Transmission of Plant Viruses by Dodder 1

TRANSMISSION OF PLANT VIRUSES BY DODDER 1

ROBERT M. HOSFORD, JR. Department of Plant Pathology North Dakota State University Fargo, North Dakota, 58102

Mechanics of virus transmission by dodder ...... 387 Review of literature on virus transmission by dodder ...... 389 Acknowledgments ...... 402 Literature cited ...... 402

MECHANICS OF VIRUS TRANSMISSION BY DODDER In 1940 Bennett discovered that a virus could be transmitted from an infected to a healthy plant through a bridging dodder that was parasitizing both plants. Since then numerous workers have shown that many viruses are transmissible. The subject has been reviewed by Mooi-Bok (1949), Sibilia (1951), Bawden (1956, 1964), and Fulton (1964). Transmission probably involves an association of dodder and host cells, and directional movement of nutrients. It has long been known that dodder haustoria establish cellular connections with the host plant. Thoday (1911) found that the protoplasts of dodder and host phloem cells are in close association but do not appear to fuse. Bennett (1944b) hypothesized that dodder acquires viruses with the food materials from the phloem of the host. His studies of dodder stems inoculated with beet curly-top virus or with cucumber mosaic virus indicated that after entering the dodder a virus moves more rapidly toward growing points than in the opposite direction. He suggested that yellows-type viruses move from the phloem of the dodder into the phloem of the healthy host by temporary reversaIs of phloem nutrient flow and that mosaic-type viruses move from the parenchyma of the haustorium to that of the host through plasmodesmatal strands or from possible naked protoplasmic connections of dodder and host, as well as through the phloem. Bennett (1956) proposed that the above idea of temporary-reversal- of-flow fits well with the theory that materials in the phloem move "... by mass flow of liquid content of the phloem from the regions of carbohydrate supply toward regions of food utilization." Cochran (1946) found that consistent transmission of tobacco mosaic virus could be achieved only by pruning the dodder and shading the healthy host while keeping the infected host in bright light; Bennett (1956) suggested that this forced a temporary reversal of phloem nutrient flow. Canova (1955) observed that Olscuta epithymum Murr. acquired beet-yellows virus but did not transmit it, and Bennett (1960) found the same to be true for C. californica Hooker &

1. The library research for this article was concluded in January, 1967. 387 388 THE BOTANICAL REVIEW

Arnott and C. campestris Yunck. This might indicate an absence of temporary reversal of phloem nutrient flow. Cochran (1947) improved transmission, compared to merely connecting virus-diseased and healthy host plants with a bridge, by making a "dodder graft" with dodder buds. He attributed the improved transmission to "... the increased number of shorter dodder stems connecting diseased and healthy tissues." Lackey (1941) found that the dodder haustoria usually do not make contact with the degenerate phloem of beet plants with severe curly-top. He considered low curly-top transmission to be related to poor cell contact. Besides association of host and parasite cells and directional movement of nutrients in the phloem, various other factors may influence transmittance of specific viruses. Miyakawa and Yoshii (1951) demonstrated the presence of an inhibitor of the poorly transmitted tobacco mosaic virus in dodder juice. Costa (1944) showed that the tobacco mosaic virus does not persist or multiply in dodder, but observed that the easily transmitted cucumber mosaic virus persists, causes a distortion of growth, and multiplies in dodder. From the above studies one might hypothesize a passive movement of tobacco mosaic virus through the dodder and an inactivation of the virus by an inhibitor in the dodder sap. When quantitative movement of the virus exceeds inactivation, transmittance might occur. Schmelzer (1956b) found virus inhibitors in dodder sap but made no corre- lation between inhibitors and the transmittance phenomenon. Bennett (1940, 1944b) found that the poorly transmitted beet curly-top virus apparently does not multiply in dodder and does not persist unless the dodder is growing on a curly-top diseased host plant. Bennett (1944a,b, 1949) reported that dodder latent virus persists but is latent (symptomless) in Cuscuta species. Its concentration rises to a high level a few days after inoculation and then declines to a low level. By means of Cuscuta subinclusa Dur. & Hilg., Yarwood (1955) transmitted apple mosaic from tobacco to tobacco, apple, and strawberry, but not to peach, apricot, or onion. Schmelzer (1956a) successfully conveyed lucerne mosaic to Nicotdana g&linosa L. by means of Cuscuta campestris, C. subinclusa, and C. europaea L. but not by C. californica or C. epithymurn. These studies indicate that virus transmission varies with the virus, the dodder species, the host plants, and the environmental stresses on the plants. Additional examples of this variation are discussed under the individual viruses. Dodder, along with grafting, insect vectors, juice inoculation, and other means of virus transmittance, has become a useful tool in the study of viruses. Separation of virus mixtures in a plant, providing evidence of the virus nature of certain diseases, and extending the host range of a number of viruses are uses to which dodder has been put. Johnson (1941a) used Cuscuta campestrds and juice inoculation to separate two viruses in a clover plant. Bennett (1940) separated cucumber mosaic virus from a mixture of it and tobacco mosaic virus in a host plant by means of dodder. Kunkel (1945) used dodder to extend the host range of vaccinium false-blossom virus to host plants that are quite different taxonomically, thus overcoming some of the limitations of virus transfer by grafting, in which unions usually occur only between closely related species. Bawden (1956) warns that this extension of virus host ranges by man through MECHANICS OF VIRUS TRANSMISSION 389 dodder could be dangerous, in that the viruses might be spread by vectors on the new hosts to previously unaffected economic plants. Bawden (1964) reported that one dodder species, Cuscuta campestris, parasitizes over 100 host species, and Johnson (1941b) stated that C. campestr& attacks plants in 26 genera of 10 plant families. Lackey (1946) observed Cuscuta species parasitizing other Cuscuta species and even themselves. Examples of uses to which dodder has been put are more fully discussed under the individual viruses.

REVIEW OF LITERATURE ON VIRUS TRANSMISSION BY DODDER Reports of virus transmission by means of Cuscuta species have been alpha- betically listed by the common name of the virus. Following this is a discussion of the relationship of the virus to its transmission by Cuscuta species, hosts involved, and other related phenomena. Wherever possible the preferred disease name as indexed in the Review of Applied Mycology (RAM) is used. Where a disease name has not been found in RAM, the name used is that given by the cited author.

AGERATUM CONYZOIDES YELLOW VEIN BANDING MOSAIC: Thung and Hadi- widjaja (1950) transmitted the causal virus to healthy plants by means of Cuscuta australis R. Br. APPLE MOSAIC: Yarwood (1955) transmitted the causal virus from tobacco to apple by means of Cuscuta subinclusa and C. campestris, and from tobacco to strawberry and tobacco by means of C. subinclusa. Attempts to pass it from tobacco to peach, apricot, or onion using C. subinc/usa were unsuccessful. No disease symptoms appeared in the transmitting Cuscuta species. ARABIS MOSAIC: Schmelzer (1962) transmitted a strain of arabis mosaic virus (causing a yellow-net disease of Forsythia intermedia Zab.) to healthy plants by means of Cuscuta subinclusa, C. ca/ifor~zica, and occasionally C. campestris. ASCLEPIAS-YELLOWS: Kunkel (1950) passed asclepias-yellows from Asclepias syriaca L. to carrot, tomato, and Vinca rosea L. by means of Cuscuta cam- pestrJs. ASTeR-YELLOWS: Johnson (1941a, b) transmitted aster-yellows to 4 of 50 Callislephus chinensis (L.) Ness plants in 40 days and to 6 of 30 Nicotiana rustica L. plants in 35 days by means of Cuscuta campestris. At the Quebec Society for the Protection of Plants Symposium (1952) it was reported that aster-yellows on potato and a purple-top disease of potato (that may also have been aster yellows) were transmitted by means of C. gronovii Willd. Brierley and Smith (1957) transmitted a strain of aster-yellows virus causing a chrysanthemum flower distortion to Villca rosea by means of Cuscuta campes/ris. Protsenko (1958) conveyed aster-yellows from Cineraria hybrida Hort. to petunia and from petunia to Nicotiana tabacum L., by means of Cuscuta europaea. Later (1959) he used C. europaea to pass aster-yellows virus from Ch'sium arvense Scop. to Petunia hybrida Hort. Hollings (1960) conveyed a strain of aster-yellows virus, causing greening of flowers of 'Bal- 390 THE BOTANICAL REVIEW

