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Home , Citrus tristeza virus

Host Effects on Natural Spread of Tristeza in Florida

R. K. Yokomi and S. M. Garnsey

ABSTRACT. Aphid transmission and natural spread of citrus tristeza virus (CTV) in different citrus receptor hosts were studied under field and laboratory conditions. After 10 years of field exposure, natural infection of 12 citrus cultivars segregated into three groups: 1) highly susceptible varieties (89-100%) which included Alemow, Volkamer , Ridge Pineapple, Orlando , and ; 2) varieties with low susceptibility (27-53%) which included , Cleopatra mandarin, sour , and Palestine sweet lime; and 3) resistant varieties (0%) which included Swingle , , and Carrizo . In greenhouse tests, Alemow and Mexican lime seedlings were the best receptor plants for transmission of the T-67 isolate of CTV by Glover with infection rates of 38 and 31%, respectively, whereas infection rates in Pineapple and Hamlin sweet oranges and Duncan were 19, 17, and 11%, respectively. No transmis- sion was obtained to sour orange or Carrizo citrange. Citms hystrix DC, sweet orange varieties, Temple, and grapefruit were good hosts for nymph survival and production of A. gossypii and Aphis citricola van der Goot in laboratory tests with detached leaves. In comparison, Mexican lime was a poor host while Alemow was a nonhost. Carrizo citrange and Swingle citrumelo were also nonhosts of the aphids. These observations indicated that many varieties susceptible to CTV were good hosts for citrus aphids under test conditions, but vector transmission to different receptor plants was not necessarily correlated to aphid host suitability. Index words. Citrus rootstocks, aphid vectors, resistance, epidemiology, transmission, host range.

Citrus varieties differ in suscepti- METHODS AND MATERIALS bility to citrus tristeza virus (CTV). The mechanism of these differences is Trees and plot. A 13-row citrus complex and not well understood. plot was planted in a commercial cit- Garnsey et al. (4) have described dif- rus grove in 1976 in Indiantown, ferences in virus titer of different Florida. Ten rows were planted with CTV isolates in different cultivars. trees infected with Some varieties such as trifoliate T-26, a mild CTV isolate, on different orange, Swingle citrumelo, and Car- rootstocks. Greenhouse-grown, 1- rizo citrange are highly resistant to year-old seedlings or rooted cuttings CTV infection, even by graft trans- of 12 cultivars (Table 1) were planted mission, whereas sweet orange vari- as tristeza-free trees in rows 1,8, and eties support high titers of virus. 13 in this plot. These trees were Natural spread of CTV is by aphid rootstock varieties and were planted vectors. The variety of the acquisition in a randomized complete block de- host and the variety of the receptor sign with six replications and three affected CTV transmission under ex- trees per replication. The entire plot perimental conditions (2, 7,9). Hence, area covered 1.4 ha with 80 trees per natural spread of CTV depends on a row and a tree spacing of 5.2 x 7.6 m. complex of factors which includes sus- The primary purpose of this plot test ceptibility to inoculation, virus repli- was to monitor incidence cation, vector feeding behavior, vec- in grafted and nongrafted trees. Since tor reproduction, and vector move- other commercial plantings near this ment. The purpose of this study was plot were infected with CTV, a sur- to gain further insight into these in- vey was conducted of all rootstocks teractions by comparing field spread trees in the plot after 10 years of field of CTV into different cultivars with exposure. These trees provided an some laboratory tests of vector trans- opportunity to measure CTV spread mission, and to measure aphid repro- in the field under replicated condi- duction on different citrus varieties. tions. Tenth IOCV Conference

CTV assay. Fully expanded cal analysis was conducted by SAS young leaves or twigs were harvested (Raleigh, NC). from two sides of each field tree in the spring of 1985 and 1986. Bark and/ RESULTS or leaf midribs were excised from Field spread. After 10 years of these samples and assayed for CTV field exposure to endemic and field infection by double antibody sandwich sources of CTV and natural popula- enzyme-linked immunosorbent assay tions of aphid vectors, sufficient field (1) using antisera to whole, unfixed spread had occurred to segregate the virus particles of CTV isolate T-4 (3). citrus varieties into three categories Vector transmission. Seedlings based on number or percentage of of nine citrus varieties were grown in trees infected (Table 1). The first the greenhouse. These plants were group was highly susceptible to CTV used as receptor plants when they with infection percentages ranging were ca. 10-20 cm tall. highly trans- from 89 to 100%. This group included missible CTV isolate, T-67, was prop- Ridge Pineapple (loo%), Alemow agated in Madam Vinous sweet (loo%), (loo%), Or- orange as the inoculum source for lando tangelo (94%), and rough lemon virus acquisition by Aphis gossypii (89%). The second group was rather Glover (9). Twenty aphids (late in- poorly susceptible to CTV with infec- stars and adults) were transferred to tion ranging from 27 to 53%. This each receptor plant. The virus acquis- group included Rangpur lime (53%), ition access and the inoculation Cleopatra mandarin (50%), sour periods were each 24 h. Donor and re- orange (52%), and Palestine sweet ceptor plants were maintained in an lime (27%). The last group, which in- air-cooled, partly shaded glasshouse. cluded Carrizo citrange, remained Daily diurnal temperatures fluctuated free of CTV. between 20-32 C. Aphid host range. Laboratory colonies of the melon aphid were TABLE 1 reared on okra, Hibiscus esculentum NATURAL INFECTION BY CITRUS L. var. Clemson spineless, while the TRISTEZA VIRUS OF CITRUS CUL- spirea aphid, Aphis citricola van der TIVARS ATER 10 YEARS IN A COMMER- Goot, was reared on C. hystrix DC. CIAL GROVE IN INDIANTOWN, Both aphids were reared in environ- FLORIDAz mental chambers at 25 C with a rela- No. tive humidity of 80 + 10% and a 16 h infectedY % photoperiod at 5000 foot candles. Two Cultivar no. tested Infected reproductively mature apterous Alemow 18/18 100 aphids were transferred from the col- Volkamer lemon 17/17 100 ony to detached leaves of each cul- Ridge Pineapple 212 100 tivar on 1% water agar, as described Orlando tangelo 17/18 94 by Yokomi and Gottwald (10). There Rough lemon 16/18 89 Rangpur lime 8/15 53 were 10 replications and the test was Cleopatra mandarin 9/18 50 repeated twice. Host suitability was Sour orange 9/17 52 evaluated by counting the number of Palestine sweet lime 4/15 27 live nymphs on each detached leaf at Swingle citrumelo 0118 0 Trifoliate orange 0118 0 day 7. This value was called the re- Canizo citrange 0117 0 productive rate. Because host precon- ditioning was not included prior to the "Trees were planted in November 1976, with a test, the early reproductive rate was row spacing of 5.2 x 7.6 m. often influenced by the colony host. YCTVinfection was determined by double anti- body sandwich enzyme-linked immunosorbent After 7 days, however, the number assay. Total treeslvariety was 18. Tree deaths of live nymphs was indicative of the due to freezes or foot rot ac- host suitability of the aphid. Statisti- counted for tree counts less than 18lvariety. Tristeza and Related Diseases

Vector transmission tests. Influ- TABLE 3 ence of host receptor variety on A. REPRODUCTION OF APHIDS ON DE- TACHED LEAVES OF DIFFERENT CIT- gossypii transmission of T-67 was de- RUS CULTIVARSz termined under laboratory condi- tions. Infection rates in Mexican lime Avg. no. and Alemow were the highest at 31% nymphslaphidY and 38%, respectively (Table 2). Li- Aphis Aphis mited tests with pummel0 and rough Host gossypii citrieola lemon receptors resulted in transmis- Hystrix sion rates of 30 and 20%, respectively. Valencia Rates for Pineapple and Hamlin Temple sweet oranges were 19 and 17%, re- Marsh spectively. Infection in grapefruit Pineapple Navel was 11%, whereas no transmission to Mexican lime sour orange or Carrizo citrange was Orlando tangelo detected. Four hosts were common to Trifoliate orange the field test described above. Volkamer lemon Rangpur lime Aphid reproduction. Nymph pro- Cleopatra mandarin duction of A. gossypii under test con- Rough lemon ditions was generally lower than that Palestine sweet lime of A. citricola on comparable hosts. Carrizo citrange Sour orange C. hystrix was the best host for the Alemow melon aphid with 37.3 nymphs per Swingle citrumelo adult (P < .05), whereas Valencia and Temple were the next best hosts at "Leaves incubated on 1% water agar for 7 days 15.9 and 15.7 nymphs per adult, re- in environmental chamber set for 25 C and 16 h photoperiod at 5000 foot candles (10). spectively (Table 3). Some reproduc- Two reproductively mature adult aphids were tion (4-5 nymphs) occurred on Pineap- placed on each detached leaf on day 0. The data ple and navel oranges, and on Mexi- represent the averages of two separate tests can lime, but this group was not per aphid host after 7 days. Each test had 10 statistically different from nonhosts replications. "Means associated with the same letter are not (0 to 1.5 nymphs). For spirea aphid, statistically different (P < .05) by Duncan's the highest reproduction was 25.6 multiple range test.

TABLE 2 nymphs on Valencia followed by C. APHID TRANSMISSION OF CTV TO DIF- FERENT RECEPTOR CULTIVARS OF hystrix, navel, and Temple with 20.9, CITRUS IN THE GREENHOUSEz 18.5, and 16.9 nymphs, respectively. Pineapple orange and Orlando tangelo No. were fair hosts along with Marsh Receptor positiveY/ % grapefruit and Mexican lime (5-8 variety no. tested transmission nymphs). However, the latter two Alemow 37/97 hosts and the nonhosts (1.8 or less) Mexican lime 481153 were in the same statistical group. Pummelo 3110 The nonhosts for both aphids in this Rough lemon 2/10 Pineapple 15/81 test included trifoliate orange, Vol- Hamlin 6/35 kamer lemon, Cleopatra mandarin, Duncan grapefruit 8/70 rough lemon, Palestine sweet lime, Sour orange 0125 Carrizo citrange, sour orange, Canizo 0125 alemow, and Swingle citrumelo. "Vector = 20 Aphis gossyiilreceptor plant; the CTV isolate was T-67. Data from several ex- DISCUSSION periments were combined and account for the different numbers of replicationslvariety. The CTV-infected Valencia YInfectionidentified by symptom expression or orange trees adjacent to the seedling by enzyme-linked immunosorbent assay. trees provided a good source of virus Tenth ZOCV Conference for natural spread of tristeza (2, 7, 9). poor or nonhosts for reproduction of Periodic field observations indicated the melon and the spirea aphids. Li- both melon and spirea aphids were mited tests with rough lemon also present in the Indiantown grove. showed lack of aphid host suitability Earlier vector tests had indicated coupled with good CTV transmission. that the T-26 isolate of CTV was not Sweet oranges and grapefruit were as readily transmissible as some other good reproductive hosts for aphids, Florida isolates tested (9). In fact, but were not as good receptors as the some of the field-infected Alemow had previous three. Roistacher et al. (8) stem pitting symptoms which are in- reported preferential feeding by the dicative of infection by a more severe melon aphid for several citrus vari- tristeza isolate. Because T-26 does eties, which was associated with CTV not induce stem pitting in Alemow (4) and CTV-seedling yellows vector and CTV infection is so prevalent in transmission to these hosts (7). The Florida sweet oranges (5), it is be- reproductive efficiency of an aphid on lieved that much of the CTV infection a citrus cultivar is not a measure of in the plot was from endemic sources infection susceptibility, but may be rather than from the T-26-infected important when citrus is the primary trees in the plot. source for generating vector popula- The susceptibility to natural CTV tions. infection in the cultivars compared The high degree of aphid host favorably with CTV susceptibility by suitability of Temple orange observed graft inoculation. As expected, known in our test was noteworthy. Out- CTV-resistant cultivars such as Car- breaks of tristeza decline in Florida rizo, Swingle, and trifoliate orange have sometimes been discovered in remained free of CTV infection, while proximity to Temple groves. Pelosi et cultivars that were good replicative al. (6) have suggested that this may hosts of CTV, such as sweet orange be due to the attraction of aphids to varieties, became naturally infected the frequent flushes of growth in with tristeza. The results of CTV Temple orange groves. Our data sup- transmission in the laboratory to dif- port their suggestion that large aphid ferent citrus receptor hosts generally populations could build up in these corroborated infection observed in groves which are also excellent hosts the field. Alemow and Mexican lime for CTV with subsequent spread of were the best receptor hosts. Sweet CTV if migration to other groves oc- oranges and grapefruit were also re- curs. In contrast, the epidemiological ceptors, but showed a lower infection importance of Mexican lime, an excel- rate. The lack of laboratory transmis- lent CTV host, depends on the abun- sion to sour orange receptors corre- dance of transient aphid vectors be- lated to the low rate of field infections cause the reproductive rate of the cit- observed in this cultivar after 10 rus aphids tested was low in relation years of field exposure. CTV prob- to the other citrus varieties. How- lems on sour-rooted citrus are due to ever, the high rate of CTV vector CTV infection to the sweet orange or transmission to Mexican lime would grapefruit scion. Risk of CTV infec- further complicate the epidemiology. tion to nursery liners (seedling rootstocks before budding) in the field ACKNOWLEDGMENTS should be low for all CTV-resistant hosts and all hosts which were in the The authors acknowledge the low infection group in our study. technical assistance of Pamela M. The detached-leaf host range tests Weschler, U.S. Department of Agri- indicated that the good CTV receptor culture, Agricultural Research Ser- hosts Mexican lime and Alemow were vice, Orlando, Florida. Tristeza and Related Diseases

LITERATURE CITED

1. BarJoseph, M., S. M. Garnsey, D. Gonsalves, M. Moscovitz, D. E. Purcifull, M. F. Clark, and G. Loebenstein 1979. The use of enzyme-linked immunosorbent assay for detection of citrus tristeza virus. Phytopathology 69: 190-194. 2. BarJoseph, M. and G. Loebenstein 1973. Effects of strain, source plant, and temperature on the transmissibility of citrus tristeza virus by the melon aphid. Phytopathology 63: 716-720. 3. Brlansky, R. H., S. M. Garnsey, R. E. Lee, and D. E. Purcifull 1984. Application of citrus tristeza virus antisera in labeled antibody, immuno-electron microscopical, and sodium dodecyl sulfate-immuno-diffusion tests, p. 337-342. In Proc. 9th Conf. IOCV., IOCV, Riverside, CA. 4. Garnsey, S. M., R. F. Lee, R. H. Brlansky, and R. K. Yokomi 1985. Serological titer of citrus tristeza virus (CTV) isolates of varying severity in different citrus hosts. Phytopathology 75: 1311. (Abst.). 5. Garnsey, S. M., R. F. Lee, C. 0. Youtsey, R. H. Brlansky, and H. C. Burnett 1980. A survey for citrus tristeza virus in registered budwood sources commercially prop- agated on sour orange rootstocks in Florida. Proc. Fla. State Hort. Soc. 93: 7-9. 6. Pelosi, R. R., M. Cohen, and R. M. Sonoda 1986. Virulence of CTV not affected by passage through Temple orange. Proc. Fla. State Hort. Soc. 99: 69-71. 7. Roistacher, C. N. and M. BarJoseph 1984. Transmission of tristeza and seedling yellows tristeza by Aphis gossypii from sweet orange, grapefruit, and lemon to 'Mexican' lime, grapefruit, and lemon, p. 9-18. In Proc. 9th Conf. IOCV, IOCV, Riverside, CA. 8. Roistacher, C. N., M. BarJoseph, and T. Carson 1984. Preferential feeding by Aphis gossypii on young leaves of sweet orange, grapefruit, and lemon, p. 19-22. in Proc. 9th Conf. IOCV. IOCV, Riverside, CA. 9. Yokomi, R. K. and S. M. Garnsey 1987. Transmission of citrus tristeza virus by Aphis gossypii and Aphis citricola in Florida. Phytophylactica 19: 169-172. 10. Yokorni, R. K. and T. R. Gottwald 1988. Virulence of Verticillium lecanii isolates in aphids determined by detached-leaf bioas- say. J. Invert. Path. (in press).