Pathogen strains and leafhopper species as factors in the transmission of western x-disease agent under varying light and temperature conditions
AuthorsRoger E. Gold
Edward S. Sylvester
Authors AffiliationsRoger E. Gold was a former graduate student, Department of Entomological Sciences, University of California, Berkeley, is Coordinator, Environmental Programs and Associate Professor of Entomology, Institute of Agriculture and Natural Resources, University of Nebraska, Lincoln; Edward S. Sylvester was Professor, Department of Entomological Sciences, University of California, Berkeley.
Hilgardia 50(3):1-43. DOI:10.3733/hilg.v50n03p043. June 1982.
The data base on transmission of western X-disease agent (WXDA) by Colladonus montanus leafhoppers was expanded in studies using celery, Apium graveolens as the host. Transmission was affected or limited by the availability threshold, instar efficiency, and acquisition and inoculation rates, along with vector biotype and pathogen strain. Transmission also was moderated by circadian rhythms. Serial passage by injection of the pathogen into a sequence of healthy insects was accomplished, and some evidence was obtained that tetracycline pressure during serial passage could result in selection of a tetracydine-resistant strain of the pathogen. Leafhoppers did not become infectious by membrane-feeding during trials made to concentrate or purify the WXDA.
Comparative tests using C. geminatus, C. montanus, and Euscelidius variegatus indicated C. montanus was the most, and E. variegatus the least, efficient experimental vector. Simultaneous feeding of the three species on a common disease source reduced vector longevity. Transmission efficiency was temperature sensitive. At 30 C, transmission by any species was rare. Comparisons at 20 and 25 C resulted in similar acquisition rates. The median latent period and longevity of both Colladonus species decreased at higher temperatures. Euscelidius variegatus however, apparently was not affected by the pathogen and survived longer at 25 C than at 20 C. When inoculated by injection, C. geminatus was a more efficient vector than E. variegatus under insectary conditions, but the reverse was true under conditions of constant light and temperature.
A fourth leafhopper species, Fieberiella florii was similar to C. montanus in acquisition efficiency and transmission of the WXDA, but it had a longer developmental time; thus, transmission could occur in the nymphal stage. The median latent period of the pathogen in F. florii, following inoculation by injection, was half of that when infectivity was established by feeding.
Amin P. W. Western X-disease of peach: Its etiology and effects on the physiology of its vector, Colladonus montanus (Van Duzee) (Homoptera, Cicadellidae) 1971. p.119. Ph.D. Thesis, University of California, Berkeley
Amin P. W., Jensen D. D. Effects of tetracycline on the transmission and pathogenicity of the western X disease agent in its insect and plant hosts. Phytopathology. 1971a. 61:696-702. DOI: 10.1094/Phyto-61-696 [CrossRef]
Amin P. W., Jensen D. D. The effect of western X-disease on the oxygen consumption of its leafhopper vector, Colladonus montanus. J. Invertebr. Pathol. 1971b. 18:109-13.
Anthon E. W., Wolfe H. R. Additional insect vectors of western X-disease. Plant Dis. Rep. 1951. 35:345-46.
Auclair J. L. Honeydew excretion in the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera: Aphididae). J. Insect Physiol. 1958. 2:330-37.
Bald J. G., Samuel G. Investigations on “spotted wilt” of tomatoes. —II. C.S.I.R.O. Australia Bull.:. 1931. 54:24
Banks C. J., Nixon H. L. The feeding and excretion rates of Aphis fabae Scop. on Vicia fabae L. Entomol. Expt. &; Appl. 1959. 2:77-81.
Bennett C. W., Wallace H. E. Relation of the curly top virus to the vector, Eutettix tenellus. J. Agric. Res. 1938. 56:31-51.
Björling K., Ossiannilsson F. Investigations on individual variations in the virus transmission ability of different aphid species. Socker Handlll. 1958. 14:1-13.
Black L. M. Genetic variation in the clover leafhopper’s ability to transmit potato yellow-dwarf virus. Genetics. 1943. 28:200-09.
Carter W. A technic for use with homopterous vectors of plant disease, with special reference to the sugar-beet leafhopper, Eutettix tenellus (Baker). J. Agric. Res. 1927. 34:449-51.
Chalfant R. B., Chapman R. K. Transmission of cabbage viruses A and B by the cabbage aphid and the green peach aphid. J. Econ. Entomol. 1962. 55:584-90.
Chamberlain R. W. Arboviruses, the arthropod-borne animal viruses. Current Topics Microbiol. Immunol. 1968. 42:38-58. DOI: 10.1007/978-3-642-46115-6_3 [CrossRef]
Chen T. A., Liao C. H. Corn stunt spiroplasma: isolation, cultivation, and proof of pathogenicity. Science. 1975. 188:1015-17. DOI: 10.1126/science.188.4192.1015 [CrossRef]
Cook P. P. Jr., Sylvester E. S. Diurnal fluctuations in nonpersistent virus transmission by aphids. J. Econ. Entomol. 1964. 57:536-38.
Day M. F., Irzykiewicz H. Feeding behaviour of the aphides Myzus persicae and Brevicoryne brassicae, studied with radio-phosphorus. Aust. J. Biol. Sci. 1953. 6:98-108.
Day M. F., McKinnon A. A study of some aspects of the feeding of the jassid Orosius. Aust. J. Sci. Res., Ser. B. 1951. 4:125-35.
Doi Y., Teranaka M., Yora K., Asuyama H. Mycoplasma- or PLT group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches’ broom, aster yellows, or paulownia witches’ broom. Ann. Phytopathol. Soc. Japan. 1967. 33:259-66. DOI: 10.3186/jjphytopath.33.259 [CrossRef]
Duffus J. E., Gold A. H. Relationship of tracer-measured aphid feeding to acquisition of beet western yellows virus and to feeding inhibitors in plant extracts. Phytopathology. 1967. 57:1237-41.
Frazier N. W. Xylem viruses and their insect vectors. Proc. Intern’l. Conf. on Virus and Vector on Perennial Hosts, with Special Reference to Vitis 1966. pp.91-99. Sept. 6-10, Davis, California. 1965.
Frazier N. W., Jensen D. D. Strawberry, an experimental host of peach western X-disease. Phytopathology. 1970. 60:1527-28. DOI: 10.1094/Phyto-60-1527 [CrossRef]
Gilmer R. M. Insect transmission of X-disease virus in New York. Plant Dis. Rep. 1954. 38:628-29.
Gilmer R. M. Recovery of X-disease virus from naturally infected milkweeds. Phytopathology (Abstr.). 1960. 50:636
Gilmer R. M., Palmiter D. H., Schaefers G. A., McEwen F. L. Leafhopper transmission of X-disease virus of stone fruits in New York. New York State Agric. Exp. Stn. Bull. 1966. 813:22
Gilmer R. M., Blodgett E. C. X-disease. Virus Diseases and Noninfectious Disorders of Stone Fruits 1976. pp.145-55. USDA Handbook No. 437, 433 pp. DOI: 10.1586/14737126.96.36.1999 [CrossRef]
Gold R. E., Maramorosch K., Harris K. F. Leafhopper vectors and western X disease. Leafhopper Vectors and Plant Disease Agents. 1979. New York: Academic Press. p. 587-602. 654p.
Govier D. A., Kassanis B. Evidence that a component other than the virus panicle is needed for aphid transmission of potato virus Y. Virology. 1974. 57:285-86.
Granett A. L., Gilmer R. M. Mycoplasmas associated with X-disease in various Prunus species. Phytopathology. 1971. 61:1036-37.
Hamilton M. A. Further experiments on the artificial feeding ofMyzus persicae (Sulz.). Ann. Appl. Biol. 1935. 22:243-58.
Hamner K., Hoshizaki T. Photoperiodism and circadian rhythms: an hypothesis. BioScience. 1974. 24:407-14. DOI: 10.2307/1296912 [CrossRef]
Hildebrand E. M. The dodder vector of woody plant viruses. Plant Dis. Rep. 1945. 29:196-97.
Huang J., Nyland G. The morphology of a mycoplasma associated with peach X-disease. Phytopathology (Abstr.). 1970. 60:1534
Ishii T., Doi Y., Yora K., Asuyama H. Suppressive effects of antibiotics of tetracycline group on symptom development of mulberry dwarf disease. Ann. Phytopathol. Soc. Japan. 1967. 33:267-75. DOI: 10.3186/jjphytopath.33.267 [CrossRef]
Jensen D. D. Leafhopper-virus relationships of peach yellow leaf roll. Phytopathology. 1953a. 43:561-64.
Jensen D. D. Longevity of the leafhoppers, Colladonus geminatus (Van Duzee) and Colladonus montanus (Van Duzee) on peach. J. Econ. Entomol. 1953b. 46:1120-21.
Jensen D. D. Insect transmission of virus between tree and herbaceous plants. Virology. 1956. 2:249-60. DOI: 10.1016/0042-6822(56)90020-4 [CrossRef]
Jensen D. D. Transmission of peach yellow leaf roll virus by Fieberiella florii (Stäl) and a new vector, Osbornellus borealis. DeL. &; M. J. Econ. Entomol. 1957a. 50:668-72.
Jensen D. D. Differential transmission of peach yellow leaf roll virus to peach and celery by the leafhopper, Colladonus montanus. Phytopathology. 1957b. 47:575-78.
Jensen D. D. A plant virus lethal to its insect vector. Virology. 1959. 8:164-75. DOI: 10.1016/0042-6822(59)90002-9 [CrossRef]
Jensen D. D. Effects of plant viruses on insects. Ann. New York Acad. Sci. 1963. 105:685-712. DOI: 10.1111/j.1749-6632.1963.tb42958.x [CrossRef]
Jensen D. D. Influence of high temperatures on the pathogenicity and survival of western X-disease virus in leafhoppers. Virology. 1968. 36:662-67. DOI: 10.1016/0042-6822(68)90197-9 [CrossRef]
Jensen D. D. Comparative transmission of western X-disease virus by Colladonus montanus, C. geminatus, and a new leafhopper vector, Euscelidius variegatus. J. Econ. Entomol. 1969a. 62:1147-50.
Maramorosch K. Insect diseases induced by plant-pathogenic viruses. Viruses, Vectors and Vegetation. 1969b. John Wiley &; Sons, Inc. p. 505-25. 666p.
Maramorosch K. Herbaceous host plants of western X-disease agent. Phytopathology. 1971a. 61:1465-70.
Maramorosch K. Vector fecundity reduced by western X-disease. J. Invertebr. Pathol. 1971b. 17:389-94.
Maramorosch K. Temperature and transmission of the western X-disease agent by Colladonus montanus. Phytopathology. 1972. 62:452-56.
Jensen D. D., Frazier N. W., Thomas H. E. Insect transmission of yellow leaf roll virus of peach. J. Econ. Entomol. 1952. 45:335-37.
Jensen D. D., Richardson J. Effects of bacteria on leafhopper transmission of the western X-disease agent. J. Invertebr. Pathol. 1972. 19:131-38. DOI: 10.1016/0022-2011(72)90199-1 [CrossRef]
Jensen D. D., Thomas H. E. Leafhopper transmission of the Napa strain of cherry buckskin virus from cherry to peach. Phytopathology (Abstr.). 1954. 44:494
Jensen D. D., Thomas H. E. Transmission of the green valley strain of cherry buckskin virus by means of leafhoppers. Phytopathology (Abstr.). 1955. 45:694
Jensen D. D., Whitcomb R. F., Richardson J. Lethality of injected peach western X-disease virus to its leafhopper vector. Virology. 1967. 31:532-38. DOI: 10.1016/0042-6822(67)90235-8 [CrossRef]
Jones A. L., Hooper G. R., Rosenberger D. A. Association of mycoplasmalike bodies with little peach and X-disease. Phytopathology. 1974. 64:755-56. DOI: 10.1094/Phyto-64-755 [CrossRef]
Kunkel L. O. Transmission of virus from X-diseased peach trees to herbaceous plants. Phytopathology (Abstr.). 1944. 34:1006
Lee P. E., Jensen D. D. Crystalline inclusions in Colladonus montanus (Van Duzee), a vector of western X-disease virus. Virology. 1963. 20:328-32.
Long D. L., Timian R. G. Acquisition through artificial membranes and transmission of oat blue dwarf virus by Macrosteles fascifrons. Phytopathology. 1971. 61:1230-32.
Lott T. B. “Small bitter cherry,” a fruit abnormality of the Bing cherry variety. Sci. Agric. 1947. 27:260-62.
Macbeath J. H., Nyland G., Spurr A. R. Morphology of mycoplasmalike bodies associated with peach X-disease in Prunus persica. Phytopathology. 1972. 62:935-37.
Magyarosy A. C., Sylvester E. S. The latent period of beet curly top virus in the beet leafhopper, Circulifer tenellus, mechanically injected with infectious phloem exudate. Phytopathology. 1979. 69:736-38.
Maramorosch K. Incubation period of aster-yellows virus. Amer. J. Bol. 1953. 40:797-809. DOI: 10.2307/2438277 [CrossRef]
Maramorosch K. Interrelationships between plant pathogenic viruses and insects. Ann. New York Acad. Sci. 1964. 118:363-70. DOI: 10.1111/j.1749-6632.1964.tb33984.x [CrossRef]
Maramorosch K., Jensen D. D. Harmful and beneficial effects of plant viruses in insects. Ann. Rev. Microbiol. 1963. 17:495-530. DOI: 10.1146/annurev.mi.17.100163.002431 [CrossRef]
Messenger P. S. The influence of rhythmically fluctuating temperatures on the development and reproduction of the spotted alfalfa aphid, Therioaphis maculata. J. Econ. Entomol. 1964. 57:71-76.
Mittler T. E. The excretion of honey-dew by Tuberolachnus salignus (Gmelin) (Homoptera: Aphididae). Proc. Roy. Entomol. Soc. Lond. 1958. 33:49-55.
Mittler T. E., Dadd R. H. An improved method for feeding aphids on artificial diets. Ann. Entomol. Soc. Amer. 1964. 57:139-40.
Mittler T. E., Sylvester E. S. A comparison of the injury to alfalfa by the aphids, Therioaphis maculata and Macrosiphum pisi. J. Econ. Entomol. 1961. 54:615-22.
Nasu S, Jensen D. D., Richardson J. Electron microscopy of mycoplasma-like bodies associated with insect and plant hosts of peach western X-disease. Virology. 1970. 41:583-95. DOI: 10.1016/0042-6822(70)90424-1 [CrossRef]
Nasu S, Jensen D. D., Richardson J. Extraction of western-X mycoplasmalike organism from leafhoppers and celery infected with peach western X-disease. Appl. Ent. Zool. 1974. 9:53-57.
Nielson M. W., Jones L. S. Insect transmission of western-X-little-cherry virus. Phytopathology. 1954. 44:218-19.
Nyland G. Interference between the viruses or virus strains causing yellow leaf roll and western-X disease of peach. Phytopathology. 1955. 35:694-95.
Nyland G. Remission of symptoms of pear decline in pear and peach X-disease in peach after treatment with a tetracycline. Phytopathology (Abstr.). 1971. 61:904-05.
Nyland G., Moller W. J. Control of pear decline with a tetracycline. Plant Dis. Rep. 1973. 57:634-37.
Nyland G., Schlocker A. Yellow leaf roll of peach. Plant Dis. Rep. 1951. 35:33
Palmiter D. H., Parker K. G. Peach X-disease on sour cherry. Phytopathology (Abstr.). 1948. 38:20
Purcell A. H. Transmission of X-disease agent by the leafhoppers Scaphytopius nitridus and Acinopterus angulatus. Plant Dis. Rep. 1979. 63:549-52.
Raju B. C., Purcell A. H., Nyland G. Isolation of spiroplasmas from leafhoppers exposed to aster yellows and X disease. (Abstr.). 1980. August 13-17: Florida. 12p. 1979 4th Meeting of Intern’l Council on Lethal Yellowing, Fort Lauderdale
Rana G. L., Kaloostian G. H., Oldfield G. N., Granett A. L., Calavan E. C., Pierce H. D., Lee I. M., Gumpf D. J. Acquisition of Spiroplasma citri through membranes by homopterous insects. Phytopathology. 1975. 65:1143-45. DOI: 10.1094/Phyto-68-681 [CrossRef]
Rawlins T. E., Horne W. T. “Buckskin”, a destructive graft-infectious disease of the cherry. Phytopathology. 1931. 21:331-35.
Rawlins T. E., Thomas H. E. The buckskin disease of cherry and other stone fruits. Phytopathology. 1941. 31:916-25.
Rawlins T. E., Thomas H. E. Virus Diseases of sweet cherry. Virus Diseases and Other Disorders with Viruslike Symptoms of Stone Fruits in North America, “Buckskin”—. USDA Agric. Hndbk 10 1951. pp.98-102. 276
Reeves E. L., Hutchins L. M. A progress report on western X-disease, a virus disease of peaches. Wash. State Hort. Assoc. Proc. 1941. 37:27-30.
Reeves E. L., Blodgett E. C., Lott T. B., Milbrath J. A., Richards B. L., Zeller S. M. Western X-disease. Virus Diseases and Other Disorders with Viruslike Symptoms of Stone Fruits in North America 1951. pp.43-52. USDA Agric. Hndbk 10, 276 pp.
Regenmortel van M. H. V. Purification of plant viruses by zone electrophoresis. Virology. 1964. 23:495-503. DOI: 10.1016/0042-6822(64)90233-8 [CrossRef]
Richards B. L., Hutchins L. M. A new virosis of peach in Utah, resembling X-disease (yellow-red virosis). Phytopathology (Abstr.). 1941. 31:19
Richards B. L., Hutchins L. M., Reeves E. L. The western “X” virus a cause of “little cherry” in Utah. Phytopathology (Abstr.). 1949. 39:19
Richards B. L., Reeves E. L., Hutchins L. M. Wilt and decline, a virus disease of sweet and sour cherries in Utah. Phytopathology. 1946. 36:409 (abstr.).
Richards B. L., Wadley B. N., Cochran G. W. Little cherry, a virus disease of sweet and sour cherries in Utah. Farm and Home Sci., Utah. Agric. Exp. Sta. Cir. 1948. 9:10-12.
Richardson J., Jensen D. D. Tissue culture of monolayer cell lines of Colladonus montanus (Homoptera: Cicadellidae) a vector of the causal agent of western X-disease of peach. Ann. Entomol. Soc. Amer. 1971. 64:722-29.
Rochow W. F. Variation within and among aphid vectors of plant viruses. Ann. New York Acad. Sci. 1963. 105:713-29. DOI: 10.1111/j.1749-6632.1963.tb42959.x [CrossRef]
Rochow W. F., Eastop V. F. Variation within Rhopalosiphum padi and transmission of barley yellow dwarf virus by clones of four aphid species. Virology. 1966. 30:286-96.
Sakimura K., Maramorosch K. The present status of thrips-borne viruses. Biological Transmission of Disease Agents. 1962. New York: Academic Press. p. 33-40. 192p.
Schlocker A. Peach yellow leaf roll and western X-disease of peach. Calif. Dept. Agric. Bull. 1957. 46:173-76.
Schwarz R. E., Van Vuuren S. P. Decrease in fruit greening of sweet orange by trunk injection of tetracyclines. Plant Dis. Rep. 1971. 55:747-50.
Severin H. H. P. Minimum incubation periods of causative agent of curly leaf in beet leafhopper and sugar beet. Phytopathology. 1921. 11:424-29.
Severin H. H. P. Modes of curly-top transmission by the beet leafhopper, Eutettix tenellus (Baker). Hilgardia. 1931. 6:253-76. DOI: 10.3733/hilg.v06n08p253 [CrossRef]
Smith L. M. Growth, reproduction, feeding and wing development of the mealy plum aphid in relation to climatic factors. J. Agric. Res. 1937. 54:345-64.
Stoddard E. M., Hildebrand E. M., Palmiter D. H., Parker K. G. X-disease. Virus Diseases and Other Disorders with Viruslike Symptoms of Stone Fruits in North America 1951. pp.37-42. USDA Hndbk. 40, 276 pp.
Storey H. H. The inheritance by an insect vector of the ability to transmit a plant virus. Proc. Roy. Soc. (London). 1932. 112:46-60. DOI: 10.1098/rspb.1932.0077 [CrossRef]
Storey H. H. Investigations of the mechanism of the transmission of plant viruses by insect vectors. I. Proc. Roy. Soc. (London). 1933. 113:463-85.
Storey H. H. Investigations of the mechanism of the transmission of plant viruses by insect vectors. II. The part played by puncture in transmission. Proc. Roy. Soc. (London). 1938. 125:455-77. DOI: 10.1098/rspb.1938.0037 [CrossRef]
Stubbs L. L. Strains of Myzus persicae (Sulz.) active and inactive with respect to virus transmission. Austr. J. Biol. Sci. 1955. 8:68-74.
Sylvester E. S. The yellow-net virus disease of sugar beets. Phytopathology. 1948. 38:429-39.
Sylvester E. S. Aphid transmission of nonpersistent plant viruses with special reference to the Brassica nigra virus. Hilgardia. 1954. 23:53-98. DOI: 10.3733/hilg.v23n03p053 [CrossRef]
Sylvester E. S. The latent period of pea-enation mosaic virus in the pea aphid, Acyrthosiphon pisum (Harris)—an approach to its estimation. Virology. 1965. 25:62-67. DOI: 10.1097/01.meg.0000216934.22114.51 [CrossRef]
Sylvester E. S. Retention of inoculativity in the transmission of pea enation mosaic virus by pea aphids as associated with virus isolates, aphid reproduction and excretion. Virology. 1967. 32:524-31. DOI: 10.1016/0042-6822(67)90304-2 [CrossRef]
Sylvester E. S., Richardson J. Some effects of temperature on the transmission of pea enation mosaic virus and on the biology of the pea aphid vector. J. Econ. Entomol. 1966. 59:255-61.
Sylvester E. S., Richardson J. Decreased survival of Hyperomyzus lactucae inoculated with serially passed sowthistle yellow vein virus. Virology. 1971. 46:310-17. DOI: 10.1097/01.meg.0000216934.22114.51 [CrossRef]
Thomas H. E., Rawlins T. E., Parker K. G. A transmissible leaf-casting yellows of peach. Phytopathology. 1940. 30:322-28.
Thompson S., Garrott D. G., Raju B. C., Davis M. J., Purcell A. H., Nyland G. A spiroplasma consistently isolated from western X-infected plants. (Abstr.) 1978. p.975. IVth Intern’l Conf. on Plant Pathogenic Bacteria, Angers
Thornberry H. H. Preliminary report on insect transmission of eastern peach X-disease virus in Illinois. Plant Dis. Rep. 1954. 38:12-13.
Watson M. A. Factors affecting the amount of infection obtained by aphis transmission of the virus HY. III. Phil. Trans. Roy. Soc. London Ser. B. 1936. 226:457-89.
Watson M. A. Studies on the transmission of sugar-beet yellows virus by the aphid, Myzus persicae (Sulz.). Proc. Roy. Soc. London Ser. B. 1940. 128:535-52.
Watson M. A., Okusanya B. M. A. Studies on the transmission of groundnut virus by Aphis craccivora Koch. Ann. Appl. Biol. 1967. 60:199-208.
Watson M. A., Roberts F. M. A comparative study of the transmission of Hyoscyamus virus 3, potato virus Y and cucumber virus 1 by the vectors Myzus persicae (Sulz), M. circumflexus (Buckton), and Macrosiphum gei (Koch). Proc. Roy. Soc. (London) Ser. B. 1939. 127:543-76.
Weathers L. G., Cochran G. W. Transmission of components of the western-X virus complex to herbaceous plants. Phytopathology (Abstr.). 1950. 40:970
Whitcomb R. F., Jensen D. D. Proliferative symptoms in leafhoppers infected with western X-disease virus. Virology. 1968. 35:174-77. DOI: 10.1016/0042-6822(68)90319-X [CrossRef]
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus I. Frequency of transmission after injection or acquisition feeding. Virology. 1966a. 28:448-53.
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus II. Fluctuation of virus concentration in the hemolymph after injection. Virology. 1966b. 28:454-58.
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus III. Salivary, neural, and adipose histopathology. Virology. 1967. 31:539-49. DOI: 10.1016/0042-6822(67)90236-X [CrossRef]
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus IV. Pathology in the alimentary tract. Virology. 1968a. 34:69-78.
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus V. Properties of the infectious agent. J. Invertebr. Pathol. 1968b. 12:192-201.
Whitcomb R. F., Jensen D. D., Richardson J. The infection of leafhoppers by western X-disease virus VI. Cytopathological interrelationships. J. Invertebr. Pathol. 1968c. 12:202-21.
Whitcomb R. F., Shapiro M., Richardson J. An Erwinia-like bacterium pathogenic to leafhoppers. J. Invert. Pathol. 1966. 8:299-307. DOI: 10.1016/0022-2011(66)90041-3 [CrossRef]
Wolfe H. R. Transmission of the western X-disease virus by the leafhopper, Colladonus montanus (Van D.). Plant Dis. Rep. 1955. 39:298-99.
Wolfe H. R., Anthon E. W. Insects help spread tree virus diseases. Better Fruit. 1952. 46:11-12. 35.
Wolfe H. R., Anthon E. W. Transmission of the western X-disease virus from sweet and sour cherry to peach by two species of leafhoppers. J. Econ. Entomol. 1953. 46:1090-93.
Wolfe H. R., Anthon E. W., Jones L. S. Transmission of western X-disease of peaches by the leafhopper, Colladonus geminatus (Van D.). Phytopathology (Abstr.). 1950. 40:971
Wolfe H. R., Anthon E. W., Kaloostian G. H., Jones L. S. Leafhopper transmission of western X-disease. J. Econ. Entomol. 1951. 44:616-19.
Zeller S. M. Virus diseases of stone fruits. Oregon State Hort. Soc. Ann. Rep. 1942. 34:85-90.