Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 7 Number 04 (2018) Journal homepage: http://www.ijcmas.com

Review Article https://doi.org/10.20546/ijcmas.2018.704.281

Ilarviruses and the Importance of Certified Elite Planting Material in Apple Production System - An Overview

Shelly Kapoor1, Abhilasha Sharma2, Bunty Shylla3 and Anil Handa2*

1Department of Biotechnology, 2Department of Plant Pathology, Dr. Y S Parmar University of Horticulture and Forestry, Nauni- 173230, Solan, Himachal Pradesh, India 3Horticulture Research & Training Station and KVK, Kandaghat, Himachal Pradesh, India

*Corresponding author

ABSTRACT

A wide range of graft transmissible pathogens (GTPs) of viral, viroid and phytoplasma etiology affect apple trees resulting in diseases with adverse effects in orchards around the globe. The significance of diseases caused by these GTPs on tree health, fruit

shape and quality has resulted in the imposition of legislation based quarantine measures at both domestic and international front. Losses resulting from viruses in apple often remain unnoticed as the impact of these pathogens on productivity is evident over a period of time. Out of all the viruses infecting apple, ilarviruses K e yw or ds infecting apple are of utmost importance because of their worldwide occurrence and latent nature in a number of hosts. Since effective management strategies largely Graft transmissible depend on the correct identification of diseases and their etiological agents, diagnosis pathogens (GTPs), and detection are the most important aspects of managing viruses in an economically Apple viable apple production system. Early detection of viruses in the propagative material Article Info is a pre-requisite for checking their effective spread and to guarantee a sustainable fruit production system. Many quarantine programs are in place to reduce inter- Accepted: continental spread of viruses during international exchange of germplasm. All these 20 March 2018 Available Online: phytosanitary measures are overseen by governments based on agreements produced 10 April 2018 by international organizations. Additionally, certification schemes applied to fruit trees allow the production of planting material of known variety and plant health status for local growers by controlling the propagation of pathogen-tested mother plants. They ensure to obtain propagative material not only free of quarantine organisms under the national legislation but also of important non-quarantine

pathogens. Research carried out on the description of ilarviruses (the most important viruses associated with apple industry) with respect to their geographical distribution, taxonomic position, virion properties, host range, symptomatology, transmission, detection and certification schemes for the production of virus indexed elite planting material of apple has been reviewed and discussed in the preceding paragraphs.

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Introduction management, old orchards, and low planting density, besides pathological and Temperate fruits include pome (apple, quince, entomological problems are described to be and pear) and stone fruits (apricot, peach, responsible for low productivity. Climate is plum, almond, and cherry) and are members the most significant environmental variable of the family Rosaceae. These fruits are affecting the production of apple as it needs valued for their attractiveness, taste, low temperatures to break dormancy. The nutritional quality and as a source of earning chilling requirement varies from species to foreign exchange. Cultivation of temperate species. It is an established fact that changes fruits is the mainstay of the economy of the in climatic condition have a major impact on hill farmers of India, though their national the qualitative and quantitative aspects of productivity is far below the international apple fruit production as presence of level. pathogens is influenced by changes in prevailing climatic conditions which in turn Among all temperate horticulture crops, apple increase the risk of introduction of exotic (Malus × domestica Borkh.) is the most diseases. It is particularly important in case of important fruit crop. China is the largest apple systemic pathogens like viruses, viroids and producing country in the world whereas India phytoplasma infecting apple which are of ranks third in apple productivity with an area worldwide distribution. of 3,05,000 ha and production of 22,65,000 MT (Anonymous 2017). In India, apple is Apple crop is attacked by a wide range of mainly cultivated in North Western fungal, bacterial and viral pathogens and Himalayan region which include states of amongst the pathological problems, viral Jammu and Kashmir, Himachal Pradesh and diseases need more attention because virus Uttarakhand in addition to the North Eastern infection is systemic in nature which passes to hilly states of the country. Jammu and the successive generations through the Kashmir is the leading apple growing state propagating material thus causing decline in covering an area of 1,62,971 ha with health of trees. Unlike bacterial and fungal production and productivity of 17,26,834 MT pathogens, viruses cannot be controlled or and 10.1 MT/ha, respectively followed by eliminated by chemical means. Viral Himachal Pradesh that covers an area of pathogens, particularly members of the genus 1,07,700 ha with production and productivity Ilarvirus, cause latent infection which of 7,38,700MT and 6.9 MT/ha, respectively generally remain unnoticed and gradually (Anonymous 2017). Sixty six percent of the result in the loss of plant vigour, reduction in apple production in India is contributed by quality of produce as well as yield of the crop. Jammu and Kashmir followed by Himachal In perennial crops, damage is more profound Pradesh and Uttarakhand accounting for 29.6 in comparison to annuals (Nemeth 1986; and 3.1 percent, respectively. Any losses Cambeli et al., 2003; Cieslinska and Rutkowki occurring to crop would affect the economy 2008). and livelihood of many growers for whom apple is the only cash crop. Ilarviruses in apple fruit trees

Various factors such as unfavourable climatic Losses resulting from viruses in apple often conditions, unsuitable varieties, inadequate remain unnoticed as the impact of these pollinizers, lack of pollinators, inadequate pathogens on productivity is evident over a nutrition, poor soil conditions, poor canopy period of time. Out of all the viruses infecting

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 apple, ilarviruses infecting apple are latent economically important and is a common (produce no visible symptoms) in nature in a pathogen in commercial cultivars (Mink 1989 number of hosts and their infection often and Stouffer 1989). The virus is known by results in retarded plants growth, fewer small different names such as apple infectious sized fruits with a reduced shelf life or other variegation virus, rose infectious chlorosis impacts that often go unnoticed (Hadidi and virus, rose mosaic virus, european plum line Barba, 2011). These viruses cause a wide pattern virus. range of symptoms, ranging from symptomless (latent) to a general decline in Geographical distribution and economic vigour and productivity. Leaf symptoms importance include distortion or twisting, mottling, rolling, necrotic spots, shot holes, and unusual Apple mosaic virus (ApMV), an important color patterns. Fruits may show reductions in virus of apple is prevalent in almost all apple size and quality. Economically, ilarviruses growing countries. ApMV was first reported induce financial losses and have enormous in Rosa sp. and Malus domestica from the economic and social impacts to all USA by White (1928) and Bradford and Joley components of apple production chain. (1933). It is a common pathogen in Ilarviruses induce significant losses in commercial cultivars of apple and is orchards reducing the sustainability of many economically important because considerable commercial orchards in different regions of losses have been reported in apple due to its the world. The major economically important infection. Singh et al., (1979) from India ilarviruses identified on apple are apple studied the effect of apple mosaic virus on the mosaic virus ans prunus necrotic ringspot growth, yield and quality of apple in 30 year virus. Besides these two ilarviruses, prune old ApMV infected and healthy apple trees dwarf virus (PDV) has also been reported to and found that shoot growth, fruit set, fruit be infecting apple trees though the prevalence weight, yield/tree and fruit ascorbic acid of PDV is relatively less. A detailed content were reduced by ApMV infection. description of these ilarviruses with respect to ApMV was reported to decrease bud take of their geographical distribution, taxonomic cvs. Jonathan, Jonared and Golden Delicious, position, virion properties, host range, but not that of Idared. Infected trees of all 4 symptomatology, transmission, detection and cvs. had fewer laterals and their growth was certification schemes for the production of limited. Symptoms were more pronounced on virus indexed elite healthy planting material of leaves of Jonared, Jonathan and Idared in the apple has been critically scanned and second year after budding than during the first presented in this review article. year of growth.

Apple Mosaic Virus (ApMV) The virus decreased bud take in three apple varieties but not in Idared. Most commercial Apple mosaic virus is a member of subgroup cultivars are known to be affected with III of the Ilarvirus genus in the Bromoviridae variable severity of symptoms. 'Golden family (Alrefai et al., 1994). This family also Delicious' and 'Jonathan' are severely affected, includes prunus necrotic ringspot virus whereas 'Winesap' and 'Mclntosh' are only (PNRSV) and rose mosaic virus (Rybicki mildly affected. Except in severe cases, 1995). Mosaic disease of apple is one of the infected trees can still produce a crop and oldest known and most widespread diseases yield reductions may vary from 0 to 50 caused by viruses. Apple mosaic virus is percent (Rebandel et al., 1979).

