main source of the roses’ infection with this virus is grafting in which one of the participants is infected. Furthermore, the difficulty in studying the viral mosaic may be ascribed to its duration and latent progression [25].
The study by Golino et al. [61] considered Rosa L.-affecting viruses transmission routes experimentally. As a result, the following hypotheses were set forth. The virus transmission via the rose seeds from an infected mother plant to sprouts does not occur or is a rare thing; infected pollen is ineffective in spreading viruses to recipient plants; virus transmission via cutting tools is unlikely. Wherein, a significant field spread of two rose mosaic viruses, PNRSV and ApMV, between infected and healthy roses growing close together was observed in experimental fields. This may be due to the fact that root grafting where the roots of the plants growing close together grow and fuse forming vascular links between the plants could be a mechanism for viral transmission.
Sertkaya [63] suggests that the rose mosaic virus could be transferred to these plants initially from an infected stone fruit crop via grafting, and then spread from one rose cultivar to another via infected rootstocks.
The data obtained from the studies carried out by the Research Institute of Agriculture of Crimea showed that various pests affect the essential oil rose. Among these, the green rose aphid (Macrosiphum rosea L.) and rose leaf cicada (Edwardsiana rosae L.) may be suspected vectors of viruses [80]. Since rose propagation is carried out by cutting, the virus transmission from parent plants and via instruments is likely [4,81,82].
Whereas there are a few works confirmed by experimental studies, the data presented in Table 2 and Table 3 suggests a significant contribution on the part of various pests in the spread of viruses affecting Rosa L. species (Figure 3).
The pests described for Rosa L. plant as confirmed and potential vectors of viruses are listed in Table 5.

4. Rosa L. Plants Viruses Control

The rose plant vulnerability to various diseases is due to its vegetative propagation (grafting, bud-grafting, cutting grafting, clonal micropropagation), whereby the infection is transmitted from a mother plant to a vegetative progeny [93,94] (Figure 4). When selecting cuttings for vegetative propagation or grafting, lignified young shoots from rose bushes not affected by pests and diseases are used. For propagation by cutting or in vitro clonal micropropagation, healthy plants that do not show the following damages are selected (Figure 4): changes in shape; shoot or flower deformations; changes in the leaf colour; no manifestations of marginal necrosis, spotting, chlorosis and mosaic which are specific to viral infections (Figure 2A), and raise doubts about the sources of damage (Figure 2B).
Due to the impossibility of visual identification of a viral infection, the following indirect precautions are taken to prevent viral diseases: work clothing and tool disinfection; plant residue destruction; disposal of the plants that may be a source of viruses (weed plants and cultivated plants showing signs of infection); control of insects and/or mites and/or nematodes as potential viral vectors; compliance with the spatial isolation regulations (in cases where several species of host plants are located in one area); use of virus-free planting material; observance of quarantine regulations in case of product expansion; obtaining virus-free planting material from reliable sources and/or its preliminary verification [59].
According to da Silva et al. [64], it is possible to remove the plant parts showing specific symptoms. However, this will not interfere with further progression of pathology since the plant is infected systemically and the signs of infection may manifest themselves on other organs or parts of the plant over time. Perennial plants showing clear signs of infection should be removed completely. However, in case of their spatial isolation from virus-free plants, cultivation does not pose a significant risk. If this is the case, it is important to disinfect the tools used for pruning or bud-grafting even in the absence of clear signs of infectious plant sap activity. It is also advisable to practice mixed planting where roses are planted next to other plants which are attractive to insect vectors in this way reducing the likelihood of infection spread [95].

4.1. Traditional Methods of Viruses Control

Measures to propagate essential oil roses implemented for example, by the Research Institute of Agriculture of Crimea include, among others, systemic precautions to prevent the spread of pests and diseases. The essential oil roses cultivation technology includes providing optimal conditions for their growth; implementing care measures at the right time; weed, insect and pest control, as well as the observance of quarantine regulations and preventive treatment of plants relocated from different sites of the nursery. In the selected area, the predecessor culture is harvested, and the stubble is broken as deep as 8–10 cm. Upon the emergence of weeds above ground repeated stubble breaking is carried out with the application of an herbicide (glyphosate), at a dose of 4–6 mL/ha−1. In October, fertilizers such as ammophos at a dose of 200–400 kg/ha−1 are applied, and if possible, organic fertilizers are used; finally, trench ploughing as deep as 40 cm is carried out. From March onwards, the field surface autumn fallow is to be maintained and the soil surface is to be cleared of weed seeds and vegetative rudiments; the area is cultivated three to five times. Prior to planting essential oil rose seedlings, the soil is harrowed as deep as 18 cm. Roses are planted in October-November (as well as during frost-free periods in winter) according to the scheme 3.0 × 0.85 m with a density of 4000 plants/ha−1. For planting, selected conditioned plantlets previously dipped in a mash of clay and cow manure are used. The care for non-bearing plants (during the next year after planting) focuses, mainly, on intensive weed, disease and pest control. As weeds germinate, mechanical inter-row tillage is carried out as deep as 10–16 cm for 3–5 times. If weeds are dense inter-row weed pulling is carried out. In October–November, seedlings are underplanted manually, in the required quantity. In the second year after planting, in February–March, bushes are pruned along with the culling of bushes manifesting signs of infection and deformation and collecting samples for the diagnostic laboratory. Since the essential oil rose is used both for obtaining oil and producing jam, syrups and soaps, the care for plants during the harvesting period is limited to weeding, fertilizing and watering, without the use of chemical crop protection products that may affect the quality of the essential oil rose derivatives. The crop protection interventions involving the use of herbicides, fungicides or insecto-acaricides can be carried out only a month before or after the harvesting. Therefore, the identification of phytopathological damage and phytosanitary control, during the flowering period (from late May to early July) is limited to detecting and culling infected plants, along with intensive weeding. The strongest six or seven shoots are left on the plant, two of them located in the centre of the bush are cut 30–35 cm high from the soil surface, and the rest are cut 20–25 cm high from the soil surface. All the damaged and weak shoots are cut at the level of the soil surface. Plants manifesting obvious viral damage are discarded and burned. Agronomists inspect the plots on a weekly basis under the routine procedure for plant care, pruning and weeding. When finding suspicious spots and deformations, the location of the infected plant is noted; the disease manifestations in bushes are photographed and sent to the laboratory. The rose bushes manifesting clear signs of obvious disease symptoms are removed from the area to prevent disease spread. However, regular inspection and culling of low-quality material at all stages of plant cultivation does not rule out the presence and accumulation of a viral load. For this reason, planting material renewal is most effective if in vitro collection materials are used where valuable genotypes are preserved and multiplied by clonal micropropagation [4,96].
Figure 5 presents integrated data on traditional measures to control viral infections.

4.2. Biotechnological Methods for Viruses Control

Virus-free planting material is produced through the use of biotechnological techniques: apical meristem culture methods including the use of thermotherapy or chemotherapy [97].
Apical meristem culture is based on the concept that the meristem is so structured that its upper layers (an apical meristem) give rise to cover tissues while its lower layers give rise to the conduction system. Due to the fact that these layers are compartmentalized the ability of a virus to penetrate the upper layers via the conduction system is limited. Viruses move along the vascular system at a higher speed; however, it is presumed that viral particles can slowly make their way into the upper layers via the plasmodesmata connecting the meristematic cells. Another reason for the absence of viruses in certain parts of the meristem is that cell division and virus multiplication and spread, occur at different rates. This is also the reason for the presence of certain viruses and strains in various parts of the meristem [98]. Clonal in vitro propagation is based on apical meristem culture. It is a cell engineering method whereby, within a short time, valuable cultivars are multiplied and introduced into production and virus-free planting material is produced. This method is also well-known for essential-oil roses [94,99,100].
Thermotherapy is based on inhibiting virus reproduction or preventing the viral particles’ penetration into the re-growing parts of a plant by means of a high temperature, whereby the integrity of cell compartments are not impaired, and the damage to plant cells and tissues is minimized. There are a few variations of this method: (1) Hot water dipping. This method is applied to the resting parts of a plant (tubers, buds, cuttings). These parts are dipped in hot water as they are able to survive higher temperatures than actively vegetating plants. Upon thermotherapy the plant fragments are dried a little in the air, preferably in aseptic conditions. (2) The dry-air process is preferable for vegetating parts of a plant, whereby, they are exposed to warm air at temperatures of 35–40 °C over several weeks. This method does not impair plant health and helps to produce virus-free shoot apexes, subsequently grafted on the rootstock or rooted [98,101].
Chemotherapy can be successful in combination with thermotherapy and apical meristem culture [98]. The best-known antiviral agent is ribavirin that inhibits replication of multiple animal and plant viruses [102]. The studies carried out by Yegorova [103] to look at the effect of virazole (ribavirin) identified features specific to the essential oil rose explants’ morphogenesis in vitro, subject to the agent’s concentrations in the culture medium. The chemotherapy conditions optimization, centres around the empirical identification of the virus-inhibiting agent’s concentration and exposure time, taking into account the explant type and the explant treatment method. It is critical to minimize the negative impact of the agent on the explant. For two months the meristems and apexes isolated from developing shoots were exposed to chemotherapy with virazole at concentrations of 20.0–25.0 mg/L. A decrease in the number of leaves, buds and developing explants, as well as the shoot length, by 1.2–2.7 times compared to the control group was observed. At the same time, on further micropropagation of viable shoots, the development of the plants grown with chemotherapy scarcely differed from the control group. This points to the possibility of using virazole during the stated period, and in the empirically identified concentration, for essential oil rose chemotherapy when carrying out sequential cultivation of the meristems and shoot apexes.
Mitrofanova et al. [98] described a model system for viral elimination in flower crops comprised of the following basic elements: screening the plants for viruses, thermo- or chemotherapy, apical meristem culture, the adapted plants retested for viruses. This model involves the following stages:
  • Mother plant diagnosis using test plants, electron microscopy, ELISA and PCR techniques.
  • In case the plant is infected, thermotherapy in vitro, or in vivo at 37 °C for 4–15 weeks, or chemotherapy with virucides in vitro.
  • Plant tissue culture growth and plant regeneration on artificial nutrient media over 14–20 weeks.
  • Regenerated plants adaptated in vitro at 15–20 °C over 3–4 weeks.
  • The adapted plants retested using the test plants, ELISA and PCR techniques.
  • Obtaining of virus-free plants and their certification.

