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METHODS AND CRITERIA FOR ASSESSING THE TRANSMISSION OF PLANTVIRUSES BY LONGIDORID ’S

David L. TRUDGILL*, Derek J.F. BROWN* andDavid G. “NAMARA** * Scottish Crop Research Institute, Invergowrie, Dundee, Scotland and ** East Malling Research Station, Maidstone, Kent, England.

Since Hewitt,Raski and Goheen (1958) first & Cadman, 1959). Similarlytransmission of rasp- showed that indexis a vector of grapevine berryringspot English strain (HRV-E ; fanleaf virus more than forty plant viruslnematode specific field vector rnacrosorna; Harrison, vectorcombinations have been reported. Many of 1962 ; Debrot,1964) has been reported for seven these reports have not been confirmed, but among species of longidoridnematodes (Tab. 1). If al1 thosethat have beensubstantiated a pattern of these reports of transmission are true then it would specificity between the and their longidorid seem that nematode species other than those with nematodevectors isapparent. Harrison, Mowat whichthese viruses are specificallyassociated with andTaylor (1961) observed thatthe degree. of in thefield can also act as vectors. In this conneciion, similaritybetween the different viruses seemed to Taylorand Robertson (1969)found unattached parallel the degree of systematic relationship between particles of AMV in the buccal capsuleof L. eloizqatus theirnematode vectors. This relatedness of speci- which suggested that some transmission may &,ult ficity maybe partly due to virus particles with from non-specific retention of virus. particular protein coat properties (Harrison, 1964 ; McNamara(1978) offered anotherexplanation Harrison et al., 1974)becoming attachedto the for apparent non-specific transmissions. He suggested lining of the feeding apparatusat specific sites that,inlaboratory experiments, contamination withintheir vectors. These are the inner surface of the outside of bait plant systems may Occur of the odontophore and oesophagus in vector species either from virus coming from bodies of of Xiphinerna (Taylor & Robertson, 1970 ; McGuire, entangled in, or in nematode faeces adhering to the Kim & Douthit, 1970 ; Raslri,Maggenti & Jones, outside of, the . He reached these conclusions 1973) and the inner surface of the odontostyle and afterattempting tosubstantiate the claim by between the odontostyleand the guiding sheath Valdez (1972) that RRV-E could be transmitted by in Longidorus spp.(Taylor & Robertson,1969 X. diversicaudatum. McNamara(1978) found that, & 1973 ; Taylor, Robertson & Roca, 1976). Further although he could recover this virus from the roots evidence for the “narrowness” of specificity between of bait plants exposed to X. diversicaudatum, none virusesand their nematode vectors is providedin of theseplants was systemically infected, al1 the severalreports of nematodepopulations differing RRV-Edetected apparently coming from external in their ability to transmit isolates of a virus (Dal- contamination of the roots.In contrast, when he masso,Munck-Cardin & Legin,1972 ; VanHoof, used L. macrosomu, the natural vector of RRV-E, 1966 ; Brown & Taylor, 1981). In contrast to the manybait plants eventually became systemically above,the results of somelaboratory experiments infected. McNamara (1978) concluded that evidence haveindicated nematode transmission of viruses fornematode transmission “can only be fully ac- contrary to the pattern of specificityproposed by ceptable if virus is translocatedfrom the roots of Harrison(1964). For example, six species of longi- thebait plant after transmission and is doridnematode have been reported as vectors of shown to be present in the , hypocotyl, or in (AMV ; specific field vector X. otherregions to whichnematodes have not had diversicaudatum ; Jha & Posnette, 1959 ; Harrison direct access”.

Revue Némalol. 6 (1) : 133-141 (1983) 133 D.L. Trudgill, D.J.F. Brown & D.G. McNamara

Table 1 Longidorus, and Xiphinema species reported as vectors for arabis mosaic virus (AMV) and the English strain of raspberry ringspot virus (RRV-E)

V irus Field Virus vector vectors Other

AMV X. diversicaudatum A'. coxi (Fritzsche, 1964) X. bakeri (Iwaki & Komuro, 1974) X. index (Fritzsche & Thiele, 1979) L. caespiticola (Valdez, 1972) P. maximus ' (McElroy et al. 1976) RRV-E L. macrosoma L. elongatus (Taylor & Murant, 1960) L. profundorum (Fritzsche & Kegler, 1968) L. caespiticola (Valdez,1972) L. leptocephalus (Valdez, 1972) X. diversicaudatum (Fritsche & Kegler, 1968) P. maximus (McElroy et al. 1976)

More than two-thirds of the reports of longidorid 1) Thevirus and nematode must be fully and nematodestransmitting virus fail to satisfy this correctly identified. requirement. Ako, many of thesereports give 2) Bait plant tissues must be shown to be infected inadequatedescriptions of themethods used or with the virus under test. describetests that didnot have adequate controls 3) Thenematode under test must be shown to or in which thenematode and/or virus used were be the only possible vector in that experiment. not adequately identified. In this paperwe consider the criteria bywhich the In the followingsection each of thesecriteria is results of a virus transmission test with longidorid considered in more detail. nematodesshould be judged and describe atest procedurewhich, modified wherenecessary to suit the nematode/virus combination being t*ested, should IDENTIFICATIONOF THE VIRUS AND THE NEMATODE give results which satisfy those criteria. Our experi- ence has been limited to European species of virus Onlyone nematode species shouldbe tested at vector nematodes but we believe that the procedure any one time, unless controls with other nematodes wedescribe can also give information about the are required. The virus to be transmitted should be emciency withwhich a virus is transmitted and, characterised by serology and,where possible, its withinthe limits of thenumbers of nematodes relationship wit.h other viruses be established. Any tested, useful evidence of the inabilityof a nematode virustransmitted must beidentified serologically to transmit a virus. and,where appropriate, shown to be serologically identical to that in the source plant. The nematodes testedshould be from one population and, except wherethey are from naturally infected field soil, shown to be initially virus-free by bait-testing with Thecriteria €or evaluatingthe results, of appropriate contra1 plants. Details of the source of transmission tests nematodesshould be given, as it isknown that populations of a species may differ in their ability totransmit strains of a virus,and those trans- Todemonstrate that aparticular virus is trans- mittingvirus must beidentified andpermanent mittedby agiven species of longidoridnematode mountskept. Where necessary they should be weconsider thatthe following criteriamust be comparedwith paratypes or similar specimens and satisfied : any deviations from these noted.

134 Revue Nimatol. 6 (1) : 133-141 (1983) Assessing transmission of plant viruses

EVIDENCETHAT THE BAIT PLANT IS INFECTED WITH exposed to viruliferous X. americanum S. la€. (l) and VIRUS found thatin those plant species to whichvirus was transmittedthe frequency of infectionvaried This evidence is best provided by demonstrating greatly.Similarly Trudgill and Brown (1979) and thatthe bait plant is systemically infected: This Trudgill,Brown and Robertson (1981) foundthat is mostreadily accomplished by recovering virus L. macrosoma transmittedRRV-E to Petunia from thehypocotyl or aerialparts but, in some hybrida and Fragariaananassa but not to Cheno- instances, production of symptoms may sufice. podiumquinoa whereas X. index couldacquire If testing of the root system is unavoidable, infection grapevine fanleaf virus from, but not transmit it to must be unequivocallydemonstrated. In al1 tests Gomphrena globosa. infection of either tlle bait or assay plants due to contamination or byalternative vectors must be excluded. UNSUITABLEVIRUS ISOLATE OR STRAIN

THENEMATODE MUST BE SHOWN TO BE THE VECTOR Differences in ability to transmit virus have been shown to occur within a nematode species, different In preliminarytests inhibition of transmission populationstransmitting different isolates of the bynematicides or byair-drying the soil may be samevirus (Van Hoof, 1966 ; Dalmasso,Munck- used to indicate that a nematode maybe the vector. Cardin & Legin, 1972 ; Brown & Taylor, 1981). Indefinitive tests nematodes must be extracted Viruses also differ in their ability to become system- afterexposure to the virus infected sourceplants ically distributed in source plants and in manually and individually transferred to the roots of the bait inoculatedplants and may therefore Vary in their plantswhich should be grown in containers and a availability to feeding nematodes. mediumwhich have previously been partially sterilized to ensure freedom from potential vectors. The sievings from which the nematodes have been UNFAVOURABLEENVIRONMENT removed must be tested for alternative vectors and appropriatecontrols should be used to check for An unfavourable distribution of soil particle sizes, possible transmission by stray or wind- or toohigh, too low, or rapidlyfluctuating soil borne fungal spores. Where possible, these organisms moistures or temperatures may be unsuitable to the should also berigorously excluded. The control nematodesand prevent their moving and feeding. plants should be numerous, and be an integral part Toxins,pathogens, rough handling or extreme of the bait and assay tests, and should also be used conditionsmay result inthe nematodes being to demonstrate that the source, bait and assay plants adverselyaffected or killed. Also someviruses or and the nematodes (unless they were from around a strains may be adapted for a particular temperature virus-infestedplant in the field) were al1 initially or host range. virus-free.

Suggested test procedure Demonstrating the inability of a nematode to transmit a virus The most suitable procedure for testing the ability of alongidorid nematode totransmit a particular It cannot be completely proved that a particular virusisolate depends on the nematodelvirus com- species of nematode is completely unable to transmit bination being tested but, as already indicated, there avirus. It isknown thatpopulations of a species arecertain basic requirements. A testprocedure may differ in their ability to transmit strains of a which is a development of that described by Valdez virus.However, if good techniques are used, much (1972) andTrudgill and Brown (1978) and satisfies circumstantialevidence can be obtained that the these requirements is given in Figure 1. It minimises population under study is not a vector.Lilrely causes thepossibility of contamination, uses onlysmall of failure totransmit due to poorexperimental procedures are :

UNSUITABLEVIRUS SOURCEOR BAIT PLANTS (1) X. americanum S. lat. is a complex of species and X. americanum sensu stricto has a geographical Douthitand McGuire (1978) recoveredtobacco distributionrestricted to theeastern part of North ringspot virus from only25 of 38 species of bait plants America (Lamberti & Bleve-Zacheo, 1979).

Revue Nématol. 6 (1) :133-142 (1983) 135 D.L. Trudgill, D.J.F. Brown h D.G. NcMamara numbers of nematodes,and demonstrates that the Taylorand Robertson (1970), to determine the nematodes have fed on and ingested virus from the proportion of nematodesretaining virus particles sourceplants, and have fed onthe bait plants. within their feeding apparatus. Further nematodes Inthis procedure virus-free nematodes are placed and the bodies from which the heads were removed aroundthe roots of virus-infectedsource plants are tested directly for virus in their intestine. This growing in small pots which are plunged in a bed of can be done in one of two ways. moist peat or Sand.McNamara (1978) used porous 1) If the virus in the nematode remains infective potswithout drainage holes but plasticpots may it canbe tested for by slash-testing (breaking-up beused provided they are maintained in a humid smallnumbers of nematodesin phosphate-buffer atmosphereasdescribed by Taylor and Brown (pH 6.9)and inoculating virus indicator plants (1974).Ideally only adultnematodes should be with the suspension ; Taylor, 1964). added to source plants so as to eliminate the possi- bility of negative results being obtained because of 2) A more sensitive technique, which hasbeen used the nematodesmoulting during the test. After an successfullywhere the virus particles could not be appropriateperiod of access tothe sourceplants, detected by slash-testing, is immunosorbent electron thenematodes are carefully extracted, counted microscopy (ISEM). This technique involves at>tach- and about half their number are transferred in small ingvirus particles on electron microscopegrids groups,by hand-picking, to virus-free bait plants using the appropriate antiserum (Roberts & Brown, growing in similar conditions. At the same time a 1980). few nematodeheads are taken and processed for Thenematodes that wereplaced on bait plants electronmicroscopy of thin sections, as described by are allowed to feed for a suffkient period to enable

Sectionsthrough ISEM or ISEM slash-test heu& examned with electron microscope

Nematodes counted and handpicked Tops indexed VIRUS-FRFF for virus .v-j-ENLuaE 6 Nematodes countd an3 Serologically identifid identified - r- [% SURVIVALJ virus L Plants indexed 1 Root-tip Semlogical for virus.Rwt- galls counted identification tip galls counted OPPORTUNITY ITRANSMISSION] -

Roots indexed virus VIRUS-FREE for CONTROL PLANTS - PRESENT sievings free Virus-fre frorn wspected nerratodes vector TRANSMISSION

Fig. 1. The suggested procedure for establishing the ability of longidorid nematodes to transmit plantviruses.

136 Revue Nèmafol. 6 (1) :133-141 (1983) Assessing transmission of plant viruses virus to be transmitted and then to spread system- nativevectors the controls should also testthe ically within the plant, after which the nematodes nematodes,the source, bajt and assay plants for arere-extracted and counted and the carefully initialfreedom from virus. Virus that is trans- washedroots and hypocotyl or tops of the plants mitted and the nematodes transmitting that virus tested for virus infection. must be re-identified at the endof the test. Fromthe results of the ISEM, slashand bait tests the proportions of nematodes acting as sources of viruscan be estimated using the Maximum Likelihood formula (Gibbs & Gower, 1960) provided Conclusions that the experiments are extensively replicated and that the proportion of infected plants is neither too small nor too large. Accurateinformation about the capacity of Evidence that the nematodes fed onthe source longidoridnematodes totransmit viruses causing andbait plants can be obtained by showing that plant diseases is a pre-requisite for effective disease the,nematodes developed andreproduced or by controlmeasures. Inaccurate or misleadinginform- examining theplant roots for feedingdamage ationdelays progress and causes confusion and (galls, etc.). Controls must be numerous, randomised diffIcultiesfor nematologists involved in regulatory within the bait-test and not evident to those conduct- matters (i.e. production of virus-freeplanting ing the final assay. In addition to testing for alter- stocks).Because of thecomplexity of thetrans-

Table2 Viruses and their specific Longidorus or Xiphinema vectors for which the evidence for nematode transmission is considered adequate

Virus Vector Reference

Grape fanleaf virus X. index Hewitt et al., 1958 fanleaf virus X. italiae Cohn et al. 1970 * Arabis mosaic virus X. diversicaudatum Jha & Posnette, 1959 Harrison & Cadman, 1959 latent ringspot virus X. diversicaudatum Lister, 1964 Harrison, 1967 X. americanum sensu lato * Fulton, 1962 Grifin et al., 1963 Tomato ringspot virus X. americanum sensu lato Breece & Hart, 1959 rosette mosaic virus X. americanum sensu lato Klos et al., 1967 Cherry rasp leaf virus X. americanum sensu lato Nyland et al., 1967 Tomato black ring virus (E) L. attenuatus Harrison, 1964 Tomato black ring virus (S) L. elongatus Harrison et al., 1961 Raspberry ringspot virus (E) L. macrosoma Harrison, 1962 Debrot, 1964 Raspberry ringspot virus (S) L. elongatus Taylor, 1962 Raspberry ringspot virus (S) L. macrosoma Harrison, 1964 Artichoke Italian latent virus L. apulus *** Rana & Roca, 1975 Mulberry ringspot virus L. martini Yagita & Komuro, 1972

This result has been questioned by Martelli (1975) ; See footnote p. 135 ; * * * L. attenuatus redescribed as L. apulus by Lamberti and Bleve-Zacheo (1977).

Revue Nématol. Revue 6 (1) : 133-141 (1983) 137 D.L. Trudgill, D.J.F. Brown dl- D.G. &IcNamara

Table3 Virus and vector combinations for which the evidence for nematode transmission is considered to be inadequate

Virus Descri Virus bed ueetor Reason Reference

NEPOVIRUSES Arabis mosaic X. coxi Fritzsche, 1964 1, 2 L. caespiticola Valdez, 1972 1 X. bakeri Iwaki & Komuro, 1974 P. maximus McElroy et al., 1976 X. index Fritzsche & Thiele, 1979 Strawberry latent ringspot X. coxi Putz & Stock, 1970 P. maximus McElroy et al., 1976 Cherry leaf roll X. diversicaudatum Fritzsche & Kegler, 1964 Flegg, 1969 X. coxi Fritzsche & Kegler, 1964 X. vuittenezi Flegg, 1969 Tobacco ringspot X. coxi Van Hoof, 1971 Tomato ringspot X. brevicolle Fritzsche & Kegler, 1968 Euonymus ringspot Xiphinema spp Puffinberger & Corbett,. 1973 Raspberry ringspot L. profundorum Fritzsche & Kegler, 1968 1, 2 X. diversicaudatum Fritzsche & Kegler, 1968 1, 2 L. caespi ticola Valdez, 1972 1 L. leptocephalus Valdez, 1972 P. maximus McElroy et al., 1976 Artichoke Italian latent L. attenuatus Rana & Roca,'1975 Grape chrome mosaic X. index Mali et al., 1975 ** OTHERVIRUSES Brome mosaic X. diversicaudatum Schmidt et al., 1963 x.coxi Schmidt et al., 1963 L. macrosoma Fritsche, 1968 Carnation ringspot X. diversicaudatum Fritzsche & Schmelzer, 1967 1, 2 L. macrosoma Fritzsche, 1968 1. 2 L. elongatus Fritzsche et al., 1979 2 Prunus necrotic ringspot L. macrosoma Fritzsche, 1968 1, 2 Euonymus mosaic L. euonymus Mali & Hooper, 1973 1, 2 Cowpea mosaic X. ifacolum *** Caveness et al., 1975 2 Pear stony pit L. macrosoma Kegler et al., 1976 1, 2, 3

* 1 : No systemic infection, contamination of roots possible ; 2 : Inadequate desc,ription of methods or inadequate or inappropriate control ; 3 : Vector and/or virus not adequatelyidentified. * * Rumbos et al. (1977) have reported X. indez may be a vector of a rickettsia-like organism associated with yellows disease of grapevines. However they do not provide any experimental evidence for this suggestion. +** X. basiri reported by Caveness et al. (1975) is X.ifacolum (M.Luc, in litt.).

138 Reuue Nèmatol. 6 (1) :133-141 (1983) Assessing transmission of plant viruses

mission process accurate information can be provided CAVENESS, F.E.,GILMER, R.M. & WILLIANS,R.J. only by carefulexperimentation and there is now (1975).Transmission of cowpeamosaic by Xiphi- a needfor a generallyaccepted set of criteria by nemabasiri in westernNigeria. In : Lamberti, p., which the results of transmission tests can be judged. Taylor, C.E. & Seinhorst,J.W. (Eds). Nematode Belowwe list the criteria weconsider should be Vectors of Plant Viruses, London, Plenum Press : 289-290. satisfied to demonstrate that a is trans- mitted by a species of longidorid nematode. COHN, E., TANNE, E. & NITZANY, F.E. (1970).Xiphi- nemaitaliae, a newvector of grapevinefanleaf 1) It must be shown that the virus has infected virus. Phytopathology, 60 : 181-182. the bait plant. DALMASSO,A., MUNCK-CARDIN, M.C. & LEGIN, R. 2) Thetest should be conducted with hand- (1972).Résultats préliminaires d’essaisde trans- picked nematodes and with such controls that the missions desérotypes de la mosaïque del’arabis nematode is shown to be the vector. trouvés sur vigne par l’intermédiaire de Xiphinelna diversicaudatum. Ann. Phytopathol., 4 : 410. 3) Thenematodes transmitting the virus should beidentified, preferably byan authority on the DEBROT,E.A. (1964). Studies on a strain of raspberry ’ genus, noting anydifferences from type specimens. ringspot virus occuringin England. Ann. appl. Biol., 54 : 183-191. 4) The virus isolate must be identified before and afterthe transmission test. DOUTIIIT, L.B.& “GUIRE, J.M. (1978). Transmission of tobacco ringspotvirus by Xiphinemaameri- Using these guidelines we have Iisted in Table 2 canum to a range of hosts. PlantDis. Reptr, 62 : thenematodelvirus associations forwhich we 164-166. consider there is suffkient evidence to substantiate FLEGG,J.J.M. (1969). Tests with potential nematode the authors’ claim that the virus is transmitted by vectors of cherry leaf roll virus. Rep. E. Malling a particular nematode species. Interestingly most of Res. Stn for 1968: 155-157. theseassociations have been reported causing FRITZSCHE,R.(1964). Untersuchungen über die economicaliy important disease outbreaksin the Virusiibertragungdurch Nematoden. Wiss. 2. field. The much greater number of associationsfor Univ. Rostock, Math-naturwiss. R., 13 : 343-347. whichwe consider the evidence insuficient are FRITZSCHE,R. (1968). Okologie undVektoreignung listed in Table 3. Some of the associations reported von Longidorus macrosoma Hooper. Biol. Zbl., 87 : in Table 3 may be correct but for those not involving 139-146. ,viruses such as carnationring spot FRITZSCHE, R.& KEGLER,H. (1964). Die obertragung virus which may be transferred from plant to plant desBlattrollvirus der Kirsche (cherry leaf-roll in soi1 water (Kleinhempel, Gruber & Kegler, 1980)’ virus)durch Nematoden. Naturwissenschaften, 51 : or those contrary to the pattern of specificitypre- 299. viouslyobserved we consider that unequivocal FRITZSCI-IE,R. & KEGLER,H. (1968). Nematoden als evidence is required before theyare accepted as Vektoren von Viruskrankheiten der Obstgewachse. valid. TagBer. dt. Akad. LandwWiss. Berl., 97 : 289-295. FRITZSCHE,R., KEGLER,H., THIELE,S. & GRUBER,G. (1979). Beitrag zur Epidemiologie und obertragung ACKNOWLEDGEMENTS des Nelkenringfleclien-Virus in Obstbestanden.Arch. Phytopathol. u. Pflanzenschutz, Berlin, 15 : 177-180. Wethank Drs B.D. Harrison,A.F. Murant, Mr FRITZSCHE,R. & SCHMELZER,K. (1967). Ubertrag- W.M. Robertsonand Pr C.E. Taylorfor helpful barlreitdes Nelkenringflecken-Virus durch Nema- discussions, ideas and comments. toden. Naturwissenschaften, 54 : 495-499. FRITZSCHE,R. & TIIIELE, S. (1979).Eignung von Xiphinema-Herkünften aus derUdSSR und der DDRzur obertragungdes Arabis-Mosaic-Virus. REFERENCES Nachrichtenbl. Pflanzenschutz DDR., 33 : 103-104. FULTON,J.P. (1962). Transmission of tobacco ringspot BREECE,J.R. & HART,W.H. (1959). A possible virusby Xiphinemaamericanum. Phytopathology, association of nematodes with the spread of peach 52 : 375. yellow bud mosaic virus. Pl. Dis.Reptr, 43 : 989- GIBBS,A.J. & GOWER,J.C. (1960). The use of a multi- 990. ple-transfermethod in plant virus transmission BROWN,D.J.F. & TAYLOR,C.E. (1981).Variazioni studies - some statisticalpoints arising in the nella trasmissione di virus tra popolazioni di nema- analysis of results. Ann. appl. Biol., 48 : 75-83. todi vettori . Atti Soc. Italiano Nema- GRIPFIN, G.D., HUGVELET,J.E. 22 NELSON, J.W. tol., Giornate Nematol., Firenze 1979 : 191-204. (1963). Xiphinemaamericanum as a vector of

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140 Revue Nhmatol. 6 (1) : 133-141 (1983) Assessing transmission of plant viruses

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Accepte' pour publication le 19 mars 1982.

Addendum (5 may 1983)

Further reports of virus transmission by longidorid nematodes are : 1) Artichoke Italian latent virus transmitted by L. fasciatus (Roca & Lamberti, 1981, Nematol. medit., 9 : 175- 179 ; Roca, Rana & Kyriakopoulou, 1982, Nematol. medit., 10 : 65-69). This association is accepted as valid with the reservation that the virus statusof the controls was not reported. 2) Tomato ringspot virus transmitted byX. rivesi (Forer, Hill & Powell, 1981, Phytopathology, 71 : 874, Abstract). The published evidence for this association is regardedas inadequate (2, 1 (see foot-note to Table 3)). 3) Description of X. diadecturus n. sp. (Nematoda : Longidoroidea), a vector of the peach rosette mosaic virus in peach orchards insouth-we'stern Ontario, Canada (E.S. Eveleigh & W.R. Allan, 1982, Can. J. Zool., 60 : 112-115). No evidence is presented to support this association and therefore it cannot be regarded as acceptable (2) (see foot-note Table 3). 4) L. vuittenezi (Nematoda : Dorylaimidae). Virusübertrager bei Reben 7 (Maria Rudel, 1980, Die Wein-Wissen- schaft, 35 : 117-194). The author of this paper expresses reservations, withwhich we agree, regarding the transmis- sion of grape fanleaf virus by X. vuittenezi.

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