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In some cultivars, bud set is severely affected. Transmission and host range Apart from that, the presence of ApMV was found to reduce the growth of apple trees No insect vector is known to transmit ApMV (Chamberlain et al., 1971), increase the height but the virus is transmitted by pollen, of the climacteric and decrease the content of vegetative propagation from infected trees or malic acid (Makarski and Agrios 1973). by mechanical sap inoculation to herbaceous hosts (Nemeth 1986). Dhingra (1972) reported The virus was also reported to decrease girth that apple mosaic virus was transmitted by of trees (Thomsen, 1975), decrease bud take both natural and artificial root grafting by 3-20 percent along with stunted growth between apple seedlings in glasshouse (Rebandel et al., 1979) and reduction in the experiments and also by natural root grafting quality and quantity of pollen (Lemoine, in the nursery. Simple intertwining of the roots 1982) in infected apple trees. Forty six percent of adjacent plants could not transmit the virus reduction in yield in ‗Golden Delicious‘ and 9 from infected to healthy plants. percent reduction in McIntosh cultivar due to infection with ApMV was reported by The virus can infect a number of plants and Cambeli et al., (2003). has a wide host range. Experimentally or naturally, it has infected over 65 species in 19 Symptomatology families (Fulton, 1952, 1965). Under experimental conditions, susceptibility to Infection by ApMV is characterized by infection is reported in host species of chlorotic or, more often, bright yellow Apocynaceae, Corylaceae, Leguminosae, discolourations of the leaves in the form of Papilionoideae, Rosaceae and Solanaceae blotching, mottling, vein banding or families. Species susceptible to experimental yellowing, ringspots, line and oak leaf virus infection include Catharanthus roseus, patterns, seldom accompanied by evident Corylus avellana, Malus sylvestris, Nicotiana deformation of the leaf blades (Fulton 1972, tabacum, Phaseolus vulgaris, Cucumis 1980). Pale to bright cream coloured yellow sativus (cucumber), Torenia fournier, Vinca areas develop on apple leaves as they expand rosea (periwinkle) and Vigna during early spring. The mosaic areas may be sinensis (cowpea). Malus sylvestris (apple) cv. irregular in outline or may occur in bands Lord Lambourne and Jonathan develop a along major veins. prominent mosaic and are recommended as woody indicators. These areas often become chrome yellow or white as the season progresses. Fridlund Diagnosis and Detection (1989) reported that affected leaves may be interspersed with normal leaves on individual Serological detection shoot. Leaves which exhibit strong mosaic symptoms in the early season may develop ELISA method was successfully used for the large necrotic areas during period of high detection of 41 isolates of ilarvirus in Prunus temperature or increase sunlight and drop sp. and Malus sp. representing the entire prematurely. In infected plants, symptoms are symptomatic and serological range of prunus usually outstanding in spring but tend to fade necrotic ringspot, apple mosaic virus and away as the season progresses and are little or prune dwarf virus (McMorran and Cameron not evident on summer vegetation (Halk et al., 1983). Barba (1986) used Direct ELISA tests 1984; Imed et al., 1997). for detecting the viruses in different parts of

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 two naturally infected almond trees at for routine testing and avoids the need to different times of year. PNRSV was detected eliminate contaminating DNA in extracts. The by ELISA in all tested plant parts with multiplex RT-PCR assays described are seasonal variations. Detection of the virus reliable, rapid and sensitive methods for the from the leaves was not possible after June. detection of these viruses and may replace Seeds always gave a positive reaction. Sap techniques need commonly like indexing by transmission tests gave positive reactions for woody indicators or ELISA (Menzel et al., PNRSV only in flowers. ApMV was detected 2002). by ELISA both in leaves and seeds. Sap transmission was positive only during the In serological surveys conducted to determine spring from leaves bearing symptoms. the distribution of ApMV in Turkey by using DAS-ELISA one hundred sixteen plant Systemic studies on the distribution of apple samples were collected from 24 orchards and mosaic virus in the main apple growing areas were tested by DAS- ELISA which revealed of the Czech Republic by employing ELISA the presence of ApMV in 6.9 percent of the to detect ApMV in symptomatic apple plants leaf samples (Ylmaz et al., 2005). The virus in almost all the gardens tested were was detected in 15.09 percent of the apple conducted to detect ApMV, ACLSV and plants at two orchards. Polak et al., (2008) ASGV in apple leaf extracts (Polak, 1994). detected four pome fruit viruses in germplasm Out of 220 samples collected, 34 (15.45 collection in the Czech Republic by using percent) were infected with ApMV, 63 (28.6 ELISA as well as pentaplex RT-PCR. A total percent) were infected with ACLSV and 52 of sixty-eight accessions covering native and (23.6 percent) with ASGV. Apple trees which foreign cultivars were tested for the presence gave positive reactions to ELISA were also of the main pome fruit viruses: apple stem tested on herbaceous test plants (Fidan, 1994). pitting virus (ASPV), apple stem grooving Incidence of apple mosaic virus was surveyed virus (ASGV), apple chlorotic leaf spot virus in 140 apple orchards in Tarragona and Girona (ACLSV) and apple mosaic virus (ApMV). provinces. Mosaic symptoms on leaves were Regardless of the cultivars or the origin, observed during spring. ELISA analysis different combinations of mixed infections of revealed that most trees of cv. Golden viruses were found in infected samples. All Delicious were infected with the mosaic positive samples detected by ELISA were disease (Rovira and Aramburu, 1998). confirmed by pentaplex RT-PCR; however, RT-PCR revealed more infected trees than by Multiplex RT-PCR assays are capable of ELISA. ACLSV and ASPV were the most detecting a range of different virus isolates prevailing viruses in apple and pear, the two from various geographic origins throughout viruses were detected in almost all mixed the year. Viruses were detected reliably in infections. Twenty-eight out of 29 apple composite extracts at a ratio of one part total accessions representing fifteen cultivars were nucleic acid extract from an infected sample carrying mixed infection. The most prevailing mixed with 39 parts of extract from healthy viruses of apple were ACLSV (96.5 percent), samples (from Malus, Pyrus, Prunus and ASPV (89.7 percent) and ASGV (34.5 Pyronia sp.). Based on bioassays conducted percent) whereas infection of ApMV was with Nicotiana benthamiana, N. tabacum and detected only in one apple tree. Chenopodium quinoa, the use of the internal control minimizes the risk of obtaining false In a study conducted in Turkey by Birisik et negative RT-PCR results which is desirable al., (2008) on the incidence of apple (Malus