5. Key Points and Current Prospects for Viral Disease Control in Essential Oil Rose Cultivation

Compliance with the regulations for agricultural machinery maintenance and operation, an ongoing monitoring of damage to plants, and comprehensive diagnostic interventions (including ELISA and PCR-based diagnostics of phenotypically identified manifestations of the diseases affecting a proposed planting material) may help prevent significant damage to plants and inhibit viral infection spreading. However, these interventions are economically feasible and appropriate only in the case of a significant decrease in productivity caused by disorders in the shoots, buds and flower development (apparent only in cases where the plants are affected by ‘viruses causing disorders in the plants’ development). Such manifestations are described for Prunus necrotic ringspot virus [71], Rose leaf curl virus [29], Rose rosette virus [31], Rose leaf rosette-associated virus [44], Impatiens necrotic spot virus [53], Raspberry ringspot virus [55].
Currently, a negative impact of viral diseases on rose essential oil production and its qualitative indicators, remains unevaluated, which testifies to the relevance of such studies [8]. Viral infection monitoring remains an expensive and not readily available or affordable intervention. On the other hand, a moderate ignorance of such damage can be considered, as the adverse effects of a number of viral diseases such as losses in the essential oil quantity and quality may be less significant compared to the implementation of a full range of antiviral interventions involving the use of expensive assessment and monitoring methods, with participation of external experts. Interventions for essential oil rose viral infection control may include up-to-date genetic engineering methods, such as CRISPR-Cas technology. This will enable in the longer term, a total block of one of the phases of viral assembly or replication, by inhibiting the activity of the cell systems used by the virus for replication, transport or other key mechanisms of the infection process [104,105]. It is seen as feasible for essential oil roses as clonal crops. For example, antisense technology, RNA interference-based technology or modulation of the activity of cell processes, particularly, the processes causing dissociation of the coat protein from the viral nucleic acid could be used [106,107].

6. Conclusions

Care for essential oil roses as valuable agricultural crops requires the availability of sophisticated schemes for preventing and managing various diseases, including viral infections. Research activities carried out by the Research Institute of Agriculture of Crimea, as the owner of a unique collection of essential oil crops, focus on implementing an effective system for protecting these valuable plants against pathogens. The literature provides scarce evidence of the viral diseases specific to essential oil roses, however, the affiliation to genus Rosa L. suggests typical manifestations of viral diseases in representatives of this taxon. There are Rosa L. viruses specific to this crop and typical of other plant species. They cause both localized damage (leaf discoloration) and systemic changes (impaired plant health). The best-known manifestation of the Rosa L. plants’ viral diseases is the rose viral mosaic caused by three pathogens (PNRSV, ApMV and ArMV) which may be present in plants individually or collectively. Living organisms contribute significantly to the viral infections’ spread. Aphids, nematodes, mites and thrips are the experimentally proven and suspected vectors of viral infections in Rosa L. species. However, their role in certain cases is superficialized, which leaves open the issue of many known viruses’ transmission. The essential oil rose viral infections control is complicated by the lack of a general technique for eradication of the viruses. Therefore, indirect methods based on the disinfection and disposal of the materials potentially infected with viruses, and production of virus-free plant material as well as standard and up-to-date techniques emerging from molecular biology and biotechnology are used. Unfortunately, an important limitation in plant viral disease control is the high costs for virus detection and inactivation with the use of up-to-date methods, which are more accurate and effective as compared to the classic approaches. Therefore, development of both efficient and economically feasible techniques for essential oil rose viral disease control is the goal of scientific research carried out in this area.

Author Contributions

Conceptualization, S.S., E.N.B., N.N., N.Y. and S.A.; methodology, E.N.B., N.N. and N.Y.; software, S.S.; validation, E.N.B., A.A.G. and L.R.; research, S.S., E.N.B. and S.A.; resources, S.S. and E.N.B.; data curation, E.N.B. and A.A.G.; writing—original draft preparation, S.S. and A.A.G.; writing—review and editing, S.S., E.N.B., A.A.G., N.N. and S.A.; visualization, S.S.; supervision, S.S. and E.N.B.; project administration, V.P. and L.R.; funding acquisition, V.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was carried out with the support of the Ministry of Education and Science of the Russian Federation under scientific projects No FNZW-2022-0006 (Research Institute of Agriculture of Crimea); 0431-2022-0003 (All-Russia Research Institute of Agricultural Biotechnology) and 122011400178-7 (Tsitsin Main Botanical Garden of Russian Academy of Sciences).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A. Genetic Structure of the Mosaic Viruses

Appendix A.1. Prunus Necrotic Ringspot Virus

The functional singularity of this virus is due to the features specific to RNAs making up its whole genome, particularly, the smallest RNA-3. PNRSV like all other representatives of the family Bromoviridae has a genome comprised of three segments of positive-sense single-stranded RNA: RNA-1, RNA-2 and RNA-3. RNA-1 and RNA-2 are monocistronic and encode the non-structural proteins involved in viral RNA synthesis. RNA-3 is bicistronic and encodes the movement protein and the coat protein where the movement protein is translated directly from RNA-3 while the coat protein is translated from sub genomic mRNA-4) [25,69,70,108,109]. The features of the PNRSV genomic RNAs are presented in Table A1.
Table
Table A1. Characteristics of the genomic RNAs of Prunus necrotic ringspot virus.
Table A1. Characteristics of the genomic RNAs of Prunus necrotic ringspot virus.
RNA TypeRNA Chain Length
(Number of Nucleotides) 		Encoded Protein
RNA-13332Replicase P1 protein
Methyltransferase/helicase)
RNA-22594Replicase P2 protein
RNA-dependent RNA polymerase
RNA-31951Movement protein P3a and the coat protein
The methyltransferase/helicase domain is conserved and contains several sequence motifs which are retained in the ilarviruses and are essential to the P1 protein functionality. The RNA-dependent RNA polymerase domain, for its part, contains eight conserved motifs essential to the positive-sense RNA-viruses’ replication [73].
The study of the PNRSV genome was initially based on the common features of the representatives of genus Ilarvirus which lies in the fact that the coat protein (hereinafter referred to as CP) is the initiator of the viral genome replication in host plants. If this is indeed the case, a specific interaction of the N-terminal part of CP with the 3′-terminal sequences of the viral RNA-3 occurs.
It was assumed that the hairpins flanked by the AUGC sequences near the 3′-termini of the genomic RNAs, were responsible for the specific binding with CP. The experimentally induced mutations in the AUGC-box impaired the RNA ability to bind with CP [110,111]. The functional area for the genome activation in the CP structure is the zinc-finger domains comprised of a complex of four amino acids (two histidines and two cysteines) and zinc ions [112].
Based on this data, Guo et al. [108] identified the complete nucleotide sequence of PNRSV RNA-3. It was established that it consists of 1943 nucleotides and has two large open reading frames (hereinafter referred to as ORF). The 5′-proximal ORFa begins with the 174th nucleotide and ends with the 1023–1025th nucleotides, while the 3′-proximal ORFb begins with the 1100th nucleotide and ends with the 1772–1774th nucleotide. The 5′-proximal ORF3a encodes the movement protein P3a; the 3′-proximal ORF3b encodes CP.
The 3′-noncoding region of 169 nucleotides, called the 3′-NCR, was studied also. Its terminal sequence consisting of 18–23 nucleotides is common for the representatives of genus Ilarvirus. Presumably, this particular region is able to form the hairpins flanked by the AUGC-boxes which constitute the binding sites with a high affinity for CP. Based on the data obtained, the authors presumed that this particular common structural feature of the 3′-NCR RNAs of the genus Ilarvirus representatives, may be responsible for the specific interaction with the coat protein resulting in the genome activation.
When investigating the CP gene structure, it was discovered that its N-termini includes motifs of the above-mentioned zinc-finger domains involved in binding the genomic RNA when the genome replication is encapsidated and activated.
The study of the coat protein is essential to virology research. The diversity of plant viruses is due to their genetic variability that exists behind the virus isolates. The viruses’ diversification analysis is very important for developing techniques for viral pathologies management and control. In this respect the virus coat protein gene due to its singularity and multi-functionality is one of the most common molecular markers for investigating the genetic diversity and molecular evolution of plant viruses [113].
In 1997 Sánchez-Navarro and Pallás [114] carried out a comparative phylogenetic analysis of the coat protein sequences in all the representatives of the family Bromoviridae. Their findings showed a very close affinity between CP PNRSV and the ilarviruses ApMV and TSV. It was also noted that PNRSV and ApMV are closely related, both with regard to the amino acid sequence of their coat proteins, especially taking into account that both viruses have a very similar spectrum of natural hosts (fruit trees from the genus Prunus).

