Specificity of Retention and Transmission of Viruses by Nematodes 1
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SELECTED INVITATIONAL PAPERS PRESENTED IN THE NEMATOLOGY SECTION AT THE 2nd INTERNATIONAL CONGRESS OF PHYTOPATHOLOGY, MINNEAPOLIS, MINNESOTA, U.S.A., 5-12 SEPTEMBER 1973 Specificity of Retention and Transmission of Viruses by Nematodes 1 B. D. HARRISON, W. M. ROBERTSON and C. E. TAYLOR 2 A central problem for anyone concerned grapevine fanleaf virus (2), which with the transmission of viruses by vectors is serologically is distantly related to arabis to understand how it is that a given vector can mosaic virus. In Trichodorus, vector transmit one virus but not another, and that a specificity seems somewhat less well- given virus can be transmitted by one species developed than in Xiphinema or Longidorus. of vector though not by another species that For example, van Hoof (34) showed that may be closely allied to it taxonomically. With several species of Trichodorus transmit a few exceptions, there is still little indication tobacco rattle virus in the Netherlands. But of what features underlie this specificity specificity exists nevertheless, because T. between virus and vector, although there is anemones Loof will transmit a British, but not enough information to suggest that the a Dutch, strain of pea early-browing virus (4). mechanism is probably not the same in all Also, van Hoof (34) reported that instances. Trichodorus pachydermus Seinhorst As with other vectors, so also with transmitted only one of the five Dutch isolates nematode vectors there is evidence of of tobacco rattle virus that were tested. specificity between virus and vector. Thus, Transmission of a virus by a nematode two major groups of nematode-borne viruses involves a sequence of processes: uptake of the have been described, and two corresponding virus particles from plants, survival of groups of vectors. The nepoviruses (8) have infective particles in the nematode, their small isometric particles (Fig. 1) and are inoculation by the nematode to other plant transmitted by nematodes in the genera ceils, and infection of the receptor plants by Xiphinerna Cobb and Longidorus the virus. The probability of transmission is (Micoletzky) Thorne and Swanger, which are the product of the probabilities that each of both in the superfamily Dorylaimoidea. By these processes is successfully completed. contrast, the tobraviruses (8) (previously Failure to complete any one of the processes known as netuviruses) have straight tubular will cause failure to transmit. In discussing particles (Fig. 2) and are transmitted by vector specificity, we will therefore consider species of Trichodorus Cobb, which are in the transmission, stage-by-stage. superfamily Diphtherophoroidea. With the exception of tobacco ringspot virus (17, 31), Uptake of virus from plants: S~nger et al. none of these nematode-transmitted viruses is (20) were the first to show that a plant virus known to have vectors in other phyla. could be directly detected in a nematode. They In each nematode genus there is further cut open Trichodorus nematodes that had evidence of vector specificity. For example, been allowed to feed on plants infected with Longidorus elongatus (de Man) Thorne & tobacco rattle virus, and showed that some of Swanger transmits two nepoviruses, the extracts obtained in this way produced a raspberry ringspot virus (21) and tomato few lesions when inoculated to suitable hosts black ring virus (9), but does not transmit a of the virus. Although we now think that the third, arabis mosaic virus (22). Xiphinema virus particles detected by this method came diversicaudatum (Micoletzky) Thorne from the nematodes' intestines and have transmits arabis mosaic virus (7, 14), but not nothing to do with transmission, such tests provide a convenient check of whether nematodes have taken up a virus from plants. Received for publication 30 November 1973. Using this method, van Hoof (33) detected ~Symposiumpaper presented at the 2nd International Congress of tobacco rattle virus in Xiphinema Plant Pathology, Minneapolis, Minnesota, USA, 5-12 diversicaudatum, a nonvector, and Taylor September 1973. ~Scottish Horticultural Research Institute, Invergowrie, Dundee, (22) found that Longidorus elongatus U.K. acquires, not only the two viruses that it 155 156 J~mrnal st~"Nematology, Volume 6, No. 4, October 1974 transmits (raspberry ringspot and tomato Sites in nematodes where virus particles are black ring), but also two viruses that it does retained: Taylor and Robertson (26, 27, 28) not transmit, arabis mosaic and strawberry found, by means of electron microscopy of latent ringspot. In these instances at least, thin-sections of virus-carrying nematodes, failure to transmit does not reflect a failure to that virus-like particles become associated ingest the virus particles. with the cuticular lining of the buccal capsule Longidorus Xiphinema Trichodorus 3 Fig. I-3. I and 2. Electron micrographs of purified virus preparations mounted in 1% sodium phosphotungstate (Courtesy I. M. Roberts). 1) Particles ofarabis mosaic virus. 