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 domestica) viruses, a total of 108 orchards and stone fruits simultaneously. For RT-PCR, a 10 varietal collections were visited in the degenerate antisense primer was designed districts of Adana, Antalya, K. Maras and which was used in conjunction with three Osmaniye. Some 413 samples of leaves and/or virus-specific sense primers. The dormant cuttings were obtained from apple amplification efficiencies for the detection of trees. Sanitary testing was conducted by the three viruses in the multiplex RT-PCR ELISA, biological indexing, and RT-PCR. All reaction were identical to those obtained in the samples were tested by ELISA for the single RT-PCR reactions for individual presence of apple chlorotic leaf spot virus viruses. (ACLSV), apple stem grooving virus (ASGV) and apple mosaic virus (ApMV). The overall A sensitive and reliable multiplex RT-PCR- virus infection rate as revealed by ELISA was ELISA technique for the detection of apple 18.8 percent. The prevailing viruses were chlorotic leaf spot virus, apple stem pitting ACLSV (10.6 percent), ASGV (5.0 percent) virus, apple mosaic virus and apple stem and ApMV (3.1 percent). Biological indexing grooving virus was developed by material was conducted with the indicators Malus Menzel et al., (2003). Roussel et al., (2004) pumila cultivars Virginia Crab and Radiant developed RT-PCR protocols suitable for a and R 12740 7A against apple viruses in routine diagnosis of latent and ilarviruses in Turkey. Biological indexing revealed higher fruit tree certification. This technique was rates of ACLSV (46.8 percent), ASGV (60.8 simplified by using crude plant extracts percent) and apple stem pitting virus (ASPV; instead of total RNA preparations and by the 54.5 percent) infection. RT-PCR tests also analyses of pooled samples. Paunovic and confirmed the presence of ASPV, ASGV and Jevremovic (2008) detected pome fruit viruses ACLSV detected previously by ELISA and (ACLSV, ASPV, ASGV and ApMV) in biological indexing. This preliminary survey twenty pome fruit cultivars (11 apple, 6 pear reveals high rates of virus infection in apple in and 3 quince cultivars) through the use of eastern Turkey. Concentrations of ApMV different methods. The reliability of virus varies in different plant parts as indicated by detection was tested by biological indexing Svoboda and Polak (2010) who used leaves, under field and the results were compared flower petals, dormant buds and phloem with those of laboratory DAS-ELISA tests and tissues for the detection of ApMV and RT-PCR method for ASPV and ASGV. The reported the highest relative virus viruses, either individually or in mixed concentration in young leaves in April before infection, were detected in 7 of the cultivars. flowering. ApMV was not detected in any of the cultivars by biological and laboratory testing. With Molecular detection regard to the detection of ACLSV, the results were not dependent on the detection technique The complete nucleotide sequence of ApMV and the use of DAS-ELISA for routine testing has been characterized from several parts of was justified. The results also suggested that the world (Alrefai et al., 1994; Shiel et al., ASPV and ASGV may be positively and more 1995; Shiel and Berger 2000; Petrzik and rapidly detected by RT-PCR. Both viruses Lenz 2002). Saade et al., (2000) developed were detected by DAS-ELISA tests in flower nonisotopic molecular hybridization and petals of all infected apple cultivars. Since multiplex reverse-transcription polymerase petals were not always available during chain reaction (RT-PCR) methodologies that certification process, routine usage of DAS- could detect ApMV, PNRSV and ADV in 5 ELISA was rendered unreliable in detection of