Appendix A.2. Apple Mosaic Virus

The ApMV genome structure is similar to that of other ilarviruses and is presented in Table A2.
Table
Table A2. Characteristics of the genomic RNAs of Apple mosaic virus.
Table A2. Characteristics of the genomic RNAs of Apple mosaic virus.
RNA TypeRNA Chain Length
(Number of Nucleotides)		Encoded Protein
RNA-13476Methyltransferase/helicase)
RNA-22979RNA-dependent RNA polymerase
RNA-32056Movement protein and the coat protein
In 1994 Sánchez-Navarro and Pallás [115] identified the complete nucleotide sequence of the ApMV subgenomic RNA-4 with a view to investigating the genetic affinity of ApMV with other representatives of genus Ilarvirus. This sequence comprises 891 nucleotides and one ORF beginning with the 43–45th nucleotide and ending with the 721–723rd nucleotide. The ORF encodes the coat protein, having in its structure a motif rich in cysteine and histidine and forming a zinc finger tetrahedral zinc complex. The N-terminal domain of the coat protein is cationic while the C-terminal domain is negatively charged. The N-terminal domain binds with the 3′-terminal region of RNA, while the C-terminal acid domain may interact with the replicase complex and enable its contact with the genomic RNA.
3′-regions of RNA-4 comprise several hairpin structures flanked by the AUGC sequence. The CP binding with this region initiates a cycle of replication. Thus, the RNA-4 secondary structure confirms the assumption that “the genome activation” process is a common mechanism for ilarviruses.
In 1995 Shiel et al. [116] identified the complete nucleotide sequence of ApMV RNA-3. It is 2056 bases long and comprises two ORFs. One ORF encodes the movement protein. The other encodes CP and is transcribed into sub genomic RNA-4. The 5′-noncoding region of RNA-3 comprises a 15-base sequence, suggestive of the internal control region of the eukaryotic tRNA gene promoters.
The 3′-termini of all the ilarviruses end with the AUGC sequence essential to the coat protein recognition [110,111]. In contrast, ApMV RNA-3 ends with the AGGC tetranucleotide instead of the AUGC sequence. Nevertheless, the AGGC tetranucleotide is also present in the line of 18 bases above the 3′-terminal.
In 2000 Shiel and Berger [117], in a continuation of their work, described ApMV RNA-1 and RNA-2. RNA-1 comprises 3476 nucleotides and encodes one large polypeptide comparable to the methyltransferase-like and helicase-like domains present in many plant RNA-viruses. ApMV RNA-2 is made up of 2979 bases and encodes the RNA-dependent RNA polymerase.

Appendix A.3. Arabis Mosaic Virus

Arabis mosaic virus includes a positive-sense genome composed of two RNAs the translation of which results in two polyproteins performing the function of predecessors. Both the RNAs are polyadenylated at the 3′-terminal and have a covalently attached viral protein VPg at the 5′-terminal. RNA-1 encodes a protease which breaks down polyproteins into functionally active units. The end products of the RNA-1 activity include 1A, 1B, 1CVPg (VPg), 1Dpro (proteinase) and 1Epol (polymerase). The RNA-2 activity results in the end products as follows: 2A (involved in RNA-2 replication), 2BMP (the movement protein) and 2CCP (the coat protein) [79,118].
Gao et al. [113] stated that polyprotein P1 encoded by RNA-1 breaks down into six proteins identified as X1 (functions are unknown), X2 (a putative protease cofactor), NTB (nucleotide triphosphate-binding protein), VPg, Pro (3C-like proteinase) and Pol (RNA-dependent RNA polymerase). Polyprotein P2 encoded by RNA-2 is broken down by RNA-1-encoded protease into three functional fragments: the homing protein (2A), the movement protein (MP) and the coat protein (CP).
Although ArMV is regarded as one of the viruses causing rose mosaic, the literary sources lack the data concerned with experimental study of the ArMV isolated specifically in rose plants, as was previously the case with PNRSV and ApMV. This is due to the fact that this virus is associated with grape viral diseases [76].
In 2001 Wetzel et al. [118] cloned and sequenced RNA-2 of ArMV-NW isolates affecting grapevine. It was established that the complete sequence of ArMV-NW RNA-2 comprises 3820 nucleotides except for the poly(A) tail. The analysis of the putative open reading frames (ORF) showed the availability of one large ORF (from 296 to 3626 nucleotides). The study of amino acid sequences identified the availability of putative Cys/Ala and Arg/Gly proteolytic cleavage sites for the ArMV-NW polyprotein.
Moreover, in the 5′-noncoding regions there were conserved repeats capable of forming hairpins present in RNA-2 from other isolates identified. Similar structures were found in the 5′-noncoding regions of other nepoviruses, however, their role is not yet clear. The study of RNA-2-encoded polyprotein showed the availability of three domains corresponding to the RNA activity products: N-terminal, central and C-terminal.
In 2003 Wetzel [79] presented the structure of RNA-1 of ArMV-NW isolates. The complete nucleotide sequence of RNA-1 comprises 7334 nucleotides except for the poly(A) tail. There is one ORF composed of 228-7079 nucleotides. Conserved sequences comparable to the stem-loop structures identified in the 5′-noncoding regions of RNA-2 [118] were found as well in the 5′-noncoding regions of RNA-1. The analysis of RNA-1-encoded polyprotein, identified motifs of the viral protease cofactor domain, NTP-binding domain, viral protease domain and RNA-dependent RNA polymerase domain.

References

  1. Dobreva, A.; Kovatcheva, N.; Astatkie, T.; Zheljazkov, V.D. Improvement of essential oil yield of oil-bearing (Rosa damascena Mill.) due to surfactant and maceration. Ind. Crops Prod. 2011, 34, 1649–1651. [Google Scholar] [CrossRef]
  2. Petkova, M.; Tahsin, N.; Yancheva, S.; Yancheva, H. Development of the production of aromatic oil crops in Bulgaria. In China-Bulgaria Rural Revitalization Development Cooperation Forum; Institute of Agricultural Economics: Sofia, Bulgaria, 2018; pp. 71–86. [Google Scholar]
  3. Nenov, N.; Atanasova, T.; Gochev, V.; Merdzhanov, P.; Girova, T.; Djurkov, T.; Stoyanova, A. New product from Bulgarian rose. World Sci. 2016, 1, 17–22. [Google Scholar]
  4. Pashtetskiy, V.S.; Nevkrytaya, N.V.; Mishnev, A.V.; Nazarenko, L.G. Essential Oil Sector: Yesterday, Today, Tomorrow, 2nd ed.; IT “Arial”: Simferopol, Russia, 2018; 320p. [Google Scholar]
  5. Kiani, M.; Zamani, Z.; Khalighi, A.; Fatahi, R.; Byrne, D.H. Microsatellite analysis of Iranian Damask rose (Rosa damascena Mill.) germplasm. Plant Breed. 2010, 129, 551–557. [Google Scholar] [CrossRef]
  6. Redwan, T.; Nassour, M.; Mahfoud, H. Genetic Diversity of Rosa damascena Mill. in Latakia Province as Reveled by ISSR Analysis. SSRG—IJAES 2018, 5, 18–22. [Google Scholar] [CrossRef]
  7. Rusanov, K.; Kovacheva, N.; Rusanova, M.; Atanassov, I. Flower phenotype variation, essential oil variation and genetic diversity among Rosa alba L. accessions used for rose oil production in Bulgaria. Sci. Hortic. 2013, 161, 76–80. [Google Scholar] [CrossRef]
  8. Yardimci, N.; Çulal, H. Occurrence and incidence of Prunus necrotic ringspot virus, Arabis mosaic virus, and Apple mosaic virus on oil rose (Rosa damascena) in the Lakes region of Turkey. N. Z. J. Crop Hortic. Sci. 2009, 37, 95–98. [Google Scholar] [CrossRef] [Green Version]
  9. Ahmed, S.M.; Darwish, H.Y.; Alamer, K.H. Microsatellite, inter simple sequence repeat and biochemical analyses of Rosa genotypes from Saudi Arabia. Afr. J. Biotechnol. 2017, 16, 552–557. [Google Scholar]
  10. Alotaibi, S.S.; Hassan, M.M.; Gaber, A.; Aljuaid, B.S. Genetic relationship and diversity of Taif-roses plant by using three different types of molecular markers. Res. J. Biotech. 2019, 14, 130–138. [Google Scholar]
  11. Gaurav, A.K.; Raju, D.V.S.; Ramkumar, M.K.; Singh, M.K.; Singh, B.; Krishnan, S.G.; Panwar, S.; Sevanthi, A.M. Genetic diversity analysis of wild and cultivated Rosa species of India using microsatellite markers and their comparison with morphology based diversity. J. Plant Biochem. Biotechnol. 2022, 31, 61–70. [Google Scholar] [CrossRef]
  12. Zolotilov, V.; Nevkrytaya, N.; Zolotilova, O.; Seitadzhieva, S.; Myagkikh, E.; Pashtetskiy, V.; Karpukhin, M. The Essential-Oil-Bearing Rose Collection Variability Study in Terms of Biochemical Parameters. Agronomy 2022, 12, 529. [Google Scholar] [CrossRef]
  13. Slavov, A.; Vasileva, I.; Stefanov, L.; Stoyanova, A. Valorization of wastes from the rose oil industry. Rev. Environ. Sci. Bio/Technol. 2017, 16, 309–325. [Google Scholar] [CrossRef]
  14. Nazarenko, L.G.; Korshunov, V.A.; Kochetkov, E.S. Essential Oil Rose Growing and Breeding; Tavriya: Simferopol, Ukraine, 2006; 216p. [Google Scholar]
  15. Zolotilov, V.A.; Nevkrytaya, N.V.; Zolotilova, O.M.; Skipor, O.B. The results of the essential oil rose selection for a high yield of concrete. Taurida Her. Agrar. Sci. 2020, 3, 93–104. [Google Scholar] [CrossRef]
  16. Collection of Essential-Oil, Spicy, Aromatic and Medicinal Plants. Available online: https://ckp-rf.ru/usu/507515/ (accessed on 22 February 2022).
  17. The State Register of Selection Achievements Authorized for Use (National List); Plant Cultivars (Official Publication); FGBNU “Rosinformagrotekh”: Moscow, Russia, 2021; Volume 1, 719p, Available online: https://gossortrf.ru/ (accessed on 22 February 2022).
  18. Stancheva, I.; Rosnev, B. Ornamental and Forest Crops Diseases; Pensoft: Sofia, Bulgaria, 2005; pp. 150–162. [Google Scholar]
  19. Treyvas, L.Y. Roses, Conifers and Other Ornamental Crops Diseases and Pests; Phyton: Moscow, Russia, 2017; pp. 5–115. [Google Scholar]
  20. Zakubanskiy, A.V.; Chirkov, S.N.; Mitrofanova, O.V.; Mitrofanova, I.V. Viruses of some valuable fruits, essential-oil and ornamental plants (Overview). Bull. State Nikitsk. Bot. Gard. 2016, 121, 7–18. [Google Scholar]
  21. Keldysh, M.A.; Chervyakova, O.N. Viral diseases of roses and their prevention in protected ground conditions. Gavrish 2008, 2, 16–21. [Google Scholar]
  22. EPPO Global Database. Available online: https://gd.eppo.int/ (accessed on 22 February 2022).
  23. Certification scheme for rose. EPPO Bull. 2002, 32, 159–177.
  24. Milleza, E.J.M.; Ward, L.I.; Delmiglio, C.; Tang, J.Z.; Veerakone, S.; Perez-Egusquiza, Z. Survey of viruses infecting Rosa spp. in New Zealand. Australas. Plant Pathol. 2013, 42, 313–320. [Google Scholar] [CrossRef]
  25. Moury, B.; Cardin, L.; Onesto, J.P.P.; Candresse, T.; Poupet, A. Survey of Prunus necrotic ringspot virus in Rose and Its Variability in Rose and Prunus spp. Phytopathology 2001, 91, 84–91. [Google Scholar] [CrossRef] [Green Version]
  26. Pscheidt, J.W.; Rodriguez, T.G. Diseases of Rose. In Handbook of Florists’ Crops Diseases; McGovern, R.J., Elmer, W.H., Eds.; Springer: Cham, Switzerland, 2018; pp. 736–737. [Google Scholar]
  27. Sastry, S.K.; Mandal, B.; Hammond, J.; Scott, S.W.; Briddon, R.W. Encyclopedia of Plant Viruses and Viroids; Springer: New Delhi, India, 2019; pp. 2092–2106. [Google Scholar]
  28. Unified Register of the Eurasian Economic Union Quarantine Pests. Available online: https://docs.cntd.ru/document/456047397 (accessed on 22 February 2022).
  29. Khatri, S.; Nahid, N.; Fauquet, C.M.; Mubin, M.; Nawaz-ul-Rehman, M.S. A betasatellite-dependent begomovirus infects ornamental rose: Characterization of begomovirus infecting rose in Pakistan. Virus Genes 2014, 49, 124–131. [Google Scholar] [CrossRef]
  30. Sahu, A.K.; Marwal, A.; Shahid, M.S.; Nehra, C.; Gaur, R.K. First report of a begomovirus and associated betasatellite in Rosa indica and in India. Australas. Plant Dis. Notes. 2014, 9, 147. [Google Scholar] [CrossRef] [Green Version]
  31. Epstein, A.H.; Hill, J.H. Status of Rose Rosette Disease as a Biological Control for Multiflora Rose. Plant Dis. 1999, 83, 92–101. [Google Scholar] [CrossRef] [Green Version]
  32. Chakraborty, P.; Das, S.; Saha, B.; Karmakar, A.; Saha, D.; Saha, A. Rose rosette virus: An emerging pathogen of garden roses in India. Australas. Plant Pathol. 2017, 46, 223–226. [Google Scholar] [CrossRef]
  33. Solo, K.M.; Collins, S.B.; Shires, M.K.; Ochoa, R.; Bauchan, G.R.; Schneider, L.G.; Henn, A.; Jacobi, J.C.; Williams-Woodward, J.L.; Hajimorad, M.R.; et al. A Survey of Rose rosette virus and Eriophyid Mites Associated with Roses in the Southeastern United States. HortScience 2020, 55, 1288–1294. [Google Scholar] [CrossRef]
  34. Salem, N.; Golino, D.A.; Falk, B.W.; Rowhani, A. Identification and Partial Characterization of a New Luteovirus Associated with Rose Spring Dwarf Disease. Plant Dis. 2008, 92, 508–512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Rivera, P.A.; Engel, E.A. Presence of rose spring dwarf-associated virus in Chile: Partial genome sequence and detection in roses and their colonizing aphids. Virus Genes 2010, 41, 295–297. [Google Scholar] [CrossRef]
  36. Barjadze, S.; Karaca, İ.; Yaşar, B.; Japoshvili, G. The yellow rose aphid Rhodobium porosum: A new pest of Damask rose in Turkey. Phytoparasitica 2011, 39, 59–62. [Google Scholar] [CrossRef]
  37. Xing, F.; Gao, D.; Wang, H.; Zhang, Z.; Habili, N.; Li, S. Molecular characterization of rose spring dwarf-associated virus isolated from China rose (Rosa chinensis Jacq.) in China. Arch. Virol. 2021, 166, 2059–2062. [Google Scholar] [CrossRef]
  38. Karanfil, A. Prevalence and molecular characterization of Turkish isolates of the rose viruses. Crop Prot. 2021, 143, 105565. [Google Scholar] [CrossRef]
  39. Mollov, D.; Lockhart, B. Symptoms, Transmission, and Detection of Four New Rose Viruses. Acta Hortic. 2015, 1064, 303–310. [Google Scholar] [CrossRef]
  40. Karanfil, A.; Randa-Zelyüt, F.; Ertunç, F.; Korkmaz, S. First report of Rose yellow vein virus in Turkey. New Dis. Rep. 2018, 38, 11. [Google Scholar] [CrossRef] [Green Version]
  41. Lockhart, B.; Zlesak, D.; Fetzer, J. Identification and Partial Characterization of Six New Viruses of Cultivated Roses in the USA. Acta Hortic. 2011, 901, 139–148. [Google Scholar] [CrossRef]
  42. Sabanadzovic, S.; Ghanem-Sabanadzovic, N.A. Molecular characterization and detection of a tripartite cryptic virus from rose. J. Plant Pathol. 2008, 90, 87–293. [Google Scholar]
  43. Vazquez-Iglesias, I.; Adams, I.P.; Hodgetts, J.; Fowkes, A.; Forde, S.; Ward, R.; Buxton-Kirk, A.; Kelly, M.; Santin-Azcona, J.; Skelton, A.; et al. High throughput sequencing and RT-qPCR assay reveal the presence of rose cryptic virus-1 in the United Kingdom. J. Plant Pathol. 2019, 101, 1171–1175. [Google Scholar] [CrossRef] [Green Version]
