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Plantwise Technical Factsheet

CYVV (Clover yellow vein virus)

Host plants / species affected
Alysicarpus vaginalis (alyce clover)
Ammi majus (Bishop's-weed)
Borago officinalis (Borage)
Coriandrum sativum (coriander)
Cucurbita pepo (marrow)
Daucus carota (carrot)
Gentiana (gentians)
Gladiolus hybrids (sword lily)
Glycine max (soyabean)
Impatiens walleriana (Busy-lizzy)
Iris (irises)
Lamium amplexicaule (henbit deadnettle)
Lathyrus odoratus (sweet pea)
Lens culinaris subsp. culinaris (lentil)
Limonium sinuatum (sea pink)
Lupinus (lupins)
Lupinus albus (white lupine)
Lupinus angustifolius (lupin)
Lupinus luteus (yellow lupin)
Medicago lupulina (black medick)
Medicago sativa (lucerne)
Melilotus officinalis (Field melilot)
Phaseolus vulgaris (common bean)
Pisum sativum (pea)
Plantago major (broad-leaved plantain)
Psophocarpus tetragonolobus (winged bean)
Trifolium (clovers)
Trifolium hybridum (alsike clover)
Trifolium incarnatum (Crimson clover)
Trifolium pratense (purple clover)
Trifolium repens (white clover)
Trifolium subterraneum (subterranean clover)
Trifolium vesiculosum (Arrowleaf clover)
Veronica persica (creeping speedwell)
Vicia faba (faba bean)
Viola odorata (English violet)
List of symptoms/signs
Growing point  -  dieback
Leaves  -  abnormal leaf fall
Leaves  -  abnormal patterns
Leaves  -  necrotic areas
Leaves  -  yellowed or dead
Seeds  -  distortion
Stems  -  dead heart
Stems  -  dieback
Stems  -  discoloration of bark
Stems  -  stunting or rosetting
Whole plant  -  distortion; rosetting
Whole plant  -  early senescence
Whole plant  -  plant dead; dieback
The external symptoms exhibited in natural hosts have been listed in the section on Host range. In several hosts they consist of spotting and mosaics associated with various degrees of necrosis often entailing death of leaves and premature plant death. Symptoms of ClYVV may be easily confused with those caused by other viruses. The symptoms of ClYVV are usually more necrotic than those of Bean yellow mosaic virus (BYMV), but they may closely resemble those of necrotic strains of BYMV (Bos et al., 1974; Beczner et al., 1976).

Intracellular inclusion bodies are readily visible by light microscopy of stained epidermal strips (Bos, 1969b; Christie and Edwardson, 1986). The inclusions in the cytoplasm are granular as is typical of potyviruses in general. They contain pinwheel structures when viewed by electron microscopy in ultrathin sections (Bos and Rubio-Huertos, 1969; Fox and Corbett, 1985; Lawson et al., 1985). The pinwheels or cylindrical inclusions classify together with those of BYMV in the potyvirus subdivision II inclusions containing laminated aggregates or plates attached to a central cylinder instead of scrolls (Christie and Edwardson, 1977). All ClYVV isolates studied by light microscopy, including Statice virus Y, showed a prominent, often irregular, globular enlargement of the nucleolus, sometimes nearly filling the nuclear space (Bos, 1969a, 1969b; Bos and Rubio-Huertos,1969; Beczner et al., 1976; Bos et al., 1977; Lesemann et al., 1979; Fortass et al., 1991). Such readily observed nucleolar enlargements were never seen with isolates characteristic of BYMV and seem of diagnostic value. The enlarged nucleoli of plants infected by ClYVV-E178 were provided with unusual crystalline needles radiating from the nucleolus and often deforming the nucleus by pushing out the nuclear membrane or even pricking through it (Bos, 1969a, 1969b; Bos and Rubio-Huertos, 1969).

Virus infection often increases susceptibility to parasitic fungi , but has been little studied for clovers. Weakening of plants by viruses including ClYVV is thought to make them more susceptible to damage by other diseases and environmental stresses (Gibson et al., 1981). In a clone of white clover grown in greenhouse experiments, root rot caused by Codinaea fertilis was greater in ClYVV-infected plants than in ClYVV-free plants (Campbell and Moyer, 1983). For effects on plant size and yield, see Economic impact.
Prevention and control
Virus Elimination

It is possible to obtain virus-free white clover plants and descendent clones for experiments using cold or heat treatment (10 or 40°C, respectively), followed by propagation of stem tip cuttings (Baxter and McGlohon, 1959). Up to 83% of plants were freed from ClYVV by using cold treatment followed by culture of excised meristem tips (meristematic dome plus one or two leaf primordia) on a modified Murashige and Skoog medium (Barnett et al., 1975).

Cultural Control and Sanitary Methods

For controlling disease in crops, cultural methods to prevent infection may be hard to implement. Old stands of clover, notably white clover, should be avoided when sowing new crops. Resowing clovers in old pastures is likely to lead to rapid reinfection. Likewise, it is recommended not to grow annual legumes such as faba bean, lupins, Phaseolus vulgaris and pea in the vicinity of old stands of white clover. Data on the effects of interplanting white clover with grass (Festuca arundinacea) to reduce the incidence of ClYVV and Peanut stunt virus (PSV) are conflicting (McLaughlin et al., 1992; Taylor et al., 1995). The beneficial effect of the grass may be limited to conditions where the grass is taller than the clover, thus tempting viruliferous alate aphids to land and probe on grass plants and rid their mouthparts of nonpersistently transmitted virus before moving on to clover.

Host-Plant Resistance

Control emphasis is on the use of resistant cultivars and on selection and breeding for genetic resistance. Most data on virus resistance in clovers originate from observations of field-grown collections with wide spacing that are subject to natural infection. They therefore concern multiple resistance. More targeted screening for resistance is by inoculation in the greenhouse. When submitting cultivars of Phaseolus vulgaris to ClYVV infection by mechanical, hypodermic and aphid inoculation, the percentages of infection were found to differ considerably. Because ClYVV, as well as many other clover viruses, is vectored by aphids in the field, screening plants for resistance by mechanical inoculation, may not, therefore, be a realistic means for identifying resistance or for screening breeding populations or lines (Dwadash-Shreni and Stavely, 1984). Evaluation of resistance is mainly by symptom severity, although this may not be a reliable parameter of resistance to damage (Bos and Parlevliet, 1995). Resistance to infection (true virus resistance) should be distinguished from mere tolerance, and be measured quantitatively by checking the presence of the virus and its concentration in infected plants by bioassay and/or serologically. Symptom appearance may also be delayed in more resistant genotypes (Alconero, 1983b). Considerable attention has been paid to resistance in clovers, but resistance in beans and peas has also been studied.

White clover: resistance to ClYVV was first detected by Barnett and Gibson (1975) and later studies identified resistance to various viruses, including ClYVV, in several cultivars (Harville and Derrick, 1978; Campbell and Moyer, 1983; Ragland et al., 1986). Two clones of 'Tillman' white clover with differential resistance to ClYVV and PSV were used to study the effect of ClYVV on yield (Ragland and Campbell, 1983) and on susceptibility to Codinaea fertilis (Campbell and Moyer, 1983). In Mississippi, USA, germplasm derived from polycross progenies of 22 white clover clones with drought resistance, and registered as 'Brown Loam Synthetic No. 2', exceeded 'Regal' and 'Tillman' for forage yield and persistence for 4 years of testing, and showed significantly less infection by ClYVV and PSV (Knight et al., 1988). Germplasm with resistance to viruses prevalent in southeastern USA has later been registered as 'Southern Regional Virus Resistant' (SRVR) (Gibson et al., 1989). At Lexington, Kentucky, and in Mississippi it was found to have a significantly lower incidence of ClYVV and PSV than cv. Regal (Taylor et al., 1995). Additive genetic effects were important for breeding resistance to the two viruses into SRVR clones (Pederson and McLaughlin, 1994). It is claimed that without virus resistance, particularly to ClYVV and PSV, persistence and high yields cannot be obtained in white clover (Taylor et al., 1995). White clover cultivars with promising resistance to ClYVV found in the former Czechoslovakia are 'NFG Gigant', 'Grasslands Pitau' and 'Kent Wilt White' (Musil et al., 1986).

Hybrid clover: in New York State, USA, delayed symptom development of ClYVV was observed in 87% of the 129 accessions of T. hybridum tested in the greenhouse. In six accessions, at least 20% of the plants tested remained symptomless for at least 6 months, and serology and bioassay showed low virus titres in most of them (Alconero, 1983b). However, virus symptoms appeared early and spread rapidly to result in 100% infection and rapid plant decline in all five plant introduction lines later tested in the field (Alconero et al., 1986).

Subterranean clover: in Mississippi, USA, seedlings of each of the 261 plant introduction (PI) lines and three cultivars of the US germplasm collection of T. subterraneum were mechanically inoculated in the greenhouse with ClYVV and evaluated for symptoms and infection by DAS-ELISA. Symptomless plants were reinoculated and reevaluated up to five times. Fewer than 2% of all tested plants were selected as resistant and held as first-generation parents. From these, seed was obtained through self-pollination and progeny was tested. All plants obtained from the second-generation were susceptible and showed uniformly severe reactions consisting of rapid systemic wilt and plant death. It was finally concluded that no heritable resistance to ClYVV exists in the major portion of the germplasm collection tested. However, some lines reacted hypersensitively, which was thought to be a useful management tool in limiting spread of ClYVV in the field (McLaughlin and Fairbrother, 1994).

Other clovers: T. ambiguum and T. medium performed and persisted well under natural infection pressure by four viruses including ClYVV. They were infected at very low levels as was T. alpestre, but the latter was less vigorous than the first two species (Alconero et al., 1986). Three lines studied in Mississippi, USA, were later found resistant to ClYVV and PSV and registered for release (Pederson et al., 1991). Resistance to the two viruses was also found in an interspecific hybrid of T. ambiguum x T. repens (Pederson and McLaughlin, 1989). A high degree of resistance to ClYVV and its pea necrosis strain was also found in T. alpestre, T ambiguum and T. medium in the former Czechoslovakia (Smrz et al., 1985).

Phaseolus vulgaris: some resistance has been found in cultivars (such as 'Great Northern 123') in Italy (Quagliotti and Lepori, 1981; Lisa and Dellavalle, 1983). In Czechoslovakia, seven out of 48 bean cultivars tested were immune to ClYVV (Bednarek et al., 1988). 'Great Northern 1140' has resistance to BYMV-S (now considered to have been ClYVV) conditioned by a single recessive gene by-3 (Provvidenti and Schroeder, 1973), now designated cyv (Scully et al., 1995). Breeding lines resistant to ClYVV were obtained by crossing 'GN 1140' with 'Black Turtle Soup' (Scully et al., 1991) and five multiple-virus-resistant lines were obtained by crossing with 'Great Northern B21' (Scully et al., 1995). In the Netherlands, 'Great Northern 123' reacted with local lesions to a number of isolates of ClYVV and contracted symptomless systemic infection with Hollings' type isolate of ClYVV whereas the Dutch pea necrosis strain of ClYVV did not infect the cultivar. There was differential interaction with other bean cultivars as well (Bos et al., 1974; Fortass et al., 1991). 'Lasso' was immune to the four isolates of ClYVV as well as to an isolate of pea mosaic strain, but it was susceptible and sensitive to two typical isolates of BYMV (Fortass et al., 1991).

Faba bean: in Germany, a breeding line was found to be highly resistant to three isolates of ClYVV and to 11 strains and 8 isolates of BYMV when different inoculation techniques were used, but another isolate infected 28% of the plants without producing symptoms. The line was also resistant to Aphis fabae (Schmidt et al., 1986).

Pea: results of trials in the Netherlands (Bos et al., 1974), Poland and Hungary (Kowalska, 1979; Beczner et al., 1983) showed that cultivars and breeding lines immune to BYMV were generally resistant to ClYVV. However, although this generally held true for most genotypes in a study in New York State, USA, some accessions from Ethiopia and India were resistant to ClYVV but susceptible to BYMV and some from China and the former USSR were resistant to BYMV but susceptible to ClYVV (Provvidenti, 1987). This indicates the existence of a differential genetic interaction between ClYVV and pea. In the doubly resistant cv. Bonneville, resistance to ClYVV was postulated to be controlled by a single recessive gene (cyv) closely linked to the gene mo that confers resistance to BYMV. In the accessions from Ethiopia and India resistance to ClYVV was controlled by a second gene (cyv2) of a different linkage group, while the accessions from China carried the gene mo (Provvidenti, 1987).
Most of the concern about the impact of ClYVV has focussed on clovers, particularly white clover (Trifolium repens), which are mostly grown as perennials, especially in pastures. By 1975, some 13 viruses had been detected in white clover (Barnett and Gibson, 1975). Fields are often simultaneously infested by more than one virus, and mixed infection of single plants is prevalent. It is, therefore, hard to quantify the effect of ClYVV alone.

In greenhouse experiments, five Ladino clover clones inoculated with Alfalfa mosaic virus (AMV) and ClYVV (then identified as BYMV) showed a 23-55% loss (Kreitlow et al., 1957). Other loss assessments involved comparing clones of clover infected with an accumulation of viruses, including ClYVV, from long-term natural exposure with virus-free plants from these clones obtained by meristem tip culture (Barnett et al., 1975). In six clones of 'Tillman' white clover the average seed yield was reduced by the viruses to 25% of the controls as a consequence of a reduction in the number of heads per plant, number of seeds per head and per floret, and reduced seed weight (Barnett and Gibson, 1977). In another experiment, six clones of 'Tillman' white clover obtained from virus-free seedlings were transplanted to the field and tested for infection. During the first year, Peanut stunt virus (PSV) was more prevalent than ClYVV, early during the next year their incidence was similar, and later that year the incidence of ClYVV was highest and some AMV was also detected. At that time 87% of the plants were virus-infected and the reductions in yield (foliage dry weight), mainly due to ClYVV, ranged from 29.5 to 57.1% (Campbell and Moyer, 1984). In filtered-air enclosures in the field, ClYVV was found to reduce the yield of inoculated Ladino white clover by 9-26%; this was less than PSV (22-40%) and AMV which was intermediate (Gibson et al., 1982). In similar experiments, plants of arrowleaf clover (T. vesiculosum) singly inoculated with AMV, BYMV, ClYVV and PSV, reacted similarly to BYMV and ClYVV. Yield loss was greater for ClYVV than BYMV, reducing the per plant mean weight of oven dry leaves at early inoculation from 13.0 to 1.6 g (Gibson et al., 1979). Under such conditions, ClYVV reduced the total dry weight of white clover leaves from 1.1 to 0.9 g which was less than the damage by AMV and PSV. The length of stolons, the number of rooting nodes on stolons and root nodulation were also reduced by ClYVV (Gibson et al., 1981).

When two 'Ladino' white clover clones were examined in a transplanted clover-tall fescue system under field conditions for response to ClYVV, PSV and ClYVV + PSV infection, all infected plants had considerably lower dry weight yield than plants of initially virus-free clover. Double virus infection reduced dry weights more than infection by either virus alone. Virus infections also reduced the number of stolons per plant, length of stolons, nodes per centimetre of stolon, and rooting nodes per stolon. ClYVV was less severe than PSV (Ragland et al., 1986).

Infection by viruses, including ClYVV, reduces the persistence of clovers in the field, particularly in mixed stands such as pastures (Pratt, 1967). In a field evaluation of several accessions of six clover species, 18-100% of T. pratense plants and 6-25% of T. hybridum remained 1 year after planting, indicating high rates of mortality due to Bean yellow mosaic virus (BYMV), ClYVV, White clover mosaic virus (WCMV) and Red clover vein mosaic virus (RCVMV) (Alconero et al., 1986). ClYVV is claimed to be involved in the decline of subterranean clover in Australian pasture (Helms et al., 1993). A 4-year pasture study in Mississippi, USA, involving infection by a number of viruses, including ClYVV but predominantly PSV, showed a significant decline of the white clover population so that the clover had virtually disappeared from the pasture by the following autumn (McLaughlin et al., 1992). Plants weakened by virus infection are probably more susceptible to damage by other pathogens (such as Codinaea fertilis; Campbell and Moyer, 1983) and environmental stress than uninfected plants (Gibson et al., 1981), which further contributes to the phenomenon of clover decline.

When 19 pastures throughout eight southeastern states of the USA were surveyed for five viruses, incidence of virus infection in fields varied from 0 to 86%. ClYVV was identified in 15 fields, and infection levels of up to 46% plants in a field were reached (Barnett and Gibson, 1975). Together with Alfalfa mosaic virus (AMV) and PSV, ClYVV was one of the most prevalent viruses in white clover in North Carolina and the Southeast of the USA (Lucas and Harper, 1972; Barnett and Gibson, 1975; Ragland et al., 1986; McLaughlin and Boykin, 1988). However, in a field trial in North Carolina in 1990/91, its incidence was low (Nelson and Campbell, 1993). In the southeastern USA, ClYVV was also the most frequently isolated virus from subterranean clover (T. subterraneum; McLaughlin and Fairbrother, 1994). Incidence of infection in clovers may rapidly increase with age of stand, and old stands are a source of infection for newly sown crops nearby. As a perennial, white clover is also thought to act as an important source of ClYVV infection for annual legume crops such as Phaseolus vulgaris.

Clover viruses including ClYVV usually spread rapidly in experimental fields and clonal collections, especially at spaced planting (Taylor et al., 1995). The resulting high rates of infection are helpful when resistance is sought (see also Control; Cope et al., 1978; Alconero et al., 1986). However, they become a nuisance if agronomic traits of breeders' materials are being studied, or germplasm is being multiplied and/or evaluated in the open. In accessions and cultivars of six clover species planted at Geneva, New York State, USA, ClYVV was found in all plants of five accessions of T. hybridum, most plants of T. repens and half of the T. alpestre accessions 1 year after planting (Alconero et al., 1986). In 1991, the virus caused severe disease in 60% of the experimental accessions of subterranean clover grown in field trials in Mississippi, USA (McLaughlin and Fairbrother, 1994).

There is little information on the impact of ClYVV on crops other than clovers. In northwestern Italy in 1976 the virus was present at different locations in up to 50% of the plants of Phaseolus vulgaris and symptoms were severe (Lisa and Dellavalle, 1983). BYMV-S, now considered to be ClYVV, had earlier been considered of sufficient economic importance to study the inheritance of the resistance of P. vulgaris to it (Provvidenti and Schroeder, 1973). So far, reports on the occurrence in non-legume crops such as Calanthe orchids, Gentiana and Limonium have been incidental only; however, necrotic streaking on leaves and stems of such ornamentals are significant defects.
Related treatment support
External factsheets
Cornell University Vegetable MD Online, Cornell University Plant Pathology Department, 1984, English language
Cornell University Vegetable MD Online, Cornell University Plant Pathology Department, 1984, English language
Cornell University Vegetable MD Online, Cornell University Plant Pathology Department, 1984, English language
Department of Agriculture and Food Western Australia Farmnotes, Government of Western Australia, 2010, English language
Clemson Cooperative Extension Factsheets, Clemson University Cooperative Extension, 2004, English language
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