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 these viruses. Various other workers (Seigner, Turkey is one of the most important stone fruit 2000; Petrzik and Lenz, 2002; Hou et al., suppliers as it produces around 1.3 million 2004; Petrzik, 2005; Caglayan et al., 2006; tonnes of stone fruits annually (Gumus et al., Polak et al., 2006; Yardmc et al., 2008; 2007). The studies reported the occurrence Thokchom et al., 2009) also reported the use and distribution of all the stone fruit viruses of RT-PCR for successful detection of and viroids in commercial plantings of Prunus different temperate fruit viruses. species in Western Anatolia of Turkey and the studies concluded that PNRSV along with Prunus Necrotic Ring Spot Virus (PNRSV) other viruses like PDV, PPV, ApMV, ACLSV and PLMVd were causing major losses to the Prunus necrotic ring spot virus (PNRSV) was growers of Prunus species. A total of 1732 first reported in peach from USA by Cochran specimens of stone fruits were tested and it and Hutchins (1941) and the name PNRSV was found that overall infection level with was given by Allen (1941). It is a member of these graft transmissible agents was 30 percent the subgroup 3 of the genus Ilarvirus in the with the PDV as the predominant one family Bromoviridae (Bujarski et al., 2012). followed by PPV and PNRSV. PNRSV was The virus is known by various names like reported to be the most common virus European plum line pattern virus, hop B virus, detected in peach and apricot trees grown red currant necrotic ring spot virus, rose vein throughout Algeria (Aouane, 2003). bending virus, rose yellow vein mosaic virus and sour cherry necrotic ring spot virus It is a common pathogen in commercial (Fulton 1985). The virus is of worldwide cultivars of peach and is economically occurrence and is prevalent in many countries important because considerable losses have viz., Jordan (Salem et al., 2003); India been reported in peach due to its infection. (Kulshrestha et al., 2005); Egypt (Salam et al., Scott (2018) studied the effect of prunus 2007); Croatia and Czech Republic (Sucha necrotic ring spot virus on growth, yield and and Svobodova, 2010); Albania, Bosnia, quality of peach and found a reduction in tree Herzegovina, Montenegro, Sebia, Turkey and growth between 12 to 70 percent and yield Ukrain (EPPO PQR, 2012) and Brazil loss of 5 to 70 percent with fruits having lower (Fajardo et al., 2015). Other synonyms of the soluble sugar content. PNRSV has also been virus are European plum line pattern virus, reported to cause significant crop losses hop B virus, red currant necrotic ring spot depending on the host (15 percent yield loss in virus, rose vein bending virus, rose yellow sweet cherry and up to 100 percent in peach) vein mosaic virus and sour cherry necrotic and can reduce bud-take in nurseries, decrease ring spot virus. growth of fruit from 10 to 30 percent and fruit yield reduction from 20 to 60 percent with Geographical distribution and economic delayed fruit maturity (Pallas et al., 2012). importance Symptomatology Prunus necrotic ring spot virus (PNRSV) is an economically important virus and is a Regardless of the host, infection by PNRSV common pathogen in commercial peach remains symptomless as it is a latent virus. cultivars (Brunt et al., 1996). A The virus is however, characterized by brown comprehensive description of PNRSV was lines, rings and leaf curling in most of the made by Fulton (1970) and a review of the hosts (Fulton 1970; Brunt et al., 1996 and virus was prepared by Hammond (2011). Hammond 2011).

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Plate.1 ApMV symptoms on apple cv. Golden Delicious

Plate.2 Severe mosaic symptoms on apple leaves

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Plate.3 PNRSV induced ringspots and chlorotic spots on apple leaves

Plate.4 Diffused chlorotic spots and rings from PNRSV infection in apple

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Almaraz et al., (2014) observed leaf damage to transmit the virus to cucumber or peach in the form of yellow mottle, chlorotic rings, seedlings as seedlings rootstocks remained linear pattern, mosaic, bright yellow symptomless and ELISA also showed discolourations of the leaves in the form of negative results for them. blotching, mottling, vein banding or yellowing, ringspots, line and oak leaf Thrips were used to test the transmission of patterns in commercial peach orchards in the PNRSV to cucumber and peach seedlings Estado de Mexico. The virus is seldom using thrips as vector by applying the infected accompanied by evident deformation of the plum pollen onto cucumber and peach leaf blades (Fulton 1980). Twenty one percent seedlings (Greber et al., 1991. It was found of PNRSV infected sweet cherry trees that Fifty six percent of virus was showing chlorotic ringspots that evolved to transmissible on to both seedlings with Thrips dark brown necrotic areas in both secondary tabaci and sixty six percent with a mixture of veins and interveinal regions of the leaf were five thrips species when pollen were taken reported by Sanchez et al., (2004). Smith et from highly infected flower buds whereas al., (2009) also observed chlorotic and only 7 percent transmission rate was reported necrotic spots on the leaves of sweet cherry when pollen was taken from flowers with less trees infected by PNRSV but the centres of infectivity. Hence, high rate of infection in these necrotic spots often disappeared, pollen is also very important for the affording a shothole effect. The presence of transmission of virus to the plants. PNRSV was also reported by (Scott 2018) in many woody hosts and observed that the Diagnosis and detection infection initially causes shock later developing chronic symptoms. Symptoms can Serological detection be classified as chlorosis, necrosis, leaf deformity, stunting and shot holes. Chlorosis Although many variants of agar gel symptoms include patterns of rings, lines, immunodiffusion tests were commonly used bands, spots, mottles and mosaic occuring for the detection of serological relationships only during the initial acute stage. among ilarviruses (Casper, 1973; Mink et al., 1987; Crosslin and Mink, 1992), sometimes Transmission and host range these failed to detect these viruses in infected plants due to very low concentrations in The virus is not transmissible through insect infected woody plants or the presence of vector but is transmitted by pollen, vegetative inhibitors (Thomas, 1980). Despite all these propagation from infected trees or by problems, serological reactions among mechanical sap inoculation to herbaceous ilarviruses could be easily confirmed by hosts (Brunt et al., 1996; Fulton, 1970; DAS-ELISA. A preliminary survey was Hammond, 2011) and by seeds and pollen in conducted in Tunisia to identify stone fruit several natural hosts, including Prunus sp., viruses as diseases were occurring in orchards hops and roses and in some experimental and mother block stands. Two ilarviruses viz., hosts like Cucurbita maxima (Card et al., prunus necrotic ring spot virus (PNRSV) and 2007, Hammond, 2011). Yuan et al., (1990) prune dwarf virus (PDV) were detected by studied the transmission of PNRSV via DAS-ELISA (Boulila and Marrakchi, 2001). Criconemella xenoplax handpicked from the Apple orchards were surveyed in various root zone of infected peach trees. The studies parts of Himachal Pradesh and samples from concluded that Criconemella xenoplax failed infected trees were collected on the basis of

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 necrotic lesions on leaves (Chandel et al., PCR) were used by Chandel et al., (2008) for 2008). DAS-ELISA was performed using further detection of PNRSV after ELISA. antisera for PNRSV and 88-97 percent of Almaraz et al., (2008) surveyed three virus infection was reported in samples taken locations of commercial peach orchards of from Kullu and Kalpa regions. Similar type of Mexico on the basis of symptoms after sero-surveys conducted by Kapoor and Handa performing DAS-ELISA. The infected sap (2017 b) in peach, almond, cherry, plum, was further inoculated onto Chenopodum nectarine and apricot resulted the presence of quinoa, C.amaranticolor, Nicotiana tabacum, PNRSV in all the hosts tested except for N. glutinosa and Datura stramonium and RT- apricot and plum. Scott et al., (2001) PCR was performed using these indicator conducted field trails to check the effects of plants. Expected size amplicon of PNRSV and PDV on peach and conclusively approximate 450 bp were generated from all proved it to be Peach stunt disease. The these parts thereby clearly indicating the integrity of the viral treatments was assessed presence of PNRSV in the test samples. using ELISA. Salem et al., (2003) tested the Partial characterisation of PNRSV in apple level of PNRSV infection in almond, peach was conducted by Abdel-Salam and Mokbel and plum cultivars over the course of entire (2014) in Egypt. The trees were marked on year by testing different plant parts of the basis of symptoms like chlorotic and naturally infected trees using the double necrotic ring spot along with shotholes on the antibody sandwich-enzyme linked leaves from the apple orchards. RT-PCR immunosorbent assay (DAS-ELISA). The using degenerate primer pair of CP for data revealed spring to be the best time of Ilarvirus was successfully used for the year for PNRSV detection in flowers, active detection and amplification of PNRSV. growing buds and young leaves. Similar results were reported by Kapoor and Handa Moecular detection studies by Hu et al., (2017 a) on the peach cv. July Elberta. Apples (2016) in apple orchards to assess the grown in Himachal Pradesh were found to be incidence of apple chlorotic leaf spot virus susceptible to many viruses and viroids (Rana (ACLSV), apple stem pitting virus (ASPV), et al., 2011).Symptomatic apple cultivars and apple stem grooving virus (ASGV) and apple rootstocks were selected and analysed using mosaic virus (ApMV) revealed that shoot and DAS-ELISA. The presence of five viruses leaf samples were drawn from 216 trees and viz., ApMV, ASGV, ASPV, ACLSV and total RNA was extracted using RT-PCR with PNRSV were observed on the basis of ELISA primer pair ILAR1/ ILAR 2. An amplified tests. Sanchez-Perez et al., (2017) fragment of 204 bp corresponding to the investigated the status of sour and Duke partial Coat Protein (cp) gene of ApMV AND cherry genetic resources in the Iberian PNRSV from 39 samples was obtained. It was Peninsula for the presence of PNRSV and further cloned into the pMD18-T easy vector used DAS-ELISA as the detection method and sequenced. BLAST results showed that and reported the highest infection rate of forty all the sequences had the highest identities to six percent in the leaf samples of both types CP gene of PNRSV with 78 percent identity of cherries. to one isolate (L38823) from United States (Hammond and Crosslin, 1995). To confirm Molecular detection the PNRSV infection in apple, a 1487 bp fragment from RNA3 was amplified using Coat protein gene primers in reverse primer pair PNRSV-RNA3-F1 and PNRSV- transcriptase polymerase chain reaction (RT- RNA3-R1which was further cloned and