  44. He, Y.; Yang, Z.; Hong, N.; Wang, G.; Ning, G.; Xu, W. Deep sequencing reveals a novel closterovirus associated with wild rose leaf rosette disease. Mol. Plant Pathol. 2015, 16, 449–458. [Google Scholar] [CrossRef] [PubMed]
  45. Soltani, N.; Golino, D.A.; Al Rwahnih, M. First Report of Rose Leaf Rosette-Associated Virus Infecting Rose (Rosa spp.) in California, USA. Plant Dis. 2021, 105, 2740. [Google Scholar] [CrossRef] [PubMed]
  46. Phelan, J.; James, D. Complete genome sequences of a putative new alphapartitivirus detected in Rosa spp. Arch. Virol. 2016, 161, 2623–2626. [Google Scholar] [CrossRef] [PubMed]
  47. Ohata, Y.; Nishio, T.; Tsuda, S. First isolation of rose yellow mosaic virus in Japan. J. Gen. Plant Pathol. 2021, 87, 295–299. [Google Scholar] [CrossRef]
  48. Diaz-Lara, A.; Mollov, D.; Golino, D.; Al Rwahnih, M. Complete genome sequence of rose virus A, the first carlavirus identified in rose. Arch. Virol. 2020, 165, 241–244. [Google Scholar] [CrossRef]
  49. Katsiani, A.T.; Maliogka, V.I.; Candresse, T.; Katis, N.I. Host-range studies, genetic diversity and evolutionary relationships of ACLSV isolates from ornamental, wild and cultivated Rosaceous species. Plant Pathol. 2014, 63, 63–71. [Google Scholar] [CrossRef] [Green Version]
  50. He, Y.; Chen, Y.S.; Wang, Z.H.; Wang, L.P.; Wang, G.P.; Hong, N.; Xu, W.X. First Report of Apple stem grooving virus Infecting Rosa chinensis in China. Plant Dis. 2016, 100, 1252. [Google Scholar] [CrossRef]
  51. Tzanetakis, I.E.; Gergerich, R.C.; Martin, R.R. A new Ilarvirus found in rose. Plant Pathol. 2006, 55, 568. [Google Scholar] [CrossRef]
  52. Awasthi, P.; Dhyani, D.; Ram, R.; Zaidi, A.A.; Hallan, V. Wild roses as natural reservoirs of Cherry necrotic rusty mottle virus. Eur. J. Plant Pathol. 2015, 142, 403–409. [Google Scholar] [CrossRef]
  53. Shahraeen, N.; Ghotbi, T.; Mehraban, A.H. Occurrence of Impatiens necrotic spot virus in Ornamentals in Mahallat and Tehran Provinces in Iran. Plant Dis. 2002, 86, 694. [Google Scholar] [CrossRef]
  54. Rafizadeh, N.; Jafarpour, B.; Falahati Rastegar, M. Detection of Iris yellow spot virus (IYSV) in onion and some of ornamental plants by ELISA and RT-PCR methods in Khorosan Razavi provinces. J. Plant Protect. Res. (Agric. Sci. Technol.) 2013, 27, 149–158. [Google Scholar]
  55. von Bargen, S.; Demiral, R.; Büttner, C. First detection of Raspberry ringspot virus in mosaic diseased hybrid roses in Germany. New Dis. Rep. 2015, 32, 18. [Google Scholar] [CrossRef] [Green Version]
  56. Kulshrestha, S.; Hallan, V.; Raikhy, G.; Ram, R.; Zaidi, A.A. Strawberry latent ringspot virus Infecting Roses in India. Plant Dis. 2004, 88, 86. [Google Scholar] [CrossRef]
  57. Sattary, M.; Rakhshanderoo, F.; Mozafari, J. First report of a mosaic disease caused by Tomato ringspot virus on rose and almond plants in Iran. Plant Pathol. 2015, 97, 393. [Google Scholar]
  58. Moini, A.A.; Izadpanah, K. New hosts for Tomato spotted wilt virus in Tehran. Iran. J. Plant Pathol. 2000, 36, 104–105. [Google Scholar]
  59. Matthews, R.E.F. Plant Virology; Mir: Moscow, Russia, 1973; 686p. [Google Scholar]
  60. Anikina, I.N.; Seitzhanova, L.L. Phytovirusology; Kereku: Pavlodar, Kazakhstan, 2015; pp. 26–27. [Google Scholar]
  61. Golino, D.A.; Sim, S.T.; Cunningham, M.; Rowhani, A. Transmission of Rose Mosaic Viruses. Acta Hortic. 2007, 751, 217–224. [Google Scholar] [CrossRef]
  62. Kiliç, H.Ç.; Yardimci, N.; Gübür, Ş. Serological, biological and molecular detection of Prunus necrotic ringspot virus on Rosa damascena Mill. in Turkey. Acta Sci. Pol. Hortorum Cultus. 2017, 16, 145–150. [Google Scholar]
  63. Sertkaya, G. An nvestigation on Rose Mosaic Disease of Rose in Hatay-Turkey. Julius-Kühn-Archiv 2010, 427, 309–313. [Google Scholar]
  64. da Silva, S.; Babu, B.; Paret, M.L.; Knox, G.; Iriarte, F.; Riddle, B.; Folimonova, S.Y. Rose Mosaic Virus: A Disease Caused by a Virus Complex and Symptoms on Roses and Management Practices. EDIS 2018, 4, 1–5. [Google Scholar] [CrossRef]
  65. Valasevich, N.; Cieślińska, M.; Kolbanova, E. Molecular characterization of Apple mosaic virus isolates from apple and rose. Eur. J. Plant Pathol. 2015, 141, 839–845. [Google Scholar] [CrossRef]
  66. Cui, H.; Hong, N.; Wang, G.; Wang, A. Genomic Segments RNA1 and RNA2 of Prunus necrotic ringspot virus Codetermine Viral Pathogenicity to Adapt to Alternating Natural Prunus Hosts. Mol. Plant-Microbe Interact. 2013, 26, 515–527. [Google Scholar] [CrossRef] [Green Version]
  67. Cui, H.G.; Liu, H.Z.; Chen, J.; Zhou, J.F.; Qu, L.N.; Su, J.M.; Wang, G.P.; Hong, N. Genetic diversity of Prunus necrotic ringspot virus infecting stone fruit trees grown at seven regions in China and differentiation of three phylogroups by multiplex RT-PCR. Crop Prot. 2015, 74, 30–36. [Google Scholar] [CrossRef]
  68. Huo, Y.-Y.; Li, G.-F.; Qiu, Y.-H.; Li, W.-M.; Zhang, Y.-J. Rapid Detection of Prunus necrotic ringspot virus by Reverse Transcription-cross-priming Amplification Coupled with Nucleic Acid Test Strip Cassette. Sci. Rep. 2017, 7, 16175. [Google Scholar] [CrossRef] [Green Version]
  69. Khalid, A.; Adel, R. Prunus necrotic ringspot virus in apricot (Prunus armeniaca) and peach (P. persica) newly reported in Saudi Arabia. New Dis. Rep. 2011, 23, 26. [Google Scholar]
  70. Mekuria, G.; Ramesh, S.A.; Alberts, E.; Bertozzi, T.; Wirthensohn, M.; Collins, G.; Sedgley, M. Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). J. Virol. Methods. 2003, 114, 65–69. [Google Scholar] [CrossRef]
  71. Paduch-Cichal, E.; Sala-Rejczak, K. Biological and molecular characterization of Prunus necrotic ringspot virus isolates from three rose cultivars. Acta Physiol. Plant. 2011, 33, 2349–2354. [Google Scholar] [CrossRef] [Green Version]
  72. Ulubas, C.; Ertunc, F. RT-PCR Detection and Molecular Characterization of Prunus necrotic ringspot virus Isolates Occurring in Turkey. Phytopathology 2004, 152, 498–502. [Google Scholar] [CrossRef]
  73. Xing, F.; Gao, D.; Liu, H.; Wang, H.; Habili, N.; Li, S. Molecular characterization and pathogenicity analysis of prunus necrotic ringspot virus isolates from China rose (Rosa chinensis Jacq.). Arch. Virol. 2020, 165, 2479–2486. [Google Scholar] [CrossRef]
  74. Grimová, L.; Winkowska, L.; Konrady, M.; Ryšánek, P. Apple mosaic virus. Phytopathol. Mediterr. 2016, 55, 1–19. [Google Scholar]
  75. Sánchez-Navarro, J.A.; Aparicio, F.; Herranz, M.C.; Minafra, A.; Myrta, A.; Pallás, V. Simultaneous detection and identification of eight stone fruit viruses by one-step RT-PCR. Eur. J. Plant Pathol. 2005, 111, 77–84. [Google Scholar] [CrossRef]
  76. Meng, B.; Martelli, G.P.; Golino, D.A.; Fuchs, M. Grapevine Viruses: Molecular Biology, Diagnostics and Management; Springer: Cham, Switzerland, 2018; 698p. [Google Scholar]
  77. Grimová, L.; Winkowska, L.; Ryšánek, P.; Svoboda, P.; Petrzik, K. Reflects the coat protein variability of apple mosaic virus host preference? Virus Genes 2013, 7, 119–125. [Google Scholar] [CrossRef] [PubMed]
  78. Martelli, G.P.; Taylor, C.E. Distribution of Viruses and Their Nematode Vectors. In Advances in Disease Vector Research; Harrys, K.F., Ed.; Springer: New York, NY, USA, 1990; pp. 151–189. [Google Scholar]
  79. Wetzel, T.; Beck, A.; Wegener, U.; Krczal, G. Complete nucleotide sequence of the RNA 1 of a grapevine isolate of Arabis mosaic virus. Arch. Virol. 2004, 149, 989–995. [Google Scholar] [PubMed]
  80. Drobotova, E.N. Pests of essential oil crops grown at the Research Institute of Agriculture of Crimea. In Proceedings of the Current State, Problems and Prospects of Agricultural Science Development, Simferopol, Russia, 5–9 October 2020. [Google Scholar]
  81. Zolotilov, V.A.; Nevkrytaya, N.V. Laying and Exploitation of Essential Oil Roses Breed Sheds: Methodological Recommendations; FSBSI “Research Institute of Agriculture of Crimea”: Simferopol, Russia, 2017; 28p. [Google Scholar]
  82. Pashtetskiy, V.S.; Skipor, O.B.; Kravchenko, G.D.; Zolotilova, O.M.; Zolotilov, V.A.; Myagkih, E.F.; Verdysh, M.V.; Popova, A.A.; Polyakova, N.Y.; Kolesnikova, A.V. Technologies of Traditional and Perspective Essential Oil Cultures Breeding in the Republic of Crimea; IT “Arial”: Simferopol, Russia, 2020; 36p. [Google Scholar]
  83. Vazquez-Iglesias, I.; Ochoa-Corona, F.M.; Tang, J.; Robinson, R.; Clover, G.R.; Fox, A.; Boonham, N. Facing Rose rosette virus: A risk to European rose cultivation. Plant Pathol. 2020, 69, 1603–1617. [Google Scholar] [CrossRef]
  84. Özbek, H.; Çalmaşur, O. A Review of Insects and Mites Associated with Roses in Turkey. In Proceedings of the I International Rose Hip Conference 690, Erzurum, Turkey, 7 September 2004. [Google Scholar]
  85. Smitha, R.; Rajendran, P.; Sandhya, P.T.; Aparna, V.S.; Rajees, P.C. Insect pest complex of rose at Regional Agricultural Research Station, Ambalavayal, Wayanad. In Proceedings of the International Symposium on Succulents and Other Ornamentals 1165, Wayanad, India, 24–27 January 2016. [Google Scholar]
  86. Dogadina, M.A.; Stavtseva, T.I.; Botuz, N.I. Pests of roses of the open ground in the conditions of the Orel region. Hortic. Vinic. 2015, 6, 47–52. [Google Scholar]