combe Perfection' chrysanthemum, by means of Cuscuta subinclusa to Vinca rosea, in which it caused apical rosetting, yellowing and chlorosis of the leaves, and phyllody. Frederiksen (1962) transmitted a strain of aster-yellows virus to flax by means of Macrosteles fascifrons Stal. and dodder. Mokra (1964) transferred a strain of aster-yellows virus causing a green-petal disease of primrose from Primula denticulata Sm. and P. obconica Hance. to Nicotiana glutinosa and Petunia hybrida by means of Cuscuta camlestris. Attempts were unsuccessful to pass the virus from Primula denticulata and P. malacoides Franch. to Callistelhus chinensis, Lycopersicon esculentum Mill. (So- lanum lycopersicum L.), Vinca rosea, and Nicotiana tabacum by means of C. campestris. She transmitted a virus causing witches'-broom disease (differing from green-petal disease in that the inflorescence had the character of a witches'-broom disease) from Primula malacoides to P. malacoides by grafting and by means of C. campestris. BARLEY YELLOW DWARF: Timian (1964) transmitted barley yellow dwarf from infected to healthy Hordeum vulgare L. emend. Lam. 'Black Hulless' (C.I. 666) barley plants by means of Cuscuta camlestris. BAYBERRY-YELLOWS: Raychaudhuri (1953) transmitted bayberry-yellows by means of Cuscuta campestris and C. subinclusa to bayberry (Myrica carolinien- sis Mill.), Vinca rosea, Daucus carota L., Beta vulgaris L. (sugar beet), Petunia hybrida var. nana compacta, and Allium cepa L. The virus caused a yellowing in all except the dodders in which a reduction in stem diameter occurred. Dodder growing on asters immune to bayberry-yellows retained the virus for 14 months. Attempts were unsuccessful to transmit the virus to Callistephus chinensis (China aster), Calendula officinalis L., Zinnia multi- flora L., Medicago sativa L., Phaseolus vulgaris L., Vicia /aba L., Trifolium incarnatum L. var. 'Bokhara', Vaccinium corymbosum L., V. macrocarpon Air., Gomphrena globosa L., Datura stramonium L., Solarium melongena L., S. tuberosum L., Lycopersicon esculentum, Nicotiana tabacum, N. glauca Grah., N. glutinosa, N. rustica, and Prunus persica (L.) Stokes. BEET CURLY-TOP: Bennett (1940) transmitted beet curly-top to a low percentage of healthy sugar beets (2 to 5 per cent) and to Turkish tobacco by means of Cuscuta subinclusa, which contained curly-top virus concentrations equal to those of the diseased hosts but which lost the virus within a few days after the breaking of the connection with the diseased hosts. In subsequent experiments Bennett (1944b) transmitted the virus by means of C. subinclusa, C. campestris, and C. californica to low percentages of healthy plants. When these dodders were then placed on non-hosts of the virus, the virus was recovered from the dodders for only ten days. Johnson (1941b) transmitted beet curly-top to 7 of 16 test plants in 19 days by means of C. campestris. Lackey (1941) studied the histology of the dodder, curly-top virus, and sugar beet relationship, and found that the haustoria did not make contact with the degenerate phloem of beet plants with severe curly-top. He attributed the few instances of carry-over of the virus from severely diseased to MECHANICS OF VIRUS TRANSMISSION 391

healthy beet plants (by means of C. californica) to occasional connections of the haustoria with the diseased phloem. When Giddings (1947) fed beet leafhoppers on C. subinclusa growing on Turkish tobacco infected with beet curly-top, a higher percentage of transmission of beet curly-top virus by the leafhoppers to sugar beets was attained (75 per cent) than when the leafhoppers were fed only on the tobacco (55 per cent). He proposed that the reduction in percentage of transferral from tobacco alone resulted from the leafhoppers being entangled and their feeding hindered by the leaf hairs and sticky exudates of the tobacco. Lackey and Bennett (1949) found that curly- top virus concentration in C. subinclusa and C. californica parasitizing plants with curly-top disease was about equal to that of the host. However, when the dodder was placed on hosts immune to the virus, the virus in the dodder soon disappeared. This indicated that the virus could not persist in dodder unless the latter was growing on a curly-top diseased host plant. However, they found that although in most instances C. californica appeared to be normal when growing on curly-top infected plants, in some examples it showed disease symptoms characteristic of curly-top. They suggest that "... under certain conditions curly-top virus is able to produce injury to plants that must be considered immune in the generally accepted connotation of this term." Bennett (1955) transmitted virulent strains of beet curly-top virus from Samolus parviflorus Raf. plants that had recovered from infection to healthy plants by means of Cuscuta californica. He suggested that recovery may be related to reduction of virus concentration through virus aggregation, adsorp- tion on some proteins, or both. He observed no distinct signs of cross-protection among mild to severe strains of the virus. Bennett (1957) transmitted a strain of beet curly-top virus, causing a vein yellowing, by means of four species of Cuscuta, by the beet leafhopper (Circulifer tenellus Baker), and by grafting, but not by sap inoculation or seed. The strain was not separated from typical curly-top virus but was carried with the typical virus to tobacco, sugar beet, tomato, and other plants. The typical curly-top virus then was separated from the mixture. BEET (St:cAR) ROSETTE: Bennett and Duffus (1957) transmitted sugar beet rosette virus by grafting and by means of Cuscuta campestris to a low percentage of tested sugar beets but were not able to do so by means of C. subinclusa, sap, or insects. BEET-YELLOWS: Fuchs and Beiss (1954) and Beiss (1956) reported high percentages of transmission of beet-yellows virus by means of Cuscuta gronovii. Canova (1955) did not pass two Italian forms of beet-yellows virus from beet to beet by means of Cuscuta epithymum. However, he found that the aphid, Myzus persicae Sulzer, after 24 hours of feeding on C. epithymum growing on yellows-infected beets, transferred the yellows disease to healthy beets. He suggested that the dodder acquired yellows but did not transmit it. Bennett (1960) also did not obtain carry-over of the yellows virus by means of Cuscuta americana L., C. californica, C. campestris, and C. gronovii from sugar beet to sugar beet and other hosts. He did obtain high percentages of 392 THE BOTANICAL REVIEW

transmission by feeding green peach aphids on C. californica and C. campestris growing on diseased beet plants, and then transferring the aphids to seedling beet plants; this supported Canova's (1955) observation that dodder can acquire but not transmit yellows virus. Bennett (1960) obtained no infection in tests for yellows virus in dodder 30 days after the dodder had been established from diseased beet plants onto Turkish tobacco and disconnected from the beet plants. He concluded "... that the virus did not persist in dodder for as long as 30 days after it became established on a plant immune to yellows." BEET YELLOW WILT; Bennett and Munck (1946) reported that beet yellow wilt destroyed the sugar beet industry in the Rio Negro Valley of Argentina. Yellow wilt was thought to be caused by a virus and to be transmitted by the leafhopper, Exitianus exitiosus Uhler. The virus was conveyed by grafting and in a few instances by means of Cuscuta subinclusa and C. campestris, but not by plant sap. CENTROSEMA MOSAIC: Van Velsen and Crowley (1961) transmitted centrosema mosaic, a previously undescribed virus which infects several tropical legumes, to Centrosema pubescens Benth. and other hosts by means of Cuscuta campestris, Aphis gossypii Glover and Brachycaudus helichrysi (Kltb.)? var. warei Theob., two species of Nysium (plant bugs), and plant sap. CHILLI MOSAIC: Gualaccini (1956) transmitted chilli mosaic virus by means of Cuscuta pentagona Engelm. and sap inoculation to 'Perustitza' tobacco but not to 'White Burley', an uncertain variety (Xanty YakS), and 'Herzegovina' tobacco plants, Nicotiana glutinosa, tomato, or beet. He suggested that the virus was a strain of tobacco mosaic virus. CHRYSANTHEMUM STUNT: Keller (1953) passed chrysanthemum stunt to Chrysanthemum morifolium Ramat. vat. 'Sea Gull' via Cuscuta gronovii. CITRUS EXOCORTIS: Weathers (1965) transmitted exocortis virus from West Indian lime (Citrus aurantifolia Swingle) to 'Etrog' citron (Citrus medica L.) and possibly to Petunia hybrida, and Weathers, Harjung, and Greer (1956) transferred exocortis from West Indian lime to 5 of 12 'Etrog' citrons and possibly to 8 of 22 petunia plants by means of Cuscuta subinclusa. CITRUS PSOROSlS: Price (1963) transmitted psorosis to 4 of 93 'Pineapple' sweet orange seedlings by means of Cuscuta compacta Juss. Weathers and Harjung (1964) obtained a 14 per cent carry-over of citrus psorosis by means of C. subinclusa, and approximately a 5 per cent transmission to sweet orange seedlings by means of C. compacta. Weathers, Harjung, and Greet (1965) passed psorosis from sweet orange trees to 4 of 18 lemon trees, 2 of 14 West Indian lime trees, and 3 of 16 sweet orange trees by means of C. subinclusa. CITRUS TRISTEZA: Bennett and Costa (1949) transmitted tristeza to 1 of 20 sweet orange (Citrus sinensis Osbeck) plants by means of Cuscuta subinclusa and to 1 of 20 sweet orange plants by means of an unidentified Cuscuta spe- MECHANICS OF VIRUS TRANSMISSION 393

cies. They were unsuccessful in attempts to pass it to sweet orange by means of Cuscuta americana, C. campestrJs, or C. indecora Choisy. None of the five dodder species carried the virus to carrot, tomato, tobacco, or other selected dodder host plants. Subsequently, Weathers and Harjung (1964) obtained over 14 per cent transmission of tristeza by means of C. subinclusa. Weathers, Harjung, and Greer (1965) transferred tristeza from West Indian lime to 4 of 18 healthy West Indian lime plants by means of C. subJnclusa. CITRUS VEIN-ENATION: Weathers and Harjung (1964) obtained a 28 per cent transmission of citrus vein-enation by means of Cuscuta subinclusa. Weathers, Harjung, and Greer (1965) passed vein-enation from rough lemon to 9 of 35 rough lemon plants by means of C. subinclusa. CLOVER DWARF: Mi~iga (1961) transmitted clover dwarf by means of Cuscuta campestris and C. subinclusa. Valenta and Musil (1963) transferred clover dwarf from white clover, SenecJo vulgaris L., and ]asione montana L. to 33 plant species in 11 families by means of Euscelis plebejus Fall., Aphrodes bicinctus Schrk., grafting, and dodder. Cuscuta campestris was used to carry the virus to Lycopersicon esculentum, and C. subinclusa was used to transport it to VJnca rosea and Trifolium repens L. CI.OVER-ENATION: Bos and Grancini (1963) transmitted a virus causing enation-like disease symptoms on the undersurface of the midrib of white clover by means of Cuscuta campestris and plant sap. CLOVER-MosAIC: Johnson (1941a) transmitted a mosaic disease to healthy plants by means of Cuscuta campestris. Johnson (1941b) separated white clover virus 1 into two components; one was carried through C. campestris to Vicia faba L. and MedTcago lupulina L., and the other was conveyed by juice from mosaic-diseased white clover to cow peas. He transferred clover mosaic to 9 of 12 broad-bean plants in 23 days and to 5 of 8 hop-clover (Medicago lupulina) plants in 30 days by means of C. campestris. Bos et al. (1959) found that clover mosaic was contained in and transmitted by C. campestris. CtOVER-YEtLOW MOSAIC: Pratt (1961) transmitted clover-yellow mosaic from infected Vicia faba (broad-bean) to healthy V. faba by means of Cuscuta campestris. CORN STUNT: Maramorosch (1963) conveyed corn stunt from corn to Vinca rosea var. alba by means of dodder and Dalbulus maidis Delong & Walc. His attempts to transmit it back from Vinca rosea to corn were unsuccessful. CROTALARIA WITCHES'-BROOM: Thung and Hadiwidjaja (1950) transmitted witches'-broom of Crotalaria usaramoensis Baker f., C. anagyroides HBK., C. juncea L., and C. striata Schum. & Thonn. from diseased to healthy plants by means of Cuscuta australis. CUCUMBER MOSAIC: Bennett (1940) transmitted cucumber mosaic to high percentages (over 90 per cent) of Turkish tobacco and Nicotiana glauca 394 THE BOTANICAL REVIEW

plants by means of Cuscuta subinclusa and C. californica. He found that the virus was retained by C. subinclusa growing on cucumber mosaic virus (CMV)-immune dodder hosts. He used the persistence of CMV in dodder and the ease of transmission of CMV by dodder compared to tobacco mosaic virus (TMV) to isolate CMV from a mixture of CMV and TMV in Turkish tobacco. Johnson (1941a, b) passed cucumber mosaic to 7 of 22 test plants in 21 days by means of Cuscuta campestris. The Kentucky Agricultural Experi- ment Station (1942) reported the transmission of a strain of cucumber mosaic from a red clover plant to tobacco by means of dodder. Costa (1944) found that CMV persisted, caused a distortion of growth, and multiplied in dodder, from which he transferred it to tomato, tobacco, and broad-bean. Bennett (1944b) used C. subinclusa, C. carnpestris, and C. californica to convey cucumber mosaic to up to 100 per cent of his tested plants. He observed that the virus was recovered after periods of one to four months from C. californica, C. subinclusa, and C. campestris growing on non-host plants of the virus. Hildebrand (1945) transmitted cucumber mosaic from cucumber to cucumber but not from cucumber to peach by means of C. subinclusa, C. californica, C. carnpestris, and C. repens (no authority found). Available facilities did not exclude the possibility of some insect transmission. Sakimura (1947) carried cucumber mosaic from cucumber to 21 of 40 cucumber plants by means of Cuscuta sandwichaina Choisy. Schmelzer (1956a) effectively transmitted cucumber mosaic by means of C. campestris, C. californica, C. subinclusa, C. gronovii, C. americana, C. europaea, and C. epithyrnurn to Nicotiana glutinosa, but to only 6 of 40 plants using C. lupuliforrnis Krocker. He passed a virulent green strain of the virus to a low percentage of plants by means of C. californica and C. europaea but not with C. lupul~forrnis. The virus produced disease symptoms on C. carnpestris. Schmelzer (1957) reported the transmission of cucumber mosaic to 75 of 77 'Samsun' tobacco plants by means of C. subinclusa, to 48 of 49 plants by means of C. carnpestris, 52 of 55 by C. californica, 46 of 47 by C. europaea, and 67 of 76 by C. epithyrnurn. He conveyed a yellowing strain of cucumber mosaic virus to 48 of 57 'Samsun' tobacco plants by means of C. subinclusa, to 18 of 54 plants with C. californica, 2 of 13 with C. europaea, and 0 of 2 with C. epithymurn. DODDER LATENT VIRUS: Bennett (1944a) found a persistent but latent virus in Cuscuta californica that produced disease symptoms on sugar beets when C. californica was removed from the desert shrub, Eriogonurn fasciculaturn Benth., and grown on the beet. He named the virus "dodder latent virus" and found that it caused mottling or necrosis or both on sugar beet, 'Rockyford' cantaloupe, 'White Rose' potato, tomato, 'Early Self Blanching' celery, buckwheat, pokeweed (Phytolacca americana L. [P. decandra L.]), Sarnolus florlbundus HBK, Polygonurn pennsylvanicurn L., Plantago major L., Che- nopodium murale L., and C. album L. It also brought about temporary vein clearing in Nicotiana palrneri Gray. Other symptomless carriers of the virus were Nicotiana glauca, N. rustica vars. 'English', 'Iowa', purnila, and jamaicen- sis, Turkish tobacco, and mustard (Brassica incana (L.) F. W. Schultz). The virus was sap transmissible to Phytolacca americana and transmitted in less MECHANICS OF VIRUS TRANSMISSION 395

than 5 per cent of the seed of Cuscuta campestris. It was not found occurring naturally in economic plants. Subsequently Bennett (1944b) conveyed dodder latent virus to as high as 100 per cent of his healthy test plants by means of Cuscuta subinclusa, C. campestris, and C. californica. When he grew the three dodders on non-host plants of dodder latent virus, the virus was recovered from each dodder after periods of one to four months. Five per cent of the seed of C. campestris carried the virus, whereas the seed of the virus hosts, cantaloupe, pokeweed, and buckwheat did not. Bennett (1949) found that the virus produced marked initial disease symptoms on sugar beet, 'Golden Self Blanching' celery, Phytolacca americana, tomato, and potato, but with continued growth the plants made a quasi-complete or complete recovery. As the plants recovered, the virus concentration in them was markedly reduced. No disease symptoms were observed on Nicotiana glauca, N. rustJca, Turkish tobacco, Brassica adpressa (Moench) Boiss., Cuscuta californica, or C. campestris. Three weeks after inoculation, the virus concentration in symptomless carriers was very low compared to recently inoculated P. americana plants. Virus concentration in C. campestris rose to a high level a few days after inoculation and then declined to a low level. Testing was done by counting the number of local lesions per half-leaf of sap-inoculated P. americana. Inoculation of tomato plants (that had recovered from dodder latent virus symptoms) with tobacco etch or tobacco mosaic viruses resulted in the reappearance of persistent dodder latent virus symptoms on the young foliage of the plants, and the plants remained stunted; dodder latent virus concentration was persistently much higher than in the recovered plants con- taining only dodder latent virus. Recovered plants reinoculated with dodder latent virus remained free of disease symptoms. It was suggested that recovery was related to a restriction of virus concentration to levels too low to produced marked disease symptoms and that probably no acquired immunity resulting from production of antibodies was involved. GRAPE VINE "PANACHURE": Ochs (1958) isolated three viruses from the vine (grape) and listed them as viruses 1, 2, and 3. "Panachure" isolate (virus 1) caused a leaf mosaic in grape vine and was transmitted from tobacco to tobacco by means of Cuscuta campestris and Myzus persicae. He considered the virus to be a member of the cucumber mosaic group. Virus 2, together with 1, caused a yellow mosaic of grape vine. Virus 2 was transmissible by M. persicae but not by C. campestris. Virus 3 was associated with a stunting and deformation of grape vine and was sap-transmissible but not transmissible by means of C. campestris or M. persicae. Subsequently, Ochs (1960) found that eleven strains of the "panachure virus" were indistinguishable under the electron microscope, but they differed in the disease symptoms they produced on the grape vine and on other inoculated test plants, in serological behavior, and in transmissibility by five Cuscuta species, Myzus persicae, Otiorrhynchus sulcatus Fab., and three nematode species. FLAX CR~KI~n (Oat Blue Dwarf): Frederiksen and Goth (1959) transmitted flax crinkle by means of a Cuscuta species and the six-spotted leafhopper, 396 THE BOTANICAL REVIEW

Macrosteles fascifrons. Banttari and Moore (1962) confirmed that flax crinkle virus is identical with oat blue dwarf virus.

LETTUCE BIG-VEIN" Haeske (1958) transmitted "Blattnervenmosaik-Virus" (lettuce big-vein) to 3 of 4, 6 of 6, and 0 of 3 Lactuca scarioli L. plants by means of Cuscuta gronol,ii. His attempts to pass the virus to other lettuce species and by means of other Cuscuta species were unsuccessful. Tomlinson and Garrett (1964) were able to transmit lettuce big-vein by means of OlHdium brassicae (Wor.) Dang. zoospores and by grafting but not by C. gronovii, C. campestris, C. reflexa Roxb., C. subinclusa, or plant sap.

LUCERNE MOSAIC: Schmelzer (1956a) conveyed lucerne mosaic to 'Samsun' tobacco by means of Cuscuta campestffs, C. subindusa, C. europaea, and C. epJlinum Whe. Transmission with C. lupuliformis was successful in two of five tests. Cuscuta campestris, C. subinclusa, and C. europaea were used to carry lucerne mosaic to Nicotiana glutinosa. Cuscuta californica and C. epithymum did not transmit the virus. Baldacci et al. (1962) reported that host range studies indicated that a strain of lucerne mosaic virus could be passed as a latent virus through dodder to a symptom-expressing host, Ammi majus L.

LUCERNE WITCHEs'-BROOM: In the third annual report of the Commonwealth of Australia Scientific and Industrial Research Organization (1951), it was reported that lucerne witches'-broom was transmitted to a number of new hosts by means of Cuscuta campestris and by grafting. The hosts included tomato, potato, carrot, lettuce, petunia, Calendula, Datura stramonium, D. tatula L., Vdnca rosea, V. minor L. var. alba West, Nicotiana glutinosa, N. rustica, N. tabacum var. atropurpureum, and Crotalaria goreensis Guill. & Perr. The disease symptoms on these hosts strongly resembled those of big- bud of tomato, and it was suggested that the two diseases are caused by the same virus. Kunkel (1952) transmitted lucerne witches'-broom by means of Cuscuta campestris from lucerne to carrot, tomato, and Vinca rosea, but not to lucerne or parsley. OaT BLUE DWARF VmUS: (Flax Crinkle): Frederiksen (1962) transmitted oat blue dwarf to flax by means of dodder and Macrosteles fascifrons.

PEACH ROSETTE: Kunkel (1943a) transferred peach rosette from peach trees to tomato, Nicotiana glutinosa, and Vinca rosea by means of Cuscuta campestris.

PEACH X-DISEASE: Kunkel (1944) conveyed a virus from X-diseased peach trees to carrot, parsley, periwinkle, and tomato by means of Cuscuta campestris. The virus was readily transmitted from diseased to healthy plants of each of these species, but all attempts to take it from peach to peach or from the other species to peach were unsuccessful. Since the virus could be transmitted from X-diseased trees but not from healthy trees, it was assumed to be X-disease virus. Hildebrand (1945) transferred peach X-virus from peach MECHANICS OF VIRUS TRANSMISSION 397

seedlings to tomatoes but not from tomato to peach or from peach to peach by means of C. campestris. PEANUT STUNT: Miller and Troutman (1966) reported that a new disease of peanut (Arachis hypogaea L.), designated as peanut stunt, was transmitted from 12 peanut seedlings to 12 healthy seedlings by means of an unidentified dodder species. The symptoms of the disease resembled those of rosette, an important virus disease of peanut in Africa.

POKEWEED CRINKLE-LEAF: Lackey (1965) transmitted a new virus, pokeweed crinkle-leaf virus, from high percentages of Phytolacca americana (pokeweed) and from low percentages of symptomless sugar beets, to healthy P. americana by means of Cuscuta cali]ornica and C. campestris. The virus did not persist long in dodder.

POTATO LEAF-ROLL: Williams (1957) transferred potato leaf-roll by means of Cuscuta subinclusa from Datura stramonium to D. stramonium, from potato to D. stramonium, pepper, and potato, from pepper to D. stramonium, and from tomato to D. stramonium. The percentage of transmission was increased by heavy shading of the test plants and pruning of the bridging dodder. No transmission was obtained from infected to healthy D. stramonium using Cus- cuta campestris as a bridge. POTATO METASTOLBUR: Mi~iga (1961) transmitted potato metastolbur by means of Cuscuta campestris and C. subinclusa.

POTATO PARASTOLBUR: Mi~iga (1961) transmitted potato parastolbur by means of Cuscuta campestris and C. subinclusa. Valenta and Musil (1963) transferred parastolbur to 34 plant species in 8 families by means of dodder, grafting, and Aphrodes bicinctus. Cuscuta campestris was used to transmit the the disease from Chrysanthemum carinatum Schousb. to Lycopersicon esculen- turn. POTATO STEM-MoTTLE: Schmelzer (1955) transmitted the virus from diseased to healthy 'Samsun' tobacco plants by means of C. campestris and C. subinclusa. Both dodder species displayed a shortening of the internodes, slight curvature of the shoots, and occasional tissue necrosis when carrying the virus. Attempts to transmit the virus by means of C. californica were not successful. Van der Want (1955) transferred tobacco rattle virus from diseased to healthy asters by means of C. campestris but not by C. subinclusa. Schmelzer (1956a) conveyed stem-mottle by means of C. campestris, C. gronovii, C. lupuliformis, C. europaea, and C. subinclusa. Disease symptoms were produced on the transmitting C. lupuliformis. C. californica and C. epithymum did not transport stem-mottle. Gehring (1957) transmitted the virus to potato variety 'Saskia' by means of C. campestris. POTATO WITCHES'-BRooM: Kunkel (1943a,b) transferred potato witches'- broom to Nicotiana glutinosa, N. rustica, tomato, sugar beet, and Madagascar periwinkle (Vinca rosea) by means of Cuscuta campestris. It was reported 398 THE BOTANICAL REVIEW

at the Quebec Symposium (1952) that Cuscuta gronovii was used to transmit potato witches'-broom. Fukushi and Shikata (1955) passed potato witches'- broom from potato to 2 of 37 potato plants by means of Cuscuta japonica Choisy and to 4 of 43 potato plants and 3 of 15 red clover plants by means of Cuscuta chinensis Lain. Compared to graft-inoculated plants, symptoms were slow in appearing in the dodder-inoculated plants, particularly in the potatoes which did not show symptoms until their tubers sprouted in the season following inoculation. Mi~iga (1961) transmitted Czech potato witches'-broom by means of C. campestris and C. subinclusa. RASPBERRY (BLACK) MILD STREAK: Horn and Woods (1949) transferred mild streak of Rubus occidentalis L. (black raspberry) in 8 of 30 attempts by "dodder-grafting" with Cuscuta subincIusa from diseased to healthy black raspberry plants. RASPBERRY MOSAIC COMPLEX: A raspberry mosaic that causes yellow or light green mosaic, ring-spot mottle, and oak-leaf pattern on wild Himalayan raspberry (Rubus ellipticus Smith) was transmitted from this host back to R. ellipticus by means of Cuscuta reflexa, inarch-grafting, and bottle graft (Azad and Sehgal 1958). STRAWBERRY GREEN-PETAL (CLovER PHYLLODY): Frazier and Posnette (1956) transmitted strawberry green-petal from clover to strawberry and Duchesnea indica (Andr.) Focke by means of Cuscuta subinclusa. They suggested that the virus might be a strain of aster-yellows virus. Frazier and Pos- nette (1957) passed strawberry green-petal from a mixture of strawberry green-petal and clover witches'-broom in clonal plants of white clover to Fragaria vesca L. and Duchesnea indica by means of C. subinclusa and C. campestris. Attempts to transmit either virus using Cuscuta europaea were unsuccessful. Mi~iga et al. (1960) transferred the clover phyllody virus by means of leafhoppers, grafting, C. campestris, and C. subinclusa to Trifolium repens, T. hybridum L., T. pratense L., Faba vulgaris Moench, Vinca rosea, Lycopersicon esculentum (Solanum lycopersicum), Nicotiana rustica, N. tabacum, Datura stramonium, Senecio vulgaris, Calendula o~cinalis, Chrysan- themum carinatum, and Taraxacum o~cinale Web. Mi~iga (1961) transmitted green-petal by means of C. campestris and C. subinclusa. Chiykowski (1962) transferred green-petal from Vinca rosea to V. rosea by means of Cuscuta gronovii. STRAWBERRY MOTTLE: Carver (1963) transmitted strawberry mottle by means of a Cuscuta species. STRAWBERRY VEIN-BANDING: Frazier (1955) conveyed strawberry vein-banding by means of Cuscuta subinclusa. TOBACCO ETCH: Bennett (1944b) transmitted tobacco etch from infected to healthy Turkish tobacco by means of Cuscuta californica but not by C. subinclusa or C. campestris. When C. californica with tobacco etch was grown on non-host plants of tobacco etch, this malady was recovered from the dodder MECHANICS OF VIRUS TRANSMISSION 399

for a period of two to four weeks. Schmelzer (1956a) transferred tobacco etch by means of Cuscuta lupuliformis but not with C. campestris, C. subinclusa, C. europaea, C. epilinslm, C. californica, or C. epithymum. TOBACCO MOSAIC: Johnson (1942a,b) conveyed tobacco mosaic (TMV) to 13 of 26 plants in 26 days by means of Cuscuta campeslris. He suggested that the virus does not multiply in dodder. Bennett (1944b) transmitted tobacco mosaic to a small percentage of tobacco plants by means of Cuscuta subinclusa and C. campestris but not by C. califor~ica. Costa (1944) transported both tobacco mosaic and a strain of tobacco mosaic (tomato mosaic) from tomato to tomato and tobacco by means of Cuscuta campestris, but was unable to make the transfer if the dodder from the virus-infected tomatoes was grown on virus-immune lucerne or crimson clover and then on tomato or tobacco. From this he concluded that the tobacco mosaic virus does not persist in the dodder. In two separate experiments Cochran (1946) connected TMV- infected tomato plants growing in bright light to healthy plants growing in the shade (starved for carbohydrates) by means of Cuscuta campestris. After connection he removed the extra (unconnected) growing points of C. campestris. Tobacco mosaic disease symptoms developed in 75 and 83 per cent of the starved hosts, compared to 0 and 3 per cent in the unshaded control plants. He suggested that under these "forced" conditions the virus moved with the carbohydrate from the infected tomatoes through the dodder to the healthy plants. Miyakawa and Yoshii (1951) transmitted tobacco mosaic to 11 of 54 host plants by means of Cuscuta japonica. As ascertained by the local- lesion method on NicotJana glutinosa, the active virus concentration of the press-juice of the dodder stem parasitizing the diseased tobacco plant was low compared with that of the diseased host. The active concentration increased when the dodder juice was diluted. A virus inhibitor, relatively stable to heat and soluble in alcohol, was demonstrated in the healthy dodder juice. Dilution of the dodder juice was believed to effect a reduction in in- hibition. Schmelzer (1956a) transmitted tobacco mosaic more successfully by means of C. campestris during the period of November to February than in spring or summer. He found the amounts of tobacco mosaic in C. campestris to be greatest during the winter. Jensen (1963) determined that although displaying no disease symptoms, C. campestris growing on tobacco mosaic-infected Nicotiana tabacum acquired enough virus particles to make possible the identification of the virus in the dodder by infectivity, sedimen- tation rate, and electron-microscope studies, and to demonstrate that the virus moved through the dodder in the form of particles as large as the tobacco mosaic nucleo-protein. From the above one might hypothesize a passive movement of the tobacco mosaic virus through the dodder and an inactivation of the virus by an inhibitor in the dodder sap. When quantitative movement of the virus exceeds inactivation, transmittance might occur. TOBACCO STREAK: The Kentucky Agricultural Experiment Station (1942) reported transmission of tobacco streak from tobacco to sweet clover (MelJlotus sp.) and from sweet clover to tobacco by means of dodder. 400 THE BOTANICAL REVIEW

TOMATO BIG-BUD (SEE ALSO LUCERNE WITCHES'-BROOM): Kunkel (1951) transmitted a virus causing bolting symptoms on carrots from bolted to healthy carrots by means of Cuscuta campestris. Since the symptoms were similar to but milder than those produced by tomato big-bud virus on carrot, he suggested that the disease was caused by a mild strain of tomato big-bud virus. Hill and Mandryk (1954) passed tomato big-bud from tobacco to tobacco, tomato, Nicotiana glutinosa, N. rustica, beet, and Vinca rosea by means of C. campestris. Migiga and Valenta (1957) made a low percentage of trans- missions of tomato big-bud (tomato stolbur) from naturally or experimentally infected Convolvulus arvensis L. and Lycopersicon esculentum (Solanum lycopersicum) to Trifolium repens, T. hybridum, Vinca rosea, Lycopersicon esculentum, and Nicotiana tabacum by means of Cuscuta campestris, C. trifolii Babingt. & Gibs., and C. epilinum. Valenta (1958) transferred Crimean- yellows, possibly a strain of tomato stolbur (big-bud), by means of C. cam. pestris to other plants. The virus produced a typical yellows disease and floral abnormalities in C. campestris. Mi~iga (1961) transmitted tomato stolbur by means of C. campestris and C. subinclusa. Valenta, Mi~iga, and Musil (1961) passed stolbur from Convolvulus arvensis to Trifolium hybridium and Lycopersicon esculentum, from L. esculentum to Vinca rosea and Nicotiana tabacum, from N. tabacum to L. esculentum and N. tabacum, from V. rosea to V. rosea and L. esculentum by means of Cuscuta campestris; from L. esculentum to Trifolium repens, L. esculentum, and N. tabacum, from N. tabacum to T. repens and Vinca rosea by means of Cuscuta trifolii; and from N. tabacum to T. repens by means of Cuscuta epilinum. Transmission rates were low and incubation periods were generally very long. They suggested that the concentration of the virus in dodder remains at a low level. The virus persisted in the dodder through consecutive transfers of dodder to healthy hosts. The Queensland Department of Agriculture and Stock (1962) reported that yellow-crinkle of papaw was carried to tomato by means of Cuscuta australis, and that the disease symptoms on tomato were typical of big-bud of tomato. Caudwell (1965) observed disease symptoms in Vinca rosea very similar to those caused by stolbur and parastolbur; in Cuscuta europaea and C. monogyna Auct. the disease symptoms appeared as a marked development of the gynophore and sterility of the flowers. The gynophore finally developed into almost normal shoots that differed by having floral whorls at the base. TOMATO BUSHY-STUNT: Johnson (1941a,b) transmitted tomato bushy-stunt to 5 of 20 plants by means of Cuscuta campestris in 23 days. TOMATO SPOTTED-WILT: Bennett (1944b) transmitted tomato spotted-wilt to low percentages of healthy plants by means of Cuscuta subinclusa, C. campestris, and C. californica. Jones (1959) passed tomato spotted-wilt from Tropaeolum majus L. to T. majus via C. campestris. Schmelzer (1956a) transferred tomato spotted-wilt to Nicotiana glutinosa by Cuscuta californica. TURNIP MOSAIC: Bennett (1944b) transmitted turnip mosaic to high percent- MECHANICS OF VIRUS TRANSMISSION 401

ages of test plants by means of Cuscuta cali/ornica, but he found that C. subinclusa and C. campestris were not so effective. When the three dodders were transferred from virus-infected host plants to non-hosts of the virus, the virus was recovered from the dodders after twenty but not after forty days. VACCINIUM FALSE-BLOSSOM: Kunkel (1942, 1943c) conveyed cranberry false- blossom to Vinca rosea, potato, tomato, tobacco, and Nicotiana glutinosa and from tomato to cranberry by means of Cuscuta campestris. Costa (1944) found that cranberry false-blossom virus remained in C. campestris plants that were transferred through six consecutive lucerne (dodder host) plants that were immune to the virus. Kunkel (1945) transferred vaccinium (cranberry) false-blossom by means of C. campestris and grafting but not by Macrosteles divisus Uhler or dodder seed. He proposed that cranberry false-blossom might be related to tomato big-bud in the United States and Australia, stolbur in the USSR, and little-leaf of eggplant in India. Using C. campestris he transferred the virus from cranberry to 28 plant species in 10 plant families. The species were Dianthus sp. var. 'Crown of Perfection' in the Caryophyllaceae; Eschscholtzia californica Chain. in the Papaveraceae; Pastinaca sativa L. (parsnip), Apium graveolens L. (celery), Petroselinum hortense Hoffm. (parsley), Daucus carota (carrot), all in the Umbelliferae; Vaccinium macrocarpon (cranberry) in the Ericaceae; Vinca rosea (periwinkle) in the Apocynaceae; Phlox drummondii Hook. in the Polemoniaceae; Petunia hybrida, Nierembergia frutescens Dur., Schizanthus sp., Salpiglossis sp., Lycopersicon esculentum (tomato), Nicotiana tabacum (Turkish tobacco), N. glutinosa, N. langsdor~i Schrank, N. rustica, Solanum tuberosum, all in the Solanaceae; Veronica peregrina L. in the Scrophulariaceae; Scabiosa atropurpurea L. in the Dipsacaceae; Dimorphotheca aurantiacum DC. (African daisy), Brachycome iberidifolia Benth. (Swan River daisy), Centaurea imperialis Hort., Gaillar- dia aristata Pursh, Tagetes erecta L. (African marigold), Calendula officinalis, and Tragopogon porrifolius L. (salsify), all in the Compositae. Other similarly treated plants did not acquire the virus. These were Begonia sp. in the Begoniaceae, Prunus persica (peach) in the Rosaceae, Medicago sativa (alfalfa) in the Leguminosae, and Callistephus chinensis (China aster) in the Compositae. Cuscuta campestris conveyed the disease back from Vinca rosea and tomato to cranberry, and when growing on plants immune to cranberry false-blossom virus retained the virus over a two-year period. The virus appeared to multiply in the dodder. VACCINIUM STUNT: Hutchinson et al. (1960) transmitted vaccinium (blue- berry) stunt from wild species of blueberries (Vaccinium corymbosum and V. atrococcum (Gray) Heller) to Vinca rosea by means of Cuscuta subinclusa. VINCA YELLOWS: Maramorosch (1956) transferred vinca yellows from Vinca rosea to carrot by means of C. subinclusa, He considered the disease to be a yellows type distinct from aster yellows. 402 THE BOTANICAL REVIEW

ACKNOWLEDGMENTS This review was begun while I was at the University of Arizona, nearly com- pleted at the University of Florida, and finished at North Dakota State Univer- sity. I am most grateful to Drs. G. A. Gries and Milton Zaitlin for encouraging, advising, and reviewing the preparation of the article. 1 wish especially to thank Dr. C. W. Bennett for his continuous reviewing of and advising on the many stages of the manuscript. I wish to thank Dr. Larry Littlefield for reviewing the article, Dr. Roland Timian for help with several viruses, Dr. O. A. Stevens for aid in finding authorities for Cuscuta species, Dr. J. T. Schulz for the correct naming of some insect species, Mrs. Kathy Stokes of the University of Florida Hume Library for obtaining many of the citations, Mrs. Peggy A. Jones and Mrs. Annabelle Salano for repeated typing of the manuscript, Mrs. Colleen Nelson for typing portions of the paper, and my wife, Mrs. Sylvia L. Hosford, for encouraging its completion.

LITERATURE CITED AZAD, R. N., and O. P. SEHOAL. 1958. Some virus diseases of temperate fruits, Indian Phytopath. 11: 159-164. BALDACCI, E., el al. 1962. Nuovi contributi alle rieerehe sulle malattie da virus della Vite. (English summary.) Riv. Pat. Veg., Pavia, Ser. 3, 2(1): 20-25. (Rev. Appl. Mycol. 41: 692.) BANTTARb g. E., and M. 13. MOORE. 1962. Virus cause of blue dwarf of oats and its transmission to barley and flax. Phytopathology 52: 897-902. BAWDEN, F. C. 1956. Plant viruses and virus diseases. Chroniea Botanica Company, Waltham, Mass., pp. 59-60. 1964. Plant viruses and virus diseases. Ronald Press Company, New York, pp. 88, 92, 284. BEISS, U. 1956. Untersuchungen fiber den Wirtspflanzenbereieh der Vergilbungsvirus der Beta-Rfiben (Corium betae). (Studies on the host plant range of the yellows virus of Beta beets [Corium betae].) Phytopath Zeitschr. 27(1): 83-106. BEr~NETr, C. W. 1940. Acquisition and transmission of viruses by dodder (Cuscuta subinclusa). (Abstr.) Phytopathology 80: 2. 1944a. Latent virus of dodder and its effects on sugar beet and other plants Phytopathology 84: 77-91. . 1944b. Studies of dodder transmission of plant viruses. Phytopathology 34: 905-932. , 1949. Recovery of plants from dodder latent mosaic. Phytopathology 89: 637-646. 1955. Recovery of water pimpernel from curly top and the reaction of recovered plants to reinoculation with different virus strains. Phytopathology 45: 531-536. 1956. Biological relations of plant viruses. Ann. Rev. Plant Phys. 7: 143- 170. . 1957. Interactions of sugar beet curly top virus and an unusual mutant. Virology 3: 322-342. . 1960. Sugar beet yellows disease in the U.S. U.S. Dep. Agr. Teeh. Bull. 1218, 63 pp. ., and A. S. COSTA. 1949. Tristeza disease of citrus. Jour. Agr. Res. 78: 207-237. , and J. E. Durvus. 1957. Rosette disease of sugar beet. Plant Dis. Rep. 41: 1001-1004. MECHANICS OF VIRUS TRANSMISSION 403

, and C. MUNCK. 1946. Yellow wilt of sugar beet in Argentina. Jour. Agr. Res. 73(2) : 45-64. Bos, L., et al. 1959. Investigations on white clover mosaic virus Tijdschr. Planteziek. 6.5: 89-106. , en P. GRANCINI. 1963. Een eigenaardige enatie-virusziekte bij witte klaver. (A strange enation virus disease in white clover.) Tijdschr. Planteziek. 69: 151. (Rev. Appl. Mycol. 42: 723.) BRIERLEY, P., and F. F. SMITH. 1957. Symptoms of chrysanthemum flower distortion, dodder transmission of the virus, and heat cure of infected plants Phyto- pathology 47: 448-450. CANOVA, A. 1955. Rapporti tra Cuscuta e virus del diallume della Barbabietola. (The relationships between dodder and beet yellows virus.) (English summary Ann. Sper. Agr., N. S., 9(3) : 549-552. (Rev. Appl. Mycol. 8.5: 804.) CARVER, R. G. 1963. A study of the strawberry viruses in Louisiana. Diss. Abstr. 23 (11): 4078-4079. CAUDWELL, A. 1965. Note sur un virus provoquant des prolif4rations des fleurs de cus- cutes. (Note on a virus causing proliferation of dodder flowers.) Ann. Epiphy- ties 16(1) : 77-81. CHIYKOWSKI, L. N. 1962. Clover phyllody virus in Canada and its transmission. Can. Jour. Bot. 40: 397-404. COCHRAN, G W. 1946. The effect of shading techniques on transmission of tobacco mosaic virus through dodder. Phytopathology 36: 396. 1947. The "dodder graft," a new method of using dodder to transmit plant viruses. Phytopathology 37: 5. COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANIZATION. 1951. Third annual report for the year ending 30th June, 1951. Canberra, Australia, 167 pp. (p. 18.) COSTA, A. S. 1944. Multiplication of virus in dodder, Cuscuta cam~estrls. Phytopathol- ogy 34: 151-162. FRAZIER, N. W. 1955. Strawberry vein banding virus. Phytopathology 45: 307-312. , and A. F. POSNEXTE. 1956. Leafhopper transmission of a clover virus causing green petal disease in strawberry. Nature 177: 1040-1041. , and . 1957. Transmission and host-range studies of strawberry green-petal virus. Ann. Appl. Biol. 45: 580-588. FREDERIKSEN, R. A. 1962. Studies on the transmission, effect and control of two viruses on Linum usitatissimum L. Diss. Abstr. 22: 3800-3801. , and R. W. GOTH. 1959. Crinkle, a new virus disease of flax. (Abstr.) Phytopathology 49: 538. FUCHS, W. M., und U. BEISS. 1954. Obertragung der Riibengelbsucht-Virus (Corium betae) mit Hilfe von Cuscuta. (Transmission of sugar beet yellows virus [Corium betae] with the aid of Cuscuta.) Naturwissenschaften 41(21): 506. FU:~USHI, T., and E. SHIKATA. 1955. Transmission of potato witches broom by the dodders, Cuscuta jal~onica Chois. and C. chinensis Lain. (Japanese, with English summary.) Mem. Fac. Agr. Hokkaido Univ. 2(3) : 47-51. FULTON, R. W. 1964. Transmission of plant viruses by grafting, dodder, seed, and me- chanical inoculation. In: "Plant Virology," ed. by M. K. Corbett and H. D. Sisler. Univ. Florida Press, Gainesville, pp. 42-44, 60-61. GEHRING, F. 1957. Uber ein Auftreten des Strengelbuntvirus der Kartoffel in Deutsch- land. (On an occurrence of potato stem mottle virus in Germany.) Nachricht- enbl. Deut. Pflanzenschutzdienstes (Braunschweig), Stuttgart, 9: 172-174. (Rev. Appl. Mycol. 37: 245.) GInDINGS, N. J. 1947. Dodder as an aid in testing some plant species for curly-top virus. Phytopathology 37: 278-280. GUALACCINI, F. 1956. Transmissibilita del virus producente il mosaico del Peperone, mediante la Cuscuta, e prove di identificazione di esso. (Transmissibility of the virus causing chilli mosaic by means of Cuscuta, and tests of its identification.) 404 THE BOTANICAL REVIEW

(English summary.) Boll Sta. Pat. Veg. Roma, Ser. 3(1955), 13: 79-101 (Rev. Appl. Mycol. 36: 81-82.) HAESKE, ERHARD. 1958. Untersuchungen fiber das Blattnervenmosaik des Salats. Doc- toral Dissertation, Justus Liebig Universitat, Giessen, 86 pp. HILrmBRANO, E. M. 1945. The dodder vector of woody plant viruses. Plant Dis. Rep. 29: 196-197. HILL, A. V., and M. MANDRYK. 1954. A study of the virus diseases "big bud" of tomato and "yellow dwarf" of tobacco. Australian Jour. Agr. Res. 5: 617-625. HOLUNGS, M. 1960. Chrysanthemum. Glass House Crops Res. Inst. 1959 Ann. Rep., Littlehampton (Sussex), England, pp. 67-68. HORN, N. L., and M. W. WooDs. 1949. Transmission of the mild streak virus of black- raspberry Phytopathology 39(5) : 377-385. HUTCHINSOn, M. T., et al. 1960. Wild sources of blue-berry stunt virus in New Jersey Phytopathology 50: 308-312. JENSE~, S. G. 1963. Studies on infection and systemic spread of plant viruses Diss. Abstr. 23: 2672-2673. JOHNSOg, F. 1941a. Transmission of viruses by the parasitic activities of dodder Phyto- pathology 31: 13. . 1941b. Transmission of plant viruses by dodder Phytopathology 13: 649-656. JoN~s, J. P. 1959. Failure of thrips to transmit an isolate of tomato spotted wilt virus. Phytopathology 49: 452-453. KELt.ER, J. R. 1953. Investigations on chrysanthemum stunt virus and chrysanthemum virus. Quart. Mem. Cornell Agr. Exp. Sta. 324, 33 pp. KENTUCKY AGRICULTURAL EXPERIMENT STATION. 1942. Fifty-fourth Annual Report for the year 1941, p. 15. KUNKEL, L. O. 1942. False blossom in periwinkles and its cure by heat. Science, N. S., 95(2642): 252. 1943a. New hosts as a key to progress in plant virus disease research. In: "Plant Virus Diseases," Cornell University Press, 170 pp. (pp. 63-82). 1943b. Potato witches-broom transmission by dodder and cure by heat. Proc. Amer. Phil. Soc. 86: 470-475. . 1943c. Transmission of cranberry false blossom from tomato to cranberry plants by dodder (Cuscula cam~eslris). Phytopathology $3: 19. 1944. Transmission of virus from X-diseased peach trees to herbaceous plants. Phytopathology 34: 1006. 1945. Studies on cranberry false blossom. Phytopathology 3.5: 805-821. .. 1950. Asclepias yellows. Phytopathology 40: 16. . 1951. Identification of bolting disease of carrots. Phytopathology 41: 22. 1952. Transmission of alfalfa witches broom to nonleguminous plants by dodder, and cure in periwinkle by heat. Phytopathology 42: 27-31. LACKEY, C. F. 1941. Histological studies on the relationship of dodder to healthy and curly-top-infected sugar beets and tobacco. Phytopathology 31: 861. .. 1946. Reactions of dodders to stems of other dodders and their own stems. Phytopathology 36: 386-388. 1965. Pokeweed crinkle leaf, caused by a virus transmitted by dodder from desert shrubs in Southern California. Plant Dis. Rep. 49(12): 1002-1005. , and C. W. BENNETr. 1949. Pathological effects of curly-top virus on dodder. Phytopathology 39: 860 MARAMOROSCH, K. 1956. Vinca yellows in Mexico. Plant Dis. Rep. 40: 1109-1111. . 1963. Corn stunt virus transmission and attenuation in a new host. Phy- topathology 53: 350. MILLER, L. I., and J. L. TROUTMAN. 1966. Stunt disease of peanuts in Virginia. Plant Dis. Rep. ,50: 139-143. MIIIGA, S. 1961. Prenos niektor~ch ~lta~:kovS"ch virusov kuku~finou. (Transmission of MECHANICS OF VIRUS TRANSMISSION 40~

some yellows-type viruses of dodder.) (Russian, German summary.) Biol6gia, Bratislava, 16(5): 340-350. (Rev. Appl. Mycol. 48: 244.) , et al. 1960. Niektor~ hostitel'sk6 rastliny virusu zelenokvetosti dataliny. (Some host plants of the clover phyllody virus.) (English summary.) Biol6gia, Bratislava, 15(7) : 538-542. , and V. VALENTA. 1957. Prenos virusu stolburu prostrednictvom nietor)~ch druhov kuku?:in. (Transmission of stolbur virus with the aid of some species of dodder.) (English summary.) Biol6gia, Bratislava, 12(9): 652-660. MXYAKAWA, T., and H. YosmI. 1951. Transmission of tobacco mosaic virus by the dodder, Cuscuta japonica and its inhibitory effect on the virus activity. (Jap- anese, with English summary.) Sci. Bull. Fac. Agr. Kyushu Univ. 12: 143-154. MOKRA, VERA. 1964. Studie o virov~ povaze zelenokvetosti Primuli. (Studies on the green petal virus disease of primroses.) (English summary.) Rozpravy Ces- koslovenske Akad. Ved. 74(3), 37 pp. Moo/-BoK, M. 1949. Uit de literatuur. Het overbrengen van viren met behulp van Cuscuta-soorten. (Review of current literature on the transmission of viruses by means of Cuscuta species.) Tijdschr. Planteziek. 55: 31-38. OCHS, GERTRUDE. 1958. Uber drei Viren als Erreger von Rebkrankheiten. (Concerning three viruses as agents of vine diseases.) Zeitschr. Pflanzenkrankh. 65(1) : 11-17. 1960. Uber elf Stamme des Panachfirevirus der Weinrebe. (On eleven strains of the "panachure" virus of vine.) (In German.) Phyton, Vicente Lopez, 14(1) : 1-11. PRATT, M. J. 1961. Studies on clover yellow mosaic and white clover mosaic virus. Can. Jour. Bot. 39: 655-665. PRICE, W. C. 1963. The nature of virus diseases of citrus and their interrelationships with other plant virus diseases. Florida Agr. Exp. Sta. Ann. Rep., pp. 148-149. PROTSESKO, A. E. 1958. The relation between tomato stolbur (Leptomotropus solanl) and aster yellows (L. callistephi). Vopr. Virusol. (USSR) 3(5): 292-296. 1959. Electron microscopy of the aster yellows virus (Leptomotropus callistephi Ryzhkov). Biol. Plant Acad. Sci. Bohenosl 1(3) : 187-191. QUEBEC SOCIETY FOR THE PROTECTION OF PLANTS,. 1952. Symposium--Viruses and the protection of the plant kingdom. Supplement to 34th Ann. Rep., p. 92. QUEENSLAND, DEPARTMENT or AGRICULTURE AND STOCK. 1962. 1961-1962 Report (Bris- bane), pp. 23-25. RAYCltAUDHURI, S. P. 1953. Studies on bayberry yellows. Phytopathology 48: 15-20. SAKXMURA, K. 1947. Virus transmission by Cuscuta sand~ichiana. Phytopathology 87: 66-67. SCHMELZER, K. 1955. Die Obertragbarkeit des Tabakmauche-Virus dureh Cuscuta- Arten. (The transmissibility of the tobacco stem mottle virus by species of Cus- cuta.) Naturwissenschaften 42: 19. . 1956a. Beitr/ige zur Kenntnis der r yon Viren durch Cus- cuta-Arten. (Contributions to the knowledge of the transmissibility of virus by Cuscula species.) Phytopath. Zeitschr. 28: 1-56. . 1956b. Beitr/ige zur Kenntnis der Virushemmstoffe in Cuscuta-Arten. (Contributions to the knowledge of virus-inhibitors in Cuscuta-species.) Zentralbl. Bakt., II, 109(20-22): 482-515. (Rev. Appl. Mycol. 35: 173.) . 1957. Versuehe zur l~bertragung des Tomatensasperme-Virus mit Cuscuta- Arten. (Experiments on the transmission of tomato aspermy virus by Cuscuta species.) Phytopath. Zeitschr. 30: 449-452. . 1962. (Studies on viruses of ornamental and wild woody plants 2nd Part. Viroses of Forsythia, Lonicera, Ligustrum, and Laburnum.) (German, English summary.) Phytopath. Zeitschr. 48(2) : 105-138. SIBILIA, C. 1951. Le euscute e le virosi. Boll. Staz. Pat. Veg., Roma, Serie terza, 7: 205-215. THOIIAV (SYKES), MARY G. 1911. On the histological relations between Cuscuta and its host. Ann. Bot. 25: 655-682. 406 THE BOTANICAL REVIEW

T~UNC, T. H., en T. HADIWlDJAJA. 1950. Het overbringen van viren met behulp van Cuscuta australis R. Br., 1. (The transmission of viruses with the aid of Cus- cuta australis R. Br., 1.) (English summary.) Tijdschr. Planteziek. 56: 349-351. TXMIAN, R. G. 1964. Dodder transmission of barley yellow dwarf virus. Phytopathology 54: 910. TOMLINSON, J. A., and R. G. GARRETT. 1964. Studies on the lettuce big-vein virus and its vector Olpidium brassicae (Wor.) Dang. Ann. Appl. Biol. 54: 45-61. VALENTA, V. M. 1958. A new yellows virus causing flower proliferations in the dodder, Cuscuta campestris Yunck. Phytopath. Zeitschr. 33: 316-318. , S. MI~IGA, and M. MUSlL. 1961. Investigations on European yellows-type viruses. I. The stolbur virus. Phytopath. Zeitschr. 42: 1-38. , and M. MUSIL. 1963. Investigations on European yellows-type virus. II. The clover dwarf and parastolbur viruses. Phytopath. Zeitschr. 47(1): 38-65. VAN OER WANT, J. P. H. 1955. Transmission of tobacco-rattle virus by means of dodder. Plant Dis. Rep. 89: 553-554. VAN VELSEN, R. J., and N. C. CROWLEY. 1961. Centrosema mosaic: a plant virus disease transmitted by both aphids and plant bugs. Nature 189: 858. WEATHERS, L. G. 1965. Transmission of exocortis virus of citrus by Cuscuta subinclusa. Plant Dis. Rep. 49(3) : 189-190. , and M. K. HARJUNG. 1964. Transmission of citrus viruses by dodder, Cuscuta subinclusa. Plant Dis. Rep. 48(2) : 102-103. , and F. C. GREER. 1965. Dodder as a means of transmitting citrus viruses. Calif. Citrograph 51(2) : 83-84. WII,LIAM$~ W. L. 1957. Experiments on the transmission of potato leaf roll virus. Diss. Abstr. 17 : 2784-2785. YAXWOOD, C. E. 1955. Meehanical transmission of an apple mosaic virus. Hilgardia 23(15) : 613-628.