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 sequenced. The sequence (KU144878) from and seed. Pollen transmission depends on one infected tree (FSO6) showed identities of many factors such as fruit tree species and 86.3 to 99.1 percent to previously reported circumstances affecting pollination. Pollen PNRSV genome sequences. transmission in sweet and sour cherry shows the highest transmission rates (George and Prune Dwarf Virus (PDV) Davidson 1964; Gilmer 1965). Seed transmission occurs in sweet cherry, sour Prune dwarf virus (PDV) was first described cherry, mahaleb, and myrobalan, but infection by Thomas and Hildebrand (1936) on Prunus rates vary with the species (Caglayan et al., domestica showing stunting and leaf 2006). PDV infection causes yield reduction malformation symptoms. In plum, PDV and is responsible for significant losses in causes stunting and leaf malformation and almond (Nolasco et al., 1991), peach, and shortened internodes. In Italian prune, it sweet cherry (Rampitsch et al., 1995; decreases the length of shoots, their diameter, Uyemoto and Scott, 1992). number of leaves, and the photosynthetic total area (Hadidi and Barba, 2011). In cherry, Certification schemes and programmes PDV may cause leaf chlorotic spots, rings and diffuse mottling, and possibly stem pitting Plant material produced in accordance with and flat limb. Fruits can be malformed and the certification scheme is derived from their production is reduced. In some apricot nuclear stock plants that have been tested and cultivars, PDV has been reported to induce found free from viruses and produced under gummosis on the trunk. In most peach conditions minimizing infection by other graft cultivars, PDV induces mild stunting while transmissible pathogens infecting apple trees. leaves become dark green and more erect than Certified plant material for export should in those of noninfected trees, but infection by any case satisfy the phytosanitary regulations severe isolates can cause important yield of importing countries, especially with respect reduction and poor quality of fruits. Peachs to any of the pathogens covered under the infected with both PDV and PNRSV (peach category of quarantine pests. stunt disease, PSD), display bark splitting, increased sucker production and yield is There are well established certification reduced by up to 60 percent. The virus causes programs and plant protection organizations economic losses on stone fruit trees, in developed countries operate within the especially in sour and sweet cherry, almond, framework of these certification programmes. and peach (Nolasco et al., 1991; Rampitsch et Some of these certification schemes are in al., 1995; Uyemoto and Scott, 1992). PDV operation since the 1960s and have been frequently occurs in mixed infections with delivering high quality virus indexed other ilarviruses. propagation material preventing the introduction of viruses in the fields. NCPN- PDV is a multicomponent virus with five FT (formerly NRSP5 or IR-2), NCPP, and types of particles differing in size. FPS in the USA, CTIFL and SOC in France, Unenveloped virions vary from quasi- EMLA and SASA in the UK, Naktuinbouw in isometric, about 19–20 nm in diameter, to the Netherlands, and CVIPS in Spain are only bacilliform with length up to 73 nm some examples to show the investment (Caglayan et al., 2006). Several strains of various countries have made to promote their PDV have been described. The virus is respective agricultural economy (Boye and transmitted by grafting (buds, scions), pollen Desvignes, 1984; Cutting and Montgomery,

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1973; Ebbels, 1979; Navarro et al., 2002; is older and more popular to nurserymen, the NCPN-FT 2012; Reed and Foster, 2011; preferred term nowadays is pathogen tested Rowhani et al., 2005). and covers only organisms particularly mentioned in the published scheme (usually By the end of the 1990s, Regional Plant viruses, viroids, and phytoplasmas). All Protection Organizations (RPPOs) such as the recent EPPO certification schemes refer only European and Mediterranean Plant Protection to the latter category (EPPO, 2006). Organization (EPPO) and the North American Plant Protection Organization (NAPPO) Furthermore, different approaches for the began drafting technical guidelines for their production of healthy planting material of a member countries concerning the production certain cultivated plant, certification or of certified plant propagation material. classification, may apply. In a typical EPPO According to EPPO, a certification scheme is certification scheme, the certified material is a ―System for the production of vegetatively descended by not more than a fixed number propagated plants for planting, intended for of steps from individual plants each of which further propagation or for sale, obtained from is tested and found free from pests, and is nuclear stock after several propagation stages then maintained and propagated under under conditions ensuring that stated health rigorous conditions excluding standards are met. The filiations of the recontamination. In a classification scheme, material are recorded throughout the scheme.‖ the classified material is descended by one or In line with this, NAPPO defines that a more steps from material which, as a ―virus-certified stock refers to plants for population, meets certain health standards and planting and propagation produced under an is maintained and propagated under official virus testing and certification conditions minimizing recontamination. programme‖ (NAPPO 2013). Consequently, Which of the approaches is appropriate for a certification schemes are essentially quality given cultivated plant depends on control systems for propagating and planting considerations of cost and resources, health material which will be officially certified by status required, practical possibilities for the officially delegated authorities by the testing, rate of recontamination, and value of issuing of a certificate or label. Through the final material. certification, propagating material is assured to be free not only from quarantine organisms Normally, the operation of certification but from important indigenous nonquarantine schemes is run by official governmental pathogens as well, in compliance with each authorities or officially recognized private country‘s requirements as dictated by the organizations, although there are differences local and international markets. between countries and continents. Private companies and nurseries‘ associations are not It is pertinent to note that not all pathogens or precluded from participating in an official viruses can be excluded by a certification scheme (e.g., MIVA in Italy and AVASA in scheme. In the past, two types of categories, Spain) (Pina et al., 2012; Savino, 1992) or virus free and virus tested, have been used. from running their own schemes (e.g., The first corresponds to individual plants companies producing ornamentals) tested for all virus and virus-like pathogens (Waterworth, 1998). known to infect the host in a specific region, while the second one focuses on the most The origin of each plant should be known so important pathogens. Although the first term that any problems of health or trueness to type

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Int.J.Curr.Microbiol.App.Sci (2018) 7(4): 2444-2462 may be traced throughout the certification Journal of General Virology 75: 2847- scheme. The use of propagation material in 2850. nurseries to produce certified plants should be Aouane B. 2003. Preliminary studies on stone checked by an official or officially authorized fruit tree viruses in Algeria. Peach 12: 56- organization that controls the health, origin 286. and amount of such material on the basis of Anonymous. 2017. https://www.faostat.fao.org th field inspections and of the records and (8:00 PM, 10 February, 2018) documents presented by the nursery. The Barba M. 1986. Detection of apple mosaic and nursery plant protection programme and the Prunus necrotic ringspot viruses in check inspections should also take account of almond by ELISA. Archives of other important pests that can affect quality, phytopathology and plant protection 22: 279-282. so that the certified plants delivered to the Birisik N, Myrta A, Hassan M and Baloglu S. fruit grower are substantially free from these 2008. A preliminary account on apple pests. Certified planting material for export viruses in Mediterranean Region of should in any case satisfy the phytosanitary Turkey. Acta Horticulturae 781: 125-130. regulations of importing countries. Certified Boulila M and Marrakchi M. 2001. Sequence plants leaving the scheme should carry an Amplification (RT-PCR) and Restriction official certificate (which may be a label) Fragment Polymorphism (RFLP) indicating the certifying authority, the plant Analysis of Some Isolates of Prunus producer and the certification status of the necrotic ringspot ilarvirus. EPPO Bulletin plants. 31: 173-178. Boye´ R and Desvignes JC. 1984. Bilan des References quinze anne´es de se´lection conservatrice du mate´rielve´ge´tale fruitier. Fruits 39: Almaraz TD, Sanchez-Navarro J and Pallas V. 637–645. 2014. Detection of Prunus necrotic Bradford FC and Joley L. 1933. Infectious ringspot virus in peach (Prunus persica variegation in the apple. Journal of L.) in Mexico and molecular Agricultural Research 46: 901-908. characterization of its RNA component-3. Brunt A A, Crabtree K, Dallwitz MJ, Gibbs AJ, Agrociencia 48: 583-598. Watson L and Zurcher EJ. 1996. Apple Allen WR. 1941. Prunus necrotic ringspot virus mosaic Ilarvirus. Plant Viruses Online: in Peach. Phytopathology 12: 325-333. Descriptions and Lists from the VIDE Abdel-Salam AM and Mokbel SA. 2014. Partial Database. characterization of Prunus necrotic Bujarski J, Figlerowicz M, Gallitelli D, ringspot virus on apple in Egypt. Roossinck MJ and Scott SW. 2012. Egyptian Journal of Virology 11: 280- Family Bromoviridae. In: Virus 287. Taxonomy: Classification and Almaraz Torre DL, Montoya-Piña JV, Rangel Nomenclature of Viruses. AS, Camarena-Gutiérrez G and Salazar- Caglayan K, Serce CU, Gazel M and Jelkmann Segura M. 2008. First Report of Prunus W. 2006. Detection of four apple viruses necrotic ringspot virus in Peach in by ELISA and RT-PCR assays in Turkey. Mexico. Plant Disease 92: 482-482. Turkish Journal of Agriculture and Alrefai RH, Shiel PJ, Domier LL, D‘Arcy CJ, Forestry 30: 241-246. Berger PH and Korban SS. 1994. The Cambeli T, Folwell R J. Wandschneider P. nucleotide sequence of apple mosaic virus Eastwell K C. and Howell W. 2003. coat protein has no similarity with the Economic implications of a virus other Bromoviridae coat protein genes. prevention program in deciduous tree

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How to cite this article:

Shelly Kapoor, Abhilasha Sharma, Bunty Shylla and Anil Handa. 2018. Ilarviruses and the Importance of Certified Elite Planting Material in Apple Production System - An Overview. Int.J.Curr.Microbiol.App.Sci. 7(04): 2444-2462. doi: https://doi.org/10.20546/ijcmas.2018.704.281

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