  87. Sergeeva, O.; Barinov, M.; Medvedeva, K. Study of the twospotted spider mite harmfulness on roses in the Pavlovsk State reserve museum. In Proceedings of the Scientific Contribution of Young Researchers to the Preservation of Traditions and Development of Agroindustrial Complex, Saint Petersburg, Russia, 31 March–1 April 2016. [Google Scholar]
  88. Balykina, E.B.; Klimenko, Z.K.; Zvonareva, L.N.; Plugatar, S.A.; Rybareva, T.S. Pests and diseases of garden roses cultivars from the collection of the Nikitskiy Botanical Garden. Bull. Tver. State Univ. 2017, 4, 92–102. [Google Scholar]
  89. Pizetta, P.U.C.; Pivetta, K.F.L.; Santos, J.M.; Batista, G.S.; Gimenes, R.; Martins, T.A. Resistance of Rose Rootstocks to Meloidogyne hapla Nematode. In Proceedings of the II International Conference on Landscape and Urban Horticulture 881, Bologna, Italy, 9–13 June 2009. [Google Scholar]
  90. Meressa, B.H.; Dehne, H.W.; Hallmann, J. Population Dynamics and Damage Potential of Meloidogyne hapla to Rose Rootstock Species. J. Phytopathol. 2016, 164, 711–721. [Google Scholar] [CrossRef]
  91. Manners, A.G.; Dembowski, B.R.; Healey, M.A. Biological control of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), in gerberas, chrysanthemums and roses. Aust. J. Entomol. 2013, 52, 246–258. [Google Scholar] [CrossRef] [Green Version]
  92. Avellaneda, J.; Díaz, M.; Coy-Barrera, E.; Rodríguez, D.; Osorio, C. Rose volatile compounds allow the design of new control strategies for the western flower thrips (Frankliniella occidentalis). J. Pest Sci. 2021, 94, 129–142. [Google Scholar] [CrossRef]
  93. Mitrofanova, I.V.; Mitrofanova, O.V.; Brailko, V.A.; Lesnikova-Sedoshenko, N.P. Biotechnological and physiological features of the essential oil rose valuable genotypes in vitro cultivation. News Univ. Appl. Chem. Biotechnol. 2015, 2, 37–48. [Google Scholar]
  94. Pati, P.K.; Rath, S.P.; Sharma, M.; Sood, A.; Ahuja, P.S. In vitro propagation of rose—A review. Biotechnol. Adv. 2006, 24, 94–114. [Google Scholar] [CrossRef] [PubMed]
  95. Olson, J.; Rebek, E.J.; Schnelle, M.A. Rose Rosette Disease. Available online: https://shareok.org/bitstream/handle/11244/319875/oksa_epp_7329_2017-03.pdf?sequence=1 (accessed on 22 February 2022).
  96. Pashtetskiy, V.S.; Timasheva, L.A.; Pekhova, O.A.; Danilova, I.L.; Serebryakova, O.A. Essential Oils and Their Quality; IT “Arial”: Simferopol, Russia, 2021; 212p. [Google Scholar]
  97. Panattoni, A.; Luvisi, A.; Triolo, E. Review. Elimination of viruses in plants: Twenty years of progress. Span. J. Agric. Res. 2013, 1, 173–188. [Google Scholar] [CrossRef] [Green Version]
  98. Mitrofanova, O.V.; Mitrofanova, I.V.; Lesnikova-Sedoshenko, N.P.; Ivanova, N.N. Application of biotechnological methods in plant health improvement and virus-free planting material of promising flower and ornamental crops propagation. Plant Biol. Hortic. Theory Innov. 2014, 138, 5–56. [Google Scholar]
  99. Yegorova, N.; Stavtzeva, I.; Zolotilov, V. Micropropagation in vitro of essential oil rose hybrids obtained in embryoculture. In Proceedings of the BIO Web of Conferences, Simferopol, Russia, 28 October 2021. [Google Scholar]
  100. Khosh-Khui, M. Biotechnology of Scented Roses: A Review. Int. J. Hortic. Sci. Technol. 2014, 1, 1–20. [Google Scholar]
  101. Grondeau, C.; Samson, R.; Sands, D.C. A Review of Thermotherapy to Free Plant Materials from Pathogens, Especially Seeds from Bacteria. CRC Crit. Rev. Plant Sci. 1994, 13, 57–75. [Google Scholar] [CrossRef]
  102. Lerch, B. On the inhibition of plant virus multiplication by ribavirin. Antivir. Res. 1987, 7, 257–270. [Google Scholar] [CrossRef]
  103. Yegorova, N.A.; Stavtseva, I.V.; Mitrofanova, I.V. Morphogenesis in the essential rose oil meristem culture during in vitro chemotherapy. Bull. State Nikitsk. Bot. Gard. 2017, 125, 65–72. [Google Scholar]
  104. Ghorbani, A.; Hadifar, S.; Salari, R.; Izadpanah, K.; Burmistrz, M.; Afsharifar, A.; Eskandari, M.H.; Niazi, A.; Denes, C.E.; Neely, G.G. A short overview of CRISPR-Cas technology and its application in viral disease control. Transgenic Res. 2021, 30, 221–238. [Google Scholar] [CrossRef]
  105. Khan, Z.A.; Kumar, R.; Dasgupta, I. CRISPR/Cas-Mediated Resistance against Viruses in Plants. Int. J. Mol. Sci. 2022, 23, 2303. [Google Scholar]
  106. Taliansky, M.; Samarskaya, V.; Zavriev, S.K.; Fesenko, I.; Kalinina, N.O.; Love, A.J. RNA-Based Technologies for Engineering Plant Virus Resistance. Plants 2021, 10, 82. [Google Scholar] [CrossRef] [PubMed]
  107. Zhao, Y.; Yang, X.; Zhou, G.; Zhang, T. Engineering plant virus resistance: From RNA silencing to genome editing strategies. Plant Biotechnol. J. 2020, 18, 328–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  108. Guo, D.; Maiss, E.; Adam, G.; Casper, R.M. Prunus necrotic ringspot ilarvirus: Nucleotide sequence of RNA3 and the relationship to other ilarviruses based on coat protein comparison. J. Gen. Virol. 1995, 76, 1073–1079. [Google Scholar] [CrossRef]
  109. Pallas, V.; Aparicio, F.; Herranz, M.C.; Sanchez-Navarro, J.A.; Scott, S.W. The molecular Biology of Ilarviruses. Adv. Virus Res. 2013, 87, 139–181. [Google Scholar] [PubMed]
  110. Koper-Zwarthoff, E.C.; Bol, J.F. Nucleotide sequence of the putative recognition site for coat protein in the RNAs of alfalfa mosaic virus and tobacco streak virus. Nucleic Acids Res. 1980, 8, 3307–3318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  111. Reusken, C.; Neeleman, L.; Bol, J.F. The 3′-untranslated region of alfalfa mosaic virus RNA 3 contains at least two independent binding sites for viral coat protein. Nucleic Acids Res. 1994, 22, 1346–1353. [Google Scholar] [CrossRef]
  112. Sehnke, P.C.; Mason, A.M.; Hood, S.J.; Lister, R.M.; Johnson, J.E. A “zinc-finger”-type binding domain in tobacco streak virus coat protein. Virology 1989, 168, 48–56. [Google Scholar] [CrossRef]
  113. Gao, F.; Lin, W.; Shen, J.; Liao, F. Genetic diversity and molecular evolution of arabis mosaic virus based on the CP gene sequence. Arch. Virol. 2016, 161, 1047–1051. [Google Scholar] [CrossRef]
  114. Sánchez-Navarro, J.A.; Pallás, V. Evolutionary relationships in the ilarviruses: Nucleotide sequence of prunus necrotic ringspot virus RNA 3. Arch. Virol. 1997, 142, 749–763. [Google Scholar] [CrossRef]
  115. Sánchez-Navarro, J.A.; Pallás, V. Nucleotide sequence of apple mosaic ilarvirus RNA 4. J. Gen. Virol. 1994, 75, 1441–1445. [Google Scholar] [CrossRef]
  116. Shiel, P.J.; Alrefai, R.H.; Domier, L.L.; Korban, S.S.; Berger, P.H. The complete nucleotide sequence of apple mosaic virus RNA-3. Arch. Virol. 1995, 140, 1247–1256. [Google Scholar] [CrossRef] [PubMed]
  117. Shiel, P.J.; Berger, P.H. The complete nucleotide sequence of apple mosaic virus (ApMV) RNA 1 and RNA 2: ApMV is more closely related to alfalfa mosaic virus than to other ilarviruses. J. Gen. Virol. 2000, 81, 273–278. [Google Scholar] [CrossRef] [PubMed]
  118. Wetzel, T.; Meunier, L.; Jaeger, U.; Reustle, G.M.; Krczal, G. Complete nucleotide sequences of the RNAS 2 of German isolates of Grapevine fanleaf and Arabis mosaic nepoviruses. Virus Res. 2001, 75, 139–145. [Google Scholar] [CrossRef]
Horticulturae 08 00629 g001 550
Figure 1. Features specific to viral disease progression from inoculation to viral spread in tissues and other plant organs (A) Virus entry: infiltration of viral particles or nucleic acid into the cytoplasm via a biological object or sap-transmission; infiltration into the plant cell from another infected cell via plasmodesma. (B) Further progression of a viral infection: specific damage to cellular compartments whereby the virus uses the protein synthesis and RNA/DNA synthesis systems of infected cells (nucleus, plastids and pro- and eukaryotic ribosomes); successive spread of the virus by near and far transport via plasmodesmata as well as by means of the phloem transport, subject to the nature of the virus, the speed at which it spreads and the ways it spreads. (I) The upper epidermis (II) The columnar parenchyma (III) The spongy parenchyma (IV) The vascular system (V) The lower epidermis (VI) The viral infection manifestation in the upper epidermis (VII) Progression of a viral infection in the columnar parenchyma (VIII) Progression of a viral infection in the spongy parenchyma (IX) Viral infection-caused death of cells (X) Virus entry into the vascular system (1) The cytoskeleton (2) The chloroplast (3) The mitochondrion (4) Viral particles (5) The nucleus with the reticulum elements (6) The vacuole (7) Viral proteins in the form of crystals (8) The vacuole with viral crystals and invagination (9) Crystal and viral particle formation in the plastid.
Figure 1. Features specific to viral disease progression from inoculation to viral spread in tissues and other plant organs (A) Virus entry: infiltration of viral particles or nucleic acid into the cytoplasm via a biological object or sap-transmission; infiltration into the plant cell from another infected cell via plasmodesma. (B) Further progression of a viral infection: specific damage to cellular compartments whereby the virus uses the protein synthesis and RNA/DNA synthesis systems of infected cells (nucleus, plastids and pro- and eukaryotic ribosomes); successive spread of the virus by near and far transport via plasmodesmata as well as by means of the phloem transport, subject to the nature of the virus, the speed at which it spreads and the ways it spreads. (I) The upper epidermis (II) The columnar parenchyma (III) The spongy parenchyma (IV) The vascular system (V) The lower epidermis (VI) The viral infection manifestation in the upper epidermis (VII) Progression of a viral infection in the columnar parenchyma (VIII) Progression of a viral infection in the spongy parenchyma (IX) Viral infection-caused death of cells (X) Virus entry into the vascular system (1) The cytoskeleton (2) The chloroplast (3) The mitochondrion (4) Viral particles (5) The nucleus with the reticulum elements (6) The vacuole (7) Viral proteins in the form of crystals (8) The vacuole with viral crystals and invagination (9) Crystal and viral particle formation in the plastid.
Horticulturae 08 00629 g001
Horticulturae 08 00629 g002 550
Figure 2. (A) Symptoms of viral diseases affecting Rosa L. species (mosaic, ringspot, wrinkling, bronzing). (B) Similar symptoms of viral and other diseases affecting Rosa L. (chlorosis of various origin resulting from a viral infection and nutritional deficiency; effects of the plant treatment with plant growth regulators and/or auxin herbicides or viral wilting; bacterial, fungal or viral spots; marginal effects caused by viral streak disease or micronutrients deficiency or imbalance; leaf development upon viral infection or impaired hormonal balance).
Figure 2. (A) Symptoms of viral diseases affecting Rosa L. species (mosaic, ringspot, wrinkling, bronzing). (B) Similar symptoms of viral and other diseases affecting Rosa L. (chlorosis of various origin resulting from a viral infection and nutritional deficiency; effects of the plant treatment with plant growth regulators and/or auxin herbicides or viral wilting; bacterial, fungal or viral spots; marginal effects caused by viral streak disease or micronutrients deficiency or imbalance; leaf development upon viral infection or impaired hormonal balance).
Horticulturae 08 00629 g002
Horticulturae 08 00629 g003 550
Figure 3. Pest vectors of the viruses affecting Rosa L. plants (nematodes, aphids, mites and thrips). The infection spreads from the bottom-up the phloem as the plant grows. For this reason, viral particles may be present in an outwardly healthy part of the plant.
Figure 3. Pest vectors of the viruses affecting Rosa L. plants (nematodes, aphids, mites and thrips). The infection spreads from the bottom-up the phloem as the plant grows. For this reason, viral particles may be present in an outwardly healthy part of the plant.
Horticulturae 08 00629 g003
Horticulturae 08 00629 g004 550
Figure 4. The most common causes of the viruses spread in nurseries and farms. (A) Scion. (B) Rootstock. For propagation, only intact fragments of cuttings of rose bushes are selected. Infected fragments can cause inevitable multiplication of infected and defective material resulting in a severe epiphytoty and viral spread in the nursery.
Figure 4. The most common causes of the viruses spread in nurseries and farms. (A) Scion. (B) Rootstock. For propagation, only intact fragments of cuttings of rose bushes are selected. Infected fragments can cause inevitable multiplication of infected and defective material resulting in a severe epiphytoty and viral spread in the nursery.
Horticulturae 08 00629 g004
Horticulturae 08 00629 g005 550
Figure 5. Compliance with the spatial isolation regulations and preventive agronomic practices applied to control viral diseases. (A) Plant distancing. (B) Row distancing. (C) Reducing the frequency of weeding to prevent the contact of pests with healthy plants. (D) Spacing other plants between rows. (E) Well-timed removal and disposal of weed plants. (F) Visual inspection, primary diagnosis, treatment and testing of the plants showing visual signs of damage. (G) Treatment and testing of the plants showing signs of a viral infection, removal of the infested plants.
Figure 5. Compliance with the spatial isolation regulations and preventive agronomic practices applied to control viral diseases. (A) Plant distancing. (B) Row distancing. (C) Reducing the frequency of weeding to prevent the contact of pests with healthy plants. (D) Spacing other plants between rows. (E) Well-timed removal and disposal of weed plants. (F) Visual inspection, primary diagnosis, treatment and testing of the plants showing visual signs of damage. (G) Treatment and testing of the plants showing signs of a viral infection, removal of the infested plants.
Horticulturae 08 00629 g005
Table
Table 1. List of viruses infecting Rosa L. plants.
Table 1. List of viruses infecting Rosa L. plants.
VirusAcronymReference
Prunus necrotic ringspot virusPNRSV[20,23,24,25,26,27]
Apple mosaic virusApMV
Arabis mosaic virusArMV
Tobacco streak virusTSV
Tobacco ringspot virusTRSV
Tomato ringspot virusToRSV
Tomato spotted wilt virusTSWV
Tomato yellow ring virusTYRV
Strawberry latent ringspot virusSLRSV
Blackberry chlorotic ringspot virusBCRV
Raspberry ringspot virusRpRSV
Cherry necrotic rusty mottle virusCNRMV
Impatiens necrotic spot virusINSV
Apple chlorotic leaf spot virusACLSV
Apple stem grooving virusASGV
Iris yellow spot virusIYSV
Rose rosette virusRRV
Rose leaf curl virusRoLCuV
Rose spring dwarf-associated virusRSDaV
Rose yellow vein virusRYVV
Rose cryptic virus-1RoCV-1
Rose yellow mosaic virusRoYMV
Rosa rugosa leaf distortion virusRrLDV
Rose yellow leaf virusRYLV
Rose chlorotic ringspot virusRoCRSV
Rose necrotic mosaic virusRoNMV
Rose leaf rosette-associated virusRLRaV
Rose colour break virusRCBV
Table
Table 2. Viruses specific to Rosa L. plants.
Table 2. Viruses specific to Rosa L. plants.
VirusSymptomsVirus Spread MechanismCountryReference
Rose leaf curl virusPronounced leaf stunted growth and curlingNot specifiedPakistan[29]
Dwarfing, leaf distortion and leaf curlingNot specifiedIndia[30]
Rose rosette virusShoot elongation and colouring from light pink to dark purple; thorn proliferation; leaf elongation, distortion and red pigmentation; petioles shortening; reduced flowering; lateral buds coming out of dormancy, growing and colouring red. Eriophyid mite Phyllocoptes fructiphylusUSA[31]
Leaf curling and puckering; flower distortion; persistent red pigmentationNot specifiedIndia[32]
Excessive thorn production; “witch’s broom” rosetting; abundance of lateral shoots; shoots coloring red; leaves and flowers mottling or distortion; lateral shoot growth.Eriophyid mite Phyllocoptes fructiphilusUSA[33]
Rose spring dwarf-associated virusRosetting; leaves shortening with vein clearing or netting; shoot zigzag growth pattern.Aphids Metapolophium dirhodum and Rhodobium porosumUSA[34]
Yellow vein chlorosisAphid Rhodobium porosumChile[35]
Not specifiedAphid Rhodobium porosumTurkey[36]
Leaf rosettingAphid Metapolophium dirhodumNew Zealand[24]
Not specifiedNot specifiedChina[37]
Not specifiedNot specifiedTurkey[38]
Rose yellow vein virusNot specifiedNot specifiedNew Zealand[24]
Mosaic and vein yellowingGraftingUSA[39]
Vein banding, central vein chlorosisNot specifiedTurkey[40]
Rosa rugosa leaf distortion virusLeaf stunted growth and distortion; pale circular lines appearing only on early spring growthNot specifiedUSA[41]
Leaf distortion and stunted growth; pale circular lines appearing only on early spring growthGraftingUSA[39]
Vein yellowingNot specifiedTurkey[38]
Rose color break virusDeformed, flecked and streaked petalsSap-transmission and use of infected budwoodEgypt[27]
Rose yellow leaf virusLeaf premature yellowing and senescenceNot specifiedUSA[41]
Leaf premature yellowing and senescenceGraftingUSA[39]
Rose cryptic virus 1Not specifiedNot specifiedUSA[42]
Leaf mottling and necrosisNot specifiedNew Zealand[24]
Leaf banding, mottling and distortionNot specifiedUK[43]
MottlingNot specifiedTurkey[38]
Rose transient mosaic virusLeaf mosaic and yellowingNot specifiedMinnesota, the USA[41]
Rose leaf rosette-associated virusLeaf rosette (“witch’s broom” symptom) formed by dense small leaves on branches; clearly noticeable decay, destruction and, finally, dieback of plantsNot specifiedChina[44]
Not specifiedNot specifiedUSA[45]
Rose necrotic mosaic virusMosaic, necrotic streaks, leaf distortionNot specifiedUSA[41]
Rose partitivirusNot specifiedNot specifiedCanada[46]
Rose yellow mosaic virusYellow mosaic; ring mosaic; premature leaf senescence and dark-brown rings on canesNot specifiedMinnesota, the USA[41]
Yellow mosaic; premature leaf senescenceGraftingMinnesota, the USA[39]
Yellow chlorotic spotsNot specifiedJapan[47]
Rose Chlorotic Ringspot VirusChlorotic ringspots and mosaic symptomsNot specifiedMinnesota, the USA[41]
Rose virus ALeaf distortion; mosaic symptomsNot specifiedCalifornia, the USA[48]
Table
Table 3. Viruses non-specific to Rosa L. plants.
Table 3. Viruses non-specific to Rosa L. plants.
VirusSymptomsVirus Spread MechanismCountryReference
Apple chlorotic leaf spot virusNot specifiedVegetative propagation and graftingGreece[49]
Apple stem grooving virusLeaf rosetteSap-transmission, transmission on grafting and via infected seed material [27]China[50]
Blackberry chlorotic ringspot virusLeaf rosetteSap-transmission, transmission on grafting [27]China[44]
Not specifiedUSA[51]
Cherry necrotic rusty mottle virusChlorosis and necrotic spots on leavesTransmission via budding and grafting [27]India[52]
Impatiens necrotic spot orthotospovirusSmall necrotic spots; leaves yellowing; ringspots; necrotic streaks; wilting and dwarf symptomsTransmitted by thrips Frankliniella occidentalis; sap-transmission; use of infected budwood [27]Iran[53]
Iris yellow spot orthotospovirusChlorotic and necrotic symptomsThrips, sap-transmission [27]Iran[54]
Raspberry ringspot virusMosaic; chlorosis; leaves curling and distortion; stunted growthNematodes, sap-transmission [27]Germany[55]
Strawberry latent ringspot virusYellow flecking in young leaves and reduction in leaflet sizeNematodes, sap-transmission; grafting [27]India[56]
Tomato ringspot virusBanded chlorosis wrinkling; malformation and chlorotic spots on leavesNematodes (Xiphinema spp.), sap-transmission, grafting [27]Iran[57]
Tomato spotted wilt orthotospovirusNecrotic spots and leaves marginal necrosisThrips, sap-transmission, grafting [27]Iran[58]
Table
Table 4. Description of the viruses causing mosaic in rose plants.
Table 4. Description of the viruses causing mosaic in rose plants.
VirusTaxonomic AffiliationHost PlantsGeographical Region/CountrySymptoms
Prunus necrotic ringspot virusFamily: Bromoviridae
Genus: Ilarvirus [22]		Apple tree (Malus domestica); white mulberry (Morus alba); red mulberry (Morus rubra); sour cherry tree (Prunus cerasus); oriental cherry (Prunus serrulata); sweet cherry (Prunus avium); almond (Prunus dulcis); peach tree (Prunus persica); Japanese plum (Prunus salicina); garden plum (Prunus domestica); apricot tree (Prunus armeniaca); Japanese apricot (Prunus mume); common hop (Humulus lupulus); rose (Rosa spp.)
[22,25,66,67,68,69,70,71,72,73]		Africa: Algeria, Egypt, Morocco, South Africa, Tunisia.
America: Argentina, Brazil, Canada, Chile, Mexico, USA, Uruguay.
Asia: China, India, Iran, Israel, Jordan, Japan, Korea, Lebanon, Saudi Arabia, Syria.
Oceania: Australia, Fiji, New Zealand.
Europe: Albania, Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Latvia, Malta, Moldova, Montenegro, Netherlands, Poland, Russia, Portugal, Romania, Serbia, Slovakia, Slovenia, Spain, Sweden, Turkey, Ukraine, Great Britain [22].		Chlorotic and necrotic ringspots, mottling and vein banding develop on leaves. Stems are covered with necrotic stripes. Flowers are distorted due to a significant diameter reduction, loss of fresh and dry weight as well as petal discoloration and decrease in number [62,66,70,71,73]
Apple mosaic virusFamily: Bromoviridae
Genus: Ilarvirus [22]		Some representatives of the chestnut tree genus (Aesculus); birch tree Betula); Prunus (apricot, peach, cherry, plum, cherry plum); Rosa; Rubus (raspberry, blackberry, blackcurrant); hawthorn (Crataegus); wormwood (Artemisia vulgaris); hazel (Corylus avellana); strawberry (Fragaria ananassa); common hop (Humulus lupulus); apple tree (Malus domestica); common pear (Pyrus communis); redcurrant (Ribes rubrum); wild clary (Salvia verbenaca); rowan (Sorbus aucuparia) [8,22,74,75]Africa: Algeria, Ethiopia, Kenya, Morocco, South Africa, Tunisia, Zimbabwe.
America: Argentina, Brazil, Canada, Chile, Mexico, USA, Uruguay;
Asia: China, India, Japan, Jordan, Lebanon, Syria.
Europe: Austria, Azerbaijan, Belarus, Belgium, Bosnia and Herzegovina, Bulgaria, Cyprus, Czech Republic, Denmark, Finland, France, Germany, Greece, Hungary, Italy, Latvia, Netherlands, Norway, Poland, Portugal, Romania, Russia, Serbia, Slovakia, Slovenia, Spain, Sweden, Switzerland, Turkey, Ukraine, Great Britain.
Oceania: Australia, New Zealand [22].		Leaves turn wrinkled and distorted and manifest linear patterns, chlorotic ringspots, mottling and vein banding
[65,74].
Arabis mosaic virusFamily: Secoviridae
Genus: Nepovirus [22]		Grapevine (Vitis vinifera); apricot (Prunus armeniaca); sweet cherry (Prunus avium); plum (Prunus domestica); almond (Prunus dulcis); cherry laurel (Prunus laurocerasus); peach (Prunus persica); rhubarb (Rheum rhabarbarum); raspberry (Rubus idaeus); black elderberry (Sambucus nigra); representatives of the genus Gladiolus; celery (Apium graveolens); horseradish (Armoracia rusticana); common beet (Beta vulgaris); strawberry (Fragaria ananassa); common hop (Humulus lupulus); lettuce (Lactuca sativa); olive (Olea europaea) [22,76]Africa: Egypt, South Africa.
America: Canada, Chile, Mexico, Peru, USA.
Asia: Kazakhstan, India, Iran, Japan, Lebanon, Syria.
Oceania: Australia, New Zealand.
Europe: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, Finland, France, Germany, Greece, Hungary, Ireland, Italy, Latvia, Lithuania, Luxembourg, Moldova, Netherlands, Norway, Poland, Russia, Romania, Serbia, Slovakia, Slovenia, Spain, Sweden, Switzerland, Turkey, Ukraine, Belarus, Great Britain [22,76].		Chlorotic spots on the first leaves followed by mottling and ringspots. Later on the developing leaves show little to no symptoms [27].
Table
Table 5. Pests of Rosa L. plant (potentially) contributing to the spread of viruses.
Table 5. Pests of Rosa L. plant (potentially) contributing to the spread of viruses.
PestMechanism of Damage to the PlantInfection SymptomsReference
Mites
Phyllocoptes fructiphilusMites overwintering on plants and feeding on plant tissues; transfer by insects, wind and with clothesNot specified[83]
Tetranychus urticaeNot specifiedLeaves mottling and drying[84]
Toxic substances injected by insectLeaves yellowing; reduced photosynthesis; petals darkening and falling[85]
Not specifiedWhite tiny flecks at the points of puncture by the mite’s mouthparts on the upper surface of the leaf; plants pale yellowing; dull foliage; leaves and buds inlacing with a cobweb[86]
Mites feeding on the cell content mainly on the lower surface of the lamina causing destruction of the epidermis and underlying cellsLight spots on the upper surface of leaves; leaves turning yellow-brown and drying out[87]
Female mites wintering under the plant debris and the bark of shrubs; colonizing young leaves in spring; weaving a web and laying eggs while feedingLeaves yellowing, distortion and drying; buds failing to open.[88]
Nematodes
Meloidogyne haplaNot specifiedLeaves yellowing and prematurely falling; small shoots; reduced productivity and quality of flowers (the stem length and the flower size); symptoms of mineral deficiency; roots bearing galls; necrosis, segments dying-off, bark reducing and failing, roots shrinking and cracking[89]
Not specifiedThe root system distortion; leaf chlorosis; the stem size decreasing[90]
Sedentary internal parasites cutting tunnels in the plant root and creating permanent feeding sites without leaving themGiant cells developing at the feeding site; hyperplasia of the cortical and vascular parenchyma; retarded meristematic activity in the root tips[26]
Xiphinema diversicaudatumMigratory external parasites feeding outside the root systemGalls caused by the cortical cells’ hyperplasia developing at the feeding site; cells growing in size two–three fold; retarded meristematic activity [26]
Thrips
FrankliniellaoccidentalisNot specifiedRetarded or stunted growth of leaves and transmission of certain plant viruses (for instance, Tomato spotted wilt virus).[91]
Immature and adult specimens feeding on the plant tissues by means of their piercing-sucking mouthparts; damage caused by females’ saw-like ovipositor used for laying eggs in leaves, petioles, flower bracts and petalsSurface damage followed by necrotic spots; impaired photosynthesis capacity[92]
Frankliniella triticiNot specifiedBuds turning brownish; petals curling up[84]
Thrips tabaciNot specifiedImpaired decorative value of leaves and flowers; white flecks on leaves and buds; leaves tarnishing, turning from green to various shades of brown and falling; decreased intensity of flowers’ colour and brightness; silvery dots on the petals developing into stripes[86]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Seitadzhieva, S.; Gulevich, A.A.; Yegorova, N.; Nevkrytaya, N.; Abdurashytov, S.; Radchenko, L.; Pashtetskiy, V.; Baranova, E.N. Viral Infection Control in the Essential Oil-Bearing Rose Nursery: Collection Maintenance and Monitoring. Horticulturae 2022, 8, 629. https://doi.org/10.3390/horticulturae8070629

AMA Style

Seitadzhieva S, Gulevich AA, Yegorova N, Nevkrytaya N, Abdurashytov S, Radchenko L, Pashtetskiy V, Baranova EN. Viral Infection Control in the Essential Oil-Bearing Rose Nursery: Collection Maintenance and Monitoring. Horticulturae. 2022; 8(7):629. https://doi.org/10.3390/horticulturae8070629

Chicago/Turabian Style

Seitadzhieva, Sevilia, Alexander A. Gulevich, Natalya Yegorova, Natalya Nevkrytaya, Suleiman Abdurashytov, Lyudmila Radchenko, Vladimir Pashtetskiy, and Ekaterina N. Baranova. 2022. "Viral Infection Control in the Essential Oil-Bearing Rose Nursery: Collection Maintenance and Monitoring" Horticulturae 8, no. 7: 629. https://doi.org/10.3390/horticulturae8070629

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop