Further viruses of Prunus in New Zealand

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1 New Zealand Journal of Agricultural Research ISSN: (Print) (Online) Journal homepage: Further viruses of Prunus in New Zealand P. R Fry & G. A. Wood To cite this article: P. R Fry & G. A. Wood (1973) Further viruses of Prunus in New Zealand, New Zealand Journal of Agricultural Research, 16:1, , DOI: / To link to this article: Published online: 05 Jan Submit your article to this journal Article views: 228 View related articles Citing articles: 14 View citing articles Full Terms & Conditions of access and use can be found at

2 131 Further viruses of Prunus in New Zealand By P. R. FRY AND G. A. WOOD Plant Diseases Division, DSIR, Private Bag, Auckland, New Zealand (Received 14 August 1972) ABSTRACT The symptoms and incidence of dark green sunken mottle of peach are described, and the relationship of this virus to apple chlorotic leaf spot virus is discussed. Necrotic rusty mottle virus was found infecting three sweet cherry trees and strawberry latent ringspot virus one tree. Sour cherry yellows symptoms were induced in 'Montmorency' sour cherry by dual ir.fection with necrotic ringspot and prune dwarf viruses. A previously undescribed transmissible disorder of apricots is recorded. Peach seedling chlorosis is suggested as the name for leaf symptoms transmitted to peach seedlings from symptomless plum and cherry trees. INTRODUCTION Virus diseases of Prullus species that have already been described as occurring in New Zealand are plum mosaic (Chamberlain et al. 1951), Moorpark mottle (Chamberlain et al. 1954), peach calico (Chamberlain et al. 1957), plum fruit crinkle (Chamberlain et al. 1959), little cherry (Fry & Wood 1970), cherry rasp leaf (Atkinson 1971), cherry green ring mottle (syn. rough bark) (Chamberlain et al. 1971), PrUllUS necrotic ringspot and prune dwarf (Fry & Wood 1971), and cherry rusty spot (Wood 1972). The possible relationship of dark green sunken mottle virus to the peach rosette syndrome was discussed by Fry & Wood (1969). The present paper gives further information on the incidence and identity of dark green sunken mottle virus. Necrotic rusty mottle virus and strawberry latent ringspot virus are recorded. Sour cherry yellows symptoms are shown to be induced by dual infections of Prunus necrotic ringspot and prune dwarf viruses. A transmissible disorder of apricots and a chlorosis of leaves of peach seedlings transmitted from symptomless plum and cherry trees are both described. DARK GREEN SUNKEN MOTILE OF PEACH Cropley (1968a) showed that a dark green mottle symptom was caused on peach (Prullus persica (L.) Batsch) seedlings by infection with apple chlorotic leaf spot virus. This virus has been reported also in sweet cherry (P. avium L.) (Gilmer 1967), European plum (P. domestica L.), Cropley 1968b), and apricot (P. armeniaca L.) (Marenaud 1968). mottle virus has been found infecting, without symptoms, almond (P. amygdalus Batsch) (1 cv.), apricot (~ cv.), sweet cherry (7 cv.), nectarine (P. persica var. nucipersica (Borkh.) C. K. Schneider (3 cv.), peach (9 cv.), European plum (2 cv.), and Japanese plum (P. salicin a Lind!.) (12 cv.). In bud transmission experiments dark green sunken mottle symptoms were expressed readily on seedlings of 'Golden Queen' and 'Elberta' peach. Symptoms were usually evident during November and December only, but could sometimes be seen in January. Affected leaves showed small (1 to 2 mm diameter), slightly sunken spots, often, but not always, circular, and a slightly darker green than the remainder of the leaf (Fig. 1). In some lights the spots had a rather greasy look, and were often more discernible if the leaf was held at an obtuse angle to the light. Size and number of the spots varied with the source of inoculum, suggesting that different strains of the virus might be involved. Inoculation of Chenopodium quinoa Willd. from infected Prullus hosts, using 2.5% nicotine, caused necrotic local lesions after 6 days followed by a systemic, chlorotic mottle. Usually only a few lesions occurred on C. quinoa with Prunus inoculum, but when systemic C. quinoa leaves were used as source of virus many lesions developed (Fig. 2). When Chenopodium amarallticolor Coste and Reyn. was inoculated with sap of infected C. quinoa, necrotic lesions were formed, followed by systemic chlorotic spotting with some yellow vein banding. Cucumis sativus L., Gomphrena globosa L., and Nicotiana tabacum L. cv. 'Samsun' were not infected Dark green sunken mottle virus has been found by mechanical inoculation. These symptoms of virus occurring naturally in stone fruit in New Zealand isolates from Prunus spp. on C. quinoa were similar (Fry & Wood 1969) and in Australia (Stubbs & to those produced by isolates of chlorotic leaf spot Smith 1971). In New Zealand, dark green sunken virus from Malus spp. Physical properties tested were N.Z. Journal of Agricultural Research 16:

3 132 N.Z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, 1973 similar also, the virus being unstable in C. quinoa extracts made with water. Infectivity was lost in Ie min at 50 c or 24 hr at room temperature. Although dark green mottle symptoms were induced by Cropley (1968a) in peach inoculated with apple chlorotic leafspot virus, Stubbs & Smith (1971) could not induce chlorotic leaf spot symptoms on apple with dark green sunken mottle virus from infectcd peach. This has been our experience also, but it may be attributable to the fact that peach buds do not survive in apple. We have found that most apple viruses require a permanent union for transmission to occur, whereas many Prullus viruses arc regularly transmitted by the budding technique, even when the inoculum bud dies. In our experiments we have budded apple cultivars containing various combinations of latent viruses into peach seedlings. The seven cultivars that transmitted dark green sunken mottle to peach were au infected with chlorotic leaf spot virus. After heat treatment which removed chlorotic leaf spot virus and all other latents, no dark green sunken mottle symptoms were transmitted to peach. No dark green sunken mottle occurred on peach after budding with four cultivars that were infected with stem grooving virus, or with one cultivar that was infected with flat limb and rubbery wood viruses. Similarly neither spy decline nor apple mosaic viruses could be associated with the production of dark green sunken mottle. In experiments with isolates of dark green sunken mottle, necrotic ringspot, and prune dwarf viruses, Stubbs & Smith (1971) found that rosette symptoms on peach could be induced by the combination of certain strains of dark green sunken mottle and necrotic rings pot viruses, or necrotic ringspot and prune dwarf viruses, the most severe rosette occurring with the three viruses together. In our experience dark green sunken mottle virus has had no influence on the incidence of rosette symptoms in peach. A necrotic ringspot plus prune dwarf virus mixture caused rosetting, but necrotic ringspot virus plus dark green sunken mottle virus did not, and dark green sunken mottle virus did not intensify the rosette symptom induced by the other virus mixture. When plums were indexed, 39 trees of 14 cuitivars were found infected with both necrotic ringspot and dark green sunken mottle, but none induced the rosetting symptom in peach seedlings. It is therefore highly probable that the HT-L isolate of dark green sunken mottle used by Stubbs & Smith is different from any of those with which we have worked. If the HT-L isolate is in fact the only pure isolate of dark green sunken mottle virus yet obtained, as suggested by Stubbs & Smith, the isolates Wi! have found in New Zealand stone fruit are strains of chlorotic leaf spot virus that cause dark green sunken mottle symptoms in peach. Fig. 1 - Dark green sunken mottle virus symptoms on leaf of 'Golden Queen' peach seedling (right) Healthy leaf on left. [Photo: A. P. Underhill NECROTIC RUSTY MOTTLE Necrotic rusty mottle was first described as a virus disease of cherry from Utah, U.s.A. (Richards & Reeves 1951), and has been recorded also in South

4 FRY AND WOOD: VIRUSES OF Prullus 133 Fig. 2 - Dark green sunken mottle virus symptoms on Chenopodium quinoa leaves inoculated from systemically infected C. quilloa. Necrotic local lesions (centre), systemic symptoms (left), uninoculated leaf (right). [Photo : 1. W. Endt Fig. 3 - Necrotic rusty mottle. Early summer symptoms on 'Lambert' cherry. Irregular ring pattern of green on yellow background (left), brown lesions (centre) and healthy leaf (right). [Photo: A. P. Underhill

5 134 N.z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, 1973 FIg. 4 - Necrotic rusty mottle. Midsummer symptoms on 'Lambert' "hcrry. Necrotic lesions and leaf-edge rolling of the severe strain on two leaves at left, and scattered lesions of the mild strain on two leaves at right. [Photo: A. P. Ullderhill Australia (Crowley et al. 1962) and England (Posnette & Cropley 1964). In New Zealand the virus has been found infecting three cherry trees only, each in a different orchard of Central Otago. Infection of two 'Early Lyons' and one 'Werder's Early Black' was detected when the trees were indexed as part of a virus survey in this district (Wood & Fry 1972). No necrotic rusty mottle virus symptoms were seen on the three orchard trees. Symptoms on nursery plants of 'Lambert' cherry first appeared in early December on well-expanded leaves as purple brown lesions which enlarged to form irregular red-brown areas 0.5 to 1 em across. Later the areas became lighter brown, and some developed a zonate appearance with a darker brown border. Some leaves developing during December showed a mottling and an irregular ring pattern of green on a yellow background (Fig. 3) and were soon shed. Later-developing leaves did not show this symptom, but developed necrotic lesions similar to those on the first-formed leaves. When the edges of leaves developed necrosis, the dead tissue curled either upwards or downwards. Similar symptoms occurred on the cherry cultivars 'Sam', 'Williams Favourite', 'Van', and on 'Mazzard' seedling. No symptoms occurred on F12Jl, on 'Kanzan', 'Golden Queen' peach seedlings, 'Shiro' plum, or 'Italian' prune. Although several other cherry viruses were present in the infected trees, the symptoms of necrotic rusty mottle virus did not appear to be influenced by their presence. Differences in the severity of symptoms on the indicators suggest that two distinct strains of the virus were present (Fig. 4). By mid February the severe strain of the virus had caused complete defoliation, whereas only a few leaves had fajlen from plants inoculated with the other two isolates. These retained most of their leaves until the end of the season. After defoliation by the severe strain, tip dieback occurred and progressed until in some instances the whole shoot was dead. At this stage prolific growth appeared from the stock below the dead scion. These symptoms suggest that the New Zealand virus is more closely related to the necrotic rusty mottle described by Richards & Reeves (1951) than to Lambert mottle (Lott 1951) or rusty mottle (Reeves 1951). In the cherry orchard index (Wood & Fry 1972) seven 'Early Lyons' trees, each from a different orchard, were indexed. Only two of these trees were infected with necrotic rusty mottle virus, each containing an apparently distinct strain. One infected 'Werder's Early Black' out of four trees indexed contained a virus of similar severity to the mild strain from 'Early Lyons'. In ajl, 100 trees of various cultivars were tested and only the above three were found to be infected with necrotic rusty mottle virus. Thus it appears that the incidence of this virus is considerably less than that of the other cherry viruses found.

6 FRY ANI) WOOl); VIRUSES OF Prullus 135 Fig Strawberry latent ringspot virus. Chenopodium quinoa, showing chlorotic mottle and epinasty of young leaves. [Photo: A. P. Underhill STRAWBERRY LATENT RINGSPOT Strawberry latent ringspot virus was described by Lister (1964), who found it naturally infecting it number of plant species apparently without causing any symptoms. It is also symptomless in many of a wide range of herbaceous test plants that were experimentally infected. Exceptions were C. amaranticolor, C. quilloa, Cucumis sativus L., Phaseolus vulgaris L. cv. 'Prince', and Tetragonia expansa Murr. Although having many properties similar to those of arabis mosaic virus, it was found by Lister to be serologicall y unrelated. In New Zealand the virus has been isolated from a single 30-year-old 'Bing' sweet cherry tree which showed severe rasp leaf symptoms. However, any relationship between infection with this virus and the rasp leaf symptom is not known, as we have not yet returned the virus to cherry. Also, infection was found on only one of five 'Bing' trees showing "rasps" on their leaves. The virus was initially isolated by mechanical inoculation, using 2.5% nicotine, to C. quinoa, on which it caused stunting, epinasty of young leaves, and chlorotic mottle on intermediate leaves (Fig. 5). Inoculation from C. quinoa to C. amaranticolor caused greyish discolouration of the proximal halves of young leaves, accompanied by severe epinasty. Cucumber plants infected during summer remained symptomless, but others inoculated in winter developed necrotic lesions on cotyledons followed by a chlorotic mottle on the first true leaves (Fig. 6). Infected plants of G. globosa, Nicotiana glutinosa L., and N. tabacum cvs 'Samsun' and 'White Burley' remained symptomless. Infection of symptomless hosts was confirmed by back inoculation to C. quinoa. Thermal inactivation of strawberry latent ringspot virus occurred after 10 minutes' treatment at 56 c but not at 54 c (Lister 1964). The New Zealand virus infected one plant out of 14 inoculated after treatment at 55 c and was inactivated at 60 c. The

7 136 N.Z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, 1973 Fig. 6 - Strawberry latent ringspot virus. Systemic chlorotic mottle on cucumber seedling leaves. [PhoLO: A. P. Underhill virus was purified from cucumber extracts using the butanol/chloroform method of Harrison & Nixon (1960) and sucrose density gradient centrifugation. Seven days after inoculation the yellow-mottled first true leaves yielded only half the amount of virus per gram that was recovered from the inoculated cotyledons. In agar gel irnmuno-diffusion tests, purified virus reacted specifically to a strawberry latent ringspot antiserum supplied by Mr R. A. Goold of the Scottish Horticultural Research Institute. SoUR CHERRY YELLOWS Sour cherry yellows was recognised as a disease in New York State in 1919, and its virus nature was demonstrated by Keitt & Clayton in Yellows symptoms occur on sour cherry (Prunus cerasus L.) doubly infected with certain strains of prune dwarf and necrotic ringspot viruses (Cropley et al. 1964). For several years we have attempted unsuccessfully to induce sour cherry yellows symptoms in 'Montmorency' sour cherry by inoculation with naturally occurring mixtures of prune dwarf and necrotic ringspot viruses (Fry & Wood 1971). Because several different isolates of virus mixtures had been used it seemed unlikely that none of these would produce sour cherry yellows. Thus it appeared that either climatic conditions in Auckland were unsuitable or the strain of 'Montmorency' used would not exhibit symptoms (Gardner 1943). To differentiate between these two possibilities a strain of 'Montmorency' known to develop symptoms was obtained from Professor G. Nyland, University of California, Davis. Symptoms typical of sour cherry yellows developed on this strain of ' Montmorency' inoculated with each of three prune dwarf and necrotic ringspot virus mixtures, two from cherry and one from peach. No symptoms had developed during the spring, but by mid January bright yellow areas (Fig. 7) had appeared on leaves near the base or at midheight of the maiden shoot. Shortly after the yellowing had fully developed, the affected leaves fell, all being shed by mid March. No yellowing developed on uninoculated 'Montmorency' shoots or on those inoculated with necrotic ringspot virus alone. No isolate of prune dwarf was available to test the effect of this virus alone. These results show that the strain of 'Montmorency' used previously was one that would not react to infection with prune dwarf and necrotic ringspot viruses by the development of sour cherry yellows symptoms. A TRANSMISSIBLE DISORDER OF APRICOTS In 1964 a single 60-year-old tree of 'Moorpark' apricot with severely distorted fruit (Fig. 8) was observed in a Central Otago orchard. Stones of

8 FRY AND WOOD: VIRUSES OF Prunus 137 FIg. 7 - Sour cherry yellows. Midsummer symptoms on two 'Montmorency' leaves at left. Healthy leaf on right. [Photo : I. W. Endl affected fruit had developed irregularly shaped holes through the endocarp (Fig. 9). Some leaves on the tree had chlorotic markings associated with fine veins and interveinal rings pots (Fig. 10). According to the grower the affected tree was normal until the previous season, when the fruit distortion first became apparent. A transmission trial was carried out using 'Golden Queen' peach seedlings as understock and inserting virus-free 'Moorpark' buds above buds from the affected tree. In the season following budding both the indicator shoot and the shoot from the infecting bud were stunted, and leaves developed chlorotic markings, some of which took the form of ringspots. By the following season all affected apricot shoots were dead. Leaves on the peach stock shoots were smaller than normal, sometimes twisted with wavy edges, and developed bright yellow spots, rings, and wavy line patterns (Fig. 11 ). When herbaceous indicator plants were inoculated by leaf rubbing, using 2.5% nicotine, no symptoms developed on inoculated plants of Chenopodium amaranticoior, Cucumis sarivus, Cucurbita pepo L. 'Buttercup', G. giobosa, N. giutinosa, N. tabacum cv. 'Samsun' and 'White Burley', and Vida laba L. Leaves of inoculated C. quinoa developed local lesions typical of those induced by dark green sunken mottle. Because dark green sunken mottle has been Fig. 8 - Transmissible disorder of apricot. Distorted fruit of 'Moorpark' apricot. Healthy fruit on left. [Phoro: I. W. El1dt

9 138 N.Z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, 1973 Fig. 9 - Transmissible disorder of apricot. Stones of affected 'Moorpark' fruit showing holes in the endocarp. [Photo: J. W. Emit Fig Transmissible disorder of apricot. Chlorotic markings and rings on 'Moorpark' leaves. [Photo: J. W. Elldt

10 FRY AND WOOD: VIRUSES OF PrUllUS 139 Fig Transmissible disorder of apricot. Peach seedling leaves showing twisting, distortion, and yellow line patterns after inoculation from affected 'Moorpark' apricot. [Photo: A. P. Ullderhill

11 140 N.Z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, 1973 Fig Peach seedling chlorosis on 'Golden Queen' peach seedling leaves. [Photo: I. W. Endt recovered from apricots which did not show distorted fruit, its presence in this experiment is thought to have no connection with the unusual 'Moorpark' symptoms. PEACH SEEDLING CHLOROSIS During the last few years, when plum and cherry trees have been indexed, using 'Golden Queen' peach seedlings as rootstock, a hitherto undescribed symp- tom has appeared on leaves of stock shoots. Most leaves produced by late spring developed chlorotic zones occupying from one-eight to one-half of the area of cach leaf (Fig. 12). No symptoms occurred on leaves produced during the summer, but they reappeared on leaves produced in the second season's spring growth. Neither plum and cherry trees used as sources of inoculum nor growth made from the inoculum buds showed any symptoms other than those attributable to known virus diseases.

12 FRY AND WOOD: VIRUSES OF Prunus 141 In the nursery row, three adjacent seedling ~tock plants were inoculated with single buds taken from different budsticks of each tree being indexed. One, two, or three of the stock plants budded from each infected plum or cherry tree developed the chlorotic symptom. Statistical analysis* of a trial in which 100 plum trees were indexed showed that the symptom was not randomly distributed among stock plants as would be expected if it was caused by a heritable character or mutation in the seedling stocks. Because all buds from infected trees did not induce the chlorotic symptom, it appears that distribution of infection is not fully systemic in the source trees; so it is likely that the use of only three buds was not adequate to detect infection in all infected trees. Some of the trees that did not transmit symptoms were therefore probably infected. Forty-one of 100 plum trees in 19 cultivars and 14 of 107 cherry trees in 26 cultivars were found to be infected. In 9 of the infected plums no known viruses were found, but in the remaining 32, mixtures occurred of necrotic rings pot, dark green sunken mottle, and plum mosaic viruses in various combinations. Fifty of the plums that did not transmit the chlorotic symptom were infected with these three viruses alone, or in combination. In the cherries, mixed infections only were found. Infection appears to be confined to plum and cherry cultivars, because no chlorotic symptoms have yet been observed on peach seedlings budded from many apricot, nectarine, and peach trees of several cultivars. Thus it appears that the chlorotic symptom on peach seedlings is caused by an infectious entity unrelated to any of the recorded stone fruit viruses. The nature of the infectious entity is similar to that of diseases generally accepted as fruit tree viruses, but, as with many of these, the available data are not adequate to prove the virus nature conclusively. It is suggested that a suitable name for this disorder, pending further characterisation, would be "peach seedling chlorosis". Acknowledgments Mr R. A. Goold for the strawberry latent ringspot virus antiserum; Mr F. M. Mitchell for virus purification and serological studies; Miss Alison Marshall for statistical analysis; Prof. G. Nyland for 'Montmorency' scion wood. REFERENCES Atkinson. 1. D. 1971: Cherry rasp leaf: In "Diseases of Tree Fruits". N.Z. Department of Scientific and Industrial Research Information Series 81: 28(}-2. * Goodness of fit test for binomial distribution x2 = 39.5 dj. = 2 significant at 1 % level. Chamberlain, E. E.; Atkinson, J. D.; Hunter, J. A. 1951: Plum mosaic, a virus disease of plums. peaches, and apricots in New Zealand. N.Z. Journal of Science and Technology 33A: : Moorpark mottle: a virus disease of apricots in New Zealand. Ibid. 35A: : Occurrence of peach calico in New Zealand. Ibid. 38A: : Two diseases of plum causing distortion and internal necrosis of fruits. 1. Plum fruit crinkle, a virus disease resembling plum pox of Europe. N.Z. Journal of Agricultural Rcsearch 2: Chamberlain, E. E.; Atkinson, J. D.; Wood, G. A.: Hunter, J. A. 1971: Occurrence of cherry green ring mottle virus in New Zealand. Ibid. 14: Cropley, R. 1968a: Comparison of some apple latent viruses. Annals of Applied Biology 61: b: The identification of plum pox (sharka) virus in England. Plant Pathology 17: Cropley, R.; Gilmer, R. M.; Posnette, A. F. 1964: Necrotic ring spot and prune dwarf viruses in Prunus and in herbaceous indicators. A llnals of Applied Biology 53: Crowley, N. c.; Moller, W. J.; Steed, J. N. 1962: Virus diseases of cherries in South Australia. Journal of Agriculture, South Australia 65: 53:!-7. Fry, P. R.; Wood, G. A. 1969: Peach rosette, a virus in New Zealand stone fruit. The Orchardist of New Zealand 42: : Little cherry virus in New Zealand. N.Z. Journal of Agricultural Research 13: 111-S. 1971: Prullus necrotic ringspot and prune dwarf viruses in New Zealand. Ibid. 14: Gardner, V. R. 1943: Studies in the nature of the clonal variety: III. Permanence of strain and other differences in the 'Montmorency' cherry. Michigan Agricultural Experiment Statioll Technical Bulletin 186. Gilmer, R. M. 1967: Apple chlorotic leaf spot and tobacco mosaic viruses in cherry. Plant Disease Reporter 51: Harrison, B. D.; Nixon, H. L. 1960: Purification and electron microscopy of three soil-borne plant viruses. Virology 12: Keitt, O. W.; Clayton, C. N. 1939: A destructive bud-transmissible disease of sour cherry in Wisconsin. Phytopathology 29: Lister, R. M. 1964: Strawberry latent ringspot: A new nematode-borne virus. Annals of Applied Biology 54: Lott, T. B. 1951: Lambert mottle. bl "Virus Diseases and other Disorders with Virus-1ike Symptoms of Stone Fruits in North America". U.S. Department of Agriculture Handbook 10: 123.

13 42 N.Z. JOURNAL OF AGRICULTURAL RESEARCH, VOL. 16, arenaud, C. 1968: Mise en evidence. sur l' espece abricotier, d'nne incompatibilite intraspecifique due a la presence d'un virus du type chlorotic leaf spot. Annals des Epiphyties 19, No hors Stir. Etudes de Virologie: )osnette, A. F.; Cropley, R. 1964: Necrotic rusty mottle virus disease of sweet cherries in Britain. Plant Pathology 13: Reeves. E. L. 1951: Rusty mottle. 111 "Virus Diseases and other Disorders with Virus-like Symptoms of Stone Fruits in North America". U.S. Department of Agriculture Handbook 10: Richards, B. L.; Reeves, E. L. 1951: Necrotic rusty mottle. Ibid Stubbs, L. L.; Smith, P. R. 1971: The association of PrLlllllS necrotic ringspot, prune dwarf, and dark green sunken mottle viruses in the rosetting and decline disease of peach. Australian }oumal of AgriCllllural Research 22: Wood, G. A. 1972: Cherry rusty spot virus. N.Z. }ollrnal of Agricultural Research 15: Wood, G. A.; Fry, P. R. 1972: Virus infection in Central Otago sweet cherry trees. I bid. 15: