Nematol. medit. (1978), 6: 1·27. I stituto di Patologia vegetale, Universita degli Studi 70126 Bari, Italy NEMATODE-BORNE VIRUSES OF GRAPEVINE, THEIR EPIDEMIOLOGY AND CONTROL (1) by GIOVANNI P. MARTELLI INTRODUCTION The discovery of a nematode vector for the fanleaf disease of grapevine (Hewitt et al., 1958) together with the demonstration that the viral agent was mechanically transmissible to herbaceous hosts (Cadman et aI., 1960) greatly stimulated investigations on viruses of cultivated Vi tis. Consequently, in little less than two decades many different viruses have been manually transmitted from diseased vines in several grape-growing countries. By 1976 there were 24 viruses recorded from grapevine (Martelli, 1978) half of which are either recognized or putative members of the nepovirus group (Table I). At present, nepoviruses are the only nematode-borne pathogens known to infect grapevine in which they may cause destructive diseases. Although occurring in the major viticultural areas of the world, not all the viruses are equally widespread. Thus, with the exception of grapevine fanleaf virus (GFV) which is ubiquitous (Hewitt, 1968) and uniquely specialized for having no natural host other than grapevine, other viruses like arabis mosaic (AMV), tomato black (1) The present review is largely based on an invitation paper given at the Conference on «Plant Disease Epidemiology and Dispersal of Plant Para­ sites », London, 14-18 December, 1977. Grateful thanks are espressed to Drs. T. J. W. Alphey, H. F. Dias, R. I. B. Francki, F. Lamberti, A. F. Murant, D. C. Ramsdell, M. Rudel and J. K. Uyemoto for kindly providing unpublished data or manuscripts prior to publication. I am also much endebted to Dr. C. E. Taylor for reviewing the manuscript at a very short notice and for making many helpful suggestions. -1- ring (TBRV), raspberry ringspot (RRV), strawberry latent ringspot (SLRV), grapevine chrome mosaic (GCMV), and artichoke Italian latent (AILV) are restricted to European countries (Table I). These will be referred to as European nepoviruses as opposed to American nepoviruses, i.e. tomato ringspot (TomRSV) tobacco rings pot (TRSV) and peach rosette mosaic (PRSV) which seem confined largely to North America. Besides GFV, grapevine Bulgarian latent (GBLV) is the only grapevine nepovirus recorded, so far, in both Europe and North America. Various aspects of the biology and ecology of nematode-transmit­ ted viruses have been reviewed in recent times in articles which also contain much information on those infecting grapevine (Murant, 1970; Taylor, 1971, 1972; Vuittenez et al., 1972; Weischer, 1973, 1975; Taylor and Robertson, 1975; Harrison, 1977; Lamberti, 1978). THE DISEASES Symptomatology Most European nepoviruses induce diseases which are charac­ terized by a large and rather confusing array of symptoms. Field syndromes are often the same whether caused by anyone virus or by an association of different viruses, so that it is virtually impossible to distinguish disorders evoked by specific entities on the basis of symptomatology alone. Variability in symptom expression depends on the host (Vitis species or cultivar) and, to a greater extent, on the virus strain. In fact, severa) nepoviruses e.g. GFV (Hewitt et al., 1962), GCMV (Martelli et al., 1965), AMV (Stellmach, 1970a) and TomRSV (Gooding and Hewitt, 1962; Gilmer and Uyemoto, 1972) possess «distorting» and «yellow}} strains or isolates which mayor, more commonly, may not be serologically distinguishable but are liable to induce strikingly different syndromes. Thus for example, « distorting}} strains are associated with malformations of leaves and canes sometimes accompanied by chlorotic mottles, whereas «yellow}} strains induce bright chrome-yellow discolourations of the foliage without much deformation. Reduced vigour and low yield may be associated with infection by either type of strains. -2- Among American nepoviruses, TRSV and TomRSV cause serious decline of Vitis vinifera L. cultivars and their hybrids, whereas PRMV is a major pathogen of Vitis labrusca. In all cases symptoms consist largely of delayed spring growth, mottling, malformation and rolling of the leaves, severe stunting and poor fruit set. Ultimately, affected vines may die (Gilmer et al., 1970; Ramsdell and Myers, 1974; Uye­ moto, 1975; Dias and Cation, 1976; Dias, 1977a). However, the serologically distinct yellow vein strain of TomRSV, the causal agent of grapevine decline in Northern U.S.A. and Canada, seriously affects the yield of Californian grape cultivars without hampering the growth of diseased plants which, surprisingly, appear more vigorous than healthy ones (Gooding and Hewitt, 1962). Whether or not symptoms like leaf enations and wood pitting may be associated with infection by nepoviruses is still controversial. As discussed in previous reviews (Hewitt, 1968, 1973; Martelli, 1975b; Goheen, 1977), both types of symptoms rather than characterizing specific diseases may represent host responses to more than one viral pathogen. It should be borne in mind, however, that GFV very often has been found associated with enations in Europe and California (Hewitt, 1968; Graniti and Martelli, 1970a), whereas GFV, TomRSV and TRSV have been recovered from stem-pitted vines in several countries (Hewitt et al., 1970; Graniti and Martelli, 1970b; Uyemoto, 1975). Interestingly, field spread of stem pitting is associated with the presence of Xiphinema index in Southern Italy (Graniti and Mar­ telli, 1970b) and France (Boubals, 1976a). Economic importance Nepoviruses are detrimental to the grape industry in many ways. They may cause: a) progressive decline and death of the vines; b) low quantity and quality of yield; c) shortening of the productive life of the vineyard; d) low proportion of graft take; e) reduced rooting ability of propagating material; f) decreased resistance to adverse climatic conditions (for details see: Brlickbauer, 1962; Hewitt, 1968; Stellmach, 1970b; Gilmer et al., 1970; Ramsdell and Myers, 1978). Information on crop losses due to nepoviruses is fragmentary for no systematic assessment has been carried out in any country on a sufficiently large scale. Besides, most of the available data for European nepoviruses refer only to GFV and its strains. Thus, -3 Table I - Nematode-borne viruses of grapevine, their vectors and geographical distribution. References Vir u s Vector Geographical distribution First First Sap - transmission Nematode transmission A) Recognized nepoviruses 1. Grapevine fanleaf Distorting strains x. index Worldwide Cadman et al., 1960 Hewitt et al., 1958 X. italiae Cohn et al., 1970 Yellow mosaic strain X. index Worldwide Cadman et al., 1960 Hewitt et ai., 1962 Vein banding strain X. index Worldwide Hewitt et al., 1962 Alfaro and Goheen, 1974 2. Arabis mosaic Type strain X. diversicaudatum France, Germany, Bercks and Stellmach, Vuittenez et al., 1976 Hungary 1966 3. Tomato blackring English strain L. attenuatus Germany Stellmach and Bercks, Rudel, 1977 1963 4. Raspberry rings pot Bercks' isolate unknown Germany Bercks, 1968 Palatinate strain unknown Germany Vuittenez et al., 1970 5. Strawberry latent ring­ spot Type strain unknown Germany Vuittenez et al., 1970 6. Grapevine chrome mo- saic unknown Hungary Martelli et al., 1965 7. Artichoke Italian la- tent unknown Bulgaria Jankulova et al., 1978 8. Peach rosette mosaic X. americanum U.SA. (Michigan), Dias, 1968 Dias, 1975 Canada 9. Tomato ringspot Yellow vein strain x. americanum U.S.A. (California) Gooding and Hewitt, Teliz et al., 1966 Type strain unknown U.S.A. (New York) 1962 Canada, Yugoslavia (?) Gilmer and Uyemoto, 1972 10. Tobacco ringspot unknown U.S.A. (New York) Gilmer et al., 1970 B) Possible nepoviruses 11. Grapevine Bulgarian latent Type strain unknown Bulgaria Martelli et al., 1977 New York strain unknown U.S.A. (New York) Uyemoto et al., 1977 12. Grapevine CM-112 * unknown Portugal Ferreira and De Sequeira, 1972 * Recent findings indicate that this virus is serologically related to Grapevine Bulgarian latent virus (R. Hull, per­ sonal communication) Vuittenez (1970) reckons that a 50% reduction in weight is the average crop loss caused by GFV to susceptible V. vinifera cultivars in European countries. Such losses are aggravated by the poor quality of clusters which are often unmarketable [see also review by Bovey, (1970) and recent reports by Legin (1972) and Prota and Garau (1978)]. Some American nepoviruses are even more destructive to cultivars and interspecific hybrids of V. vinifera, possibly because of the greater susceptibility of these hosts. For instance, Californian vines infected by the yellow vein strain of TomRSV are reported to be virtually unfruitful (Gooding and Hewitt, 1962), and in Canada, Dias (1977a) has recently recorded crop losses ranging from 76 to 95% in a French hybrid infected by the type strain of TomRSV. THE VIRUSES Nepoviruses have isodiametric particles about 30 nm in diameter which sediment as several components when centrifuged, and possess two species of functional RNA, each contained in a specific particle. As a group, these viruses have been extensively reviewed (Martelli, 1975b; Harrison and Murant, 1977; Francki and Hatta, 1977). Recent studies have established that: (i) GCMV, GFV and PRMV have properties typical of members of the nepovirus group (Martelli and Quacquarelli, 1972; Martelli et al., 1977; Quacquarelli et al., 1976, 1978; H. F. Dias, personal communication); (ii) GFV isolates, whatever their geographical origin, have similar physico-chemical properties