2) Particles of tobacco rattle virus. 3) Diagram of anterior port ion of vector nematodes. Broken lines indicate portions of the alimentary tracts where virus particles are retained. 4 °. "~z ~,_n'~¸, ,at 7 Fig. 4-7. 4) Transverse section of buccal region of Longidorus elongatus carrying raspberry ringspot virus. Note virusqike particles (V) between odontostyle (O) and guide sheath (G). 5) Longitudinal section of buccal region of L. elongatus carrying raspberry ringspot virus. Note numerous virus-like particles (V) lining guide sheath (G), and that none is a~sociated with stoma cuticle (C). 6) Oblique longitudinal section through odontophore and odontostyle of Xiphinema diversicaudatum carrying arabis mosaic virus. Many virus particles (V) are attached to wall of odontophore (P) lumen but not to structurally different odontostyle (O). 7) Longitudinal section of odontophore of X. diversicaudatum carrying arabis mosaic virus. Virus particles (V) are seen where esophageal lumen (L) is cut tangentially. Odontophore sinuses (S) lie parallel to lumen. 158 Journal of Nematology, Volume 6, No. 4, October 1974 or of the esophagus. They studied Longidorus lining of the stoma. No particles were found elongatus carrying raspberry ringspot virus, either within the odontophore lumen or lining L. eiongatus carrying tomato black ring virus, any other part of the esophagus, or in any part Xiphinema diversicaudatum carrying arabis of virus-free L. elongatus. In L. elongatus mosaic virus, X. index Thorne and Allen carrying tomato black ring virus, the carrying grapevine fanleaf virus, and distribution of particles was similar to that Trichodorus pachydermus carrying tobacco found with raspberry ringspot virus. rattle virus. McGuire et al. (16) have made The general morphology of the feeding similar observations on X. americanum Cobb apparatus of Xiphinema is similar to that of carrying tobacco ringspot virus, and Raski et Longidorus, but the guide sheath continues al. (19) have confirmed the behavior of strains anteriorly beyond the guide ring, as a reflexed of grapevine fanleaf virus in X. index. Taylor collar. Also, the posterior end of the and Robertson (26) proposed that, in vector odontophore has triradiate flanges (Fig. 3). nematodes, the virus particles become Figure 6 is an oblique longitudinal section of specifically associated with these surfaces, Xiphinema diversicaudatum, carrying the from which they later dissociate and are type strain of arabis mosaic virus, at the injected into plant cells along with the junction of odontophore and odontostyle. nematodes' saliva. Transmission therefore Note that many particles line the lumen of the seems not to involve multiplication of the odontophore, and that none lines the lumen of virus in the nematode or passage through its the odontostyle. The second view (Fig. 7) is gut wall or coelom. Indeed, plant virus more longitudinal, and shows many particles particles have never been found inside in close-packed arrays where the lumen is cut nematode cells. tangentially. These virus-like particles were The sites of retention found by Taylor and also found in other parts of the esophagus Robertson (26) differ somewhat from one including the lumen of the esophageal bulb; nematode genus to another. First, we will they were most numerous at the anterior ends consider the main features of the structure of of odontophore and esophageal bulb. the mouthparts and esophagus of nematodes Particles were not found lining the stoma, in each genus (Fig. 3), and then we will guide sheath or odontostyle, nor in any part of examine sections in which virus-like particles virus-free X. diversicaudatum. The readily can be discerned. In Longidorus distribution of particles was the same in X. elongatus, the long spear is in two parts. The diversicaudatum carrying the hop strain of anterior part, or odontostyle, is cast with the arabis mosaic virus, in X. index carrying outer cuticle of the nematode at each of the grapevine fanleaf virus, and also, as shown by four molts. The rear part, or odontophore, McGuire et al. (16), in X. americanum apparently is not cast but is rebuilt at molting carrying tobacco ringspot virus. (Taylor and Robertson, unpublished), and is In the genus Trichodorus, the stylet is a attached to the tubular part of the esophagus, tooth-like structure (Fig. 3), and the food which ends in a muscular bulb. At the rear end passes down the pharyngeal lumen, in which of this bulb is a nonreturn valve, the the stylet is housed, into the esophagus. In T. esophago-intestinai valve, which prevents pachydermus carrying tobacco rattle virus, material from being regurgitated from the the virus particles are associated with the intestine (30). The esophageal glands are pharyngeal wall throughout its length, but not situated in the esophageal bulb, and their with the stylet (Fig. 3 and 8). They also line the secretions pass into and move forward in the lumen of the esophagus, where the lumen of the esophagus. The stylet is characteristic long and short particles of the surrounded by a guide sheath, which forms virus can be seen clearly (Fig.