Transmission of Citrus Tristeza Virus by Aphis Gossypii Reflecting Changes in Virus Transmissibility in California
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Transmission of Citrus Tristeza Virus by Aphis gossypii Reflecting Changes in Virus Transmissibility in California C. N. Roistacher, E. M. Nauer, A. Kishaba, and E. C. Calavan In the early 1950's, the transmission rate to nearby trees. Therefore, transmissibil- of citrus tristeza virus (CTV) by the ity of CTV and CTV-SY isolates from melon aphid, Aphis gossypii Glover, many of these infected trees in the var- was very low. Dickson et al. (1956) in- iety collection by the melon aphid, A. duced five transmissions in 207 tests (2.4 gossypii, was studied and is reported in per cent) averaging 50 aphids per test, this paper. and 26 infections in 412 tests (6.3 per MATERIALS AND METHODS cent) averaging 221 aphids per test. Similar low rates of transmission were Experimental procedures generally reported in the early 1960's from Florida were those of Bar-Joseph and Loeben- by Norman et al. (1968) with A. gossypii stein (1973) and Raccah et al. (1976). and A. spiraecola Patch. A sudden out- Budwood was collected from 20 CTV- break of tristeza in Israel in 1970-73 and CTV-SY-infected trees in the prompted investigations by Bar-Joseph variety collection at the Citrus Research and Loebenstein (1973) on the trans- Center (Roistacher et al., 1979), and mission rates of three strains of CTV by from three CTV-infected trees in central four populations of A. gossypiicollected California. One to four Madam Vinous from various parts of their country. sweet orange seedlings in 4-liter con- Using 100 aphids per test, they found tainers were graft-inoculated with buds that one strain, from citrus in the from each infected tree to provide a uni- Sharon Plains area where tristeza was form acquisition host. Bar-Joseph and spreading, was transmitted to over 40 Loebenstein (1973) showed considerable per cent of the receptor plants by all differences in transmissibility of CTV four aphid populations. The other two from different hosts, with sweet orange strains were transmitted at less than 5 and mandarin showing the highest trans- per cent. mission rates. These findings from Israel and the Madam Vinous sweet orange acquisi- earlier report of Martinez and Wallace tion host plants were grown in a U.C. (1964), who found that seedling yellows potting mix (Nauer et al., 1968) in a tristeza virus (CTV-SY) from a few glasshouse at temperatures averaging varieties in the collection at the Univer- 26119°C (daytime maximumlnight- sity of California, Riverside, was trans- time minimum). Two to 18 months after missible by A. gossypiiat relatively high inoculation, they were cut back to force rates, led to a survey for CTV-SY in new growth for acquisition feeding. The some of the early citrus introductions in Mexican lime seedlings used for inocu- the variety collection at Riverside. This lation feeding and indexing were grown survey showed that 50 per cent of 38 in groups of three per 4-liter container early introductions had CTV-SY, and in a U.C. mix at warmer temperatures in a second test, 48 per cent of 27 declin- (35120°C). All plants were maintained ing trees nearby also had CTV-SY in optimum growth flush to attract (Roistacher et al., 1979). Since many of aphids for feeding. the infected trees in the second test were Aphids for most of the transmission recent seedling introductions, CTV-SY studies were progeny of R. C. Dickson's apparently was spreading from infected (A. G. 64) collection from watermelon Trrsteza and Related Disease5 in 1960 in the Palo Verde Valley near lemon isolate was transmitted to 3/42 Blythe, California. The aphids had been Mexican limes (7 per cent). There was maintained on melon plants continu- no transmission of two isolates (from ously for 18 years at Riverside. For Honey mandarin and C. webberz'). comparative studies, aphids were col- In 786 transmission tests made to lected in 1978 from melons growing Mexican limes with the Blythe culture, near Brawley in the Imperial Valley, the average number of aphids per test and from a melon vine near Tulare, in was 44.3, and aphid counts ranged from the central Valley of California. zero to over 400 per plant. In some Aphids were reared on muskmelon individual tests, transmission was (Cucumis melo L., 'PMR 45') in rearing achieved by few aphids, i.e., nine posi- cages in a small glasshouse, with tem- tive transmissions were obtained when peratures maintained at 21" + 3°C. no aphids survived and 14 transmissions Melon leaves containing mixtures of im- were obtained with two to five surviving mature and mature aphids were col- aphids per plant. Allowing for aphid lected, cut into segments, and placed in mortality, the total number of aphids cages attached to young shoots of the feeding during the 24-hour inoculation Madam Vinous acquisition plants. period was probably somewhat higher Norman and Sutton (1969) and Raccah than the counts made after 24 hours. et al. (1976) showed no differences in The low transmission rates of CTV- transmission rates between mature and SY isolates from Meyer lemon, Honey immature aphids. Acquisition and mandarin, and C. webberi suggest that inoculation feedings of 24 hours each these isolates were still being trans- were made at 24°C in a growth chamber. mitted at rates similar to or below those Light was provided for 16 hours daily. reported by Dickson.et al. (1956) for After the inoculation feeding, cages CTV in the early 1950's. were removed, and the live aphids on The three isolates of CTV from central leaves counted and killed with a 1 per California (T-505, T-5 14, and T-5 15) cent nicotine sulfate spray. The inocu- from D. Cordas of the Central Valley lated Mexican lime plants were held in Tristeza Eradication Program were all the glasshouse at 26.3"C/ 18.7"C (day- natural field infections in Valencia or time maximum/ nighttime minimum) at navel oranges. Isolate T-505, from a least 6 months and observed for tristeza 1970 collection, was transmitted at 18 symptoms. Most symptoms appeared and 32 per cent in two tests. Isolate T- within 4 to 8 weeks after inoculation 5 15, collected in 1977, was transmitted in feeding. Plants positive for tristeza were six tests at rates of 0 to 91 per cent, held for future subpropagations on whereas T-514, a severe tristeza isolate seedling yellows indicator plants. collected in 1977, was transmitted 100 Transmission tests for each isolate were per cent to 46 test plants. repeated at least once. Graft transmissions to other varieties. Graft inoculations from a number of RESULTS vector-infected Mexican lime plants to Transmission rates of CTV and CTV- grapefruit, sour orange, and Eureka SY. The results of transmission of 23 lemon indicator seedlings were made to CTV and CTV-SY isolates by A. gossYji determine if the yellows-inducing (Blythe culture) are given in table 1. potential of CTV-SY had been trans- With the exception of two isolates, mitted by A. gossypii. With few excep- T-5 15 and Citrusjunos (l487), the trans- tions, the severe potential of CTV-SY mission rates for repeated tests were was transmitted from the Madam Vinous consistent. Thirteen isolates were trans- acquisition host to Mexican limes by A. mitted at 100 per cent efficiency in at gossypii as indicated by the reactions on least one experiment, two above 90 per grapefruit, sour orange, and Eureka cent, and four isolates averaged 21-28 lemon indicator seedlings (table 2). The per cent transmission. The Meyer reactions in indicator seedlings were 78 Ei~hthIOCV Conference comparable to those made by bud- missible CTV-SY are progeny of very inoculations from infected Madam early introductions. Wallace et al. (1956) Vinous host plants or field source trees reported the presence of CTV-SY in a (table 1). In some cases, strains were few varieties in the CRC Riverside citrus separated by vector, as from Brazil navel variety collection and believed the virus and Kona oranges. However, the large was present when they were imported majority of vector-infected Mexican about 1930 or earlier. Martinez and lime buds appeared to transmit un- Wallace (1964) showed that three CTV- changed the CTV-SY isolates shown in SY isolates from the variety collection table 2, and many other isolates in un- were transmitted by A. gossjpii from reported tests. sweet orange to Mexican lime in 41 16, Comparison of different aphid cul- 114, and 719 tests. Yearly surveys of tures. Two additional cultures of A. trees in the UCR variety collection by W. gossypiiwere obtained, one from melons P. Bitters (personal communication) in the southern part of California and revealed that few trees were removed one from a melon in the Central Valley because of decline or poor performance of California, to confirm that the current between 1940 and 1970 but, within the very high transmissibility of many CTV past 9 years, the increase of declining and CTV-SY isolates depends on the trees has been exponential and rather nature of the virus and not on differences alarming. It is probable that the recent in aphid cultures. Eleven virus isolates in increase in declining trees in the UCR Madam Vinous were selected: six show- variety collection (Roistacher et al., ing high transmission, three moderate, 1979) is due to the change in transmis- and two no transmission with the Blythe sibility of severe CTV and CTV-SY aphid culture. The acquisition and inocu- strains. Raccah et al. (1977) reported a lation procedures were the same as in segregation of CTV isolates from a single previous tests.