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David G. Hall and L.G. Albrigo

Attention to the management of insects that feed on foliar flush growth has increased in Florida citrus as a result of the establishment of invasive plant diseases associated with insects that develop exclusively on flush. Citrus can be monitored to identify peak periods of flush abundance to time insecticide applications for these insects; however, guidelines for quantifying flush abundance are lacking. We therefore investigated sampling procedures for estimating flush abundance. A sampling method was devised to enable a quantitative estimation of flush shoots, defined as any shoot with immature leaves. A sample unit was the area within a 15 × 15 × 15-cm frame slipped into the outer edge of a tree with the end of a branch inside the frame. The number of flush shoots originating within the sample unit was counted. Three sample units were examined per tree in 45 randomly selected trees weekly during 2005 in each of two blocks of trees, one containing young ‘Marsh’ grapefruit (Citrus paradise Macf.) and one containing mature ‘Temple’ orange (tangors) [C. reticulate Blanco × C. sinensis (L.) Osbeck]. A pronounced abundance of flush was generally indicated by means of one or more flush shoots per sample in the particular trees studied. Variation in numbers of flush shoots per sample was similar within and among trees, differed significantly among sample dates, and did not differ significantly between the two blocks of trees overall sample dates. Taylor's power law coefficients indicated that, over all sample weeks, flush shoots were randomly distributed within the young grapefruit trees and only weakly aggregated within the block of mature oranges. Projections indicated that a sampling plan consisting of 40 trees (one sample per tree) would provide density estimates acceptable enough for general estimates at mean densities of one or more shoots per sample. An index of pest abundance based on mean pest density per flush shoot and mean density of flush shoots per sample is proposed.

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Ute Albrecht, David G. Hall, and Kim D. Bowman

Candidatus Liberibacter asiaticus (Las) is a phloem-limited bacterium associated with huanglongbing (HLB), one of the most destructive diseases of citrus in Florida and other citrus-producing countries. Natural transmission of Las occurs by the psyllid vector Diaphorina citri, but transmission can also occur through grafting with diseased budwood. As a result of the difficulty of maintaining Las in culture, screening of citrus germplasm for HLB resistance often relies on graft inoculation as the mode of pathogen transmission. This study evaluates transmission efficiencies and HLB progression in graft-inoculated and psyllid-inoculated citrus under greenhouse and natural conditions in the field. Frequencies of transmission in graft-inoculated greenhouse-grown plants varied between experiments and were as high as 90% in susceptible sweet orange plants 6 to 12 months after inoculation. Transmission frequency in a tolerant Citrus × Poncirus genotype (US-802) was 31% to 75%. In contrast, transmission of Las after controlled psyllid inoculation did not exceed 38% in any of four experiments in this study. Whereas the time from inoculation to detection of Las by polymerase chain reaction (PCR) was faster in psyllid-inoculated US-802 plants compared with graft-inoculated US-802 plants, it was similar in graft- and psyllid-inoculated sweet orange plants. HLB symptom expression was indistinguishable in graft- and psyllid-inoculated plants but was not always associated with the number of bacteria in affected leaves. The highest number of Las genomes per gram leaf tissue measured in sweet orange plants was one to four × 107 in graft-inoculated plants and one to two × 107 in psyllid-inoculated plants. Highest numbers measured in tolerant US-802 plants were one to three × 106 and two to six × 106, respectively. Compared with artificial inoculation in a greenhouse setting, natural inoculation of field-grown sweet orange trees occurred at a much slower pace, requiring more than 1 year for infection incidence to reach 50% and a minimum of 3 years to reach 100%.

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Ed Stover, Sharon Inch, Matthew L. Richardson, and David G. Hall

The citrus disease huanglongbing (HLB) has become endemic in Florida, with estimates that greater than 80% of citrus trees are currently infected. Although there are no commercial citrus varieties with strong HLB resistance, some field tolerance has been observed in trees exposed to the disease after they were mature. There is great urgency to identify citrus which may permit economic citrus production where HLB is endemic. Therefore, the objective of this study was to assess field tolerance to HLB. To expedite the trial due to urgency, nursery trees were purchased on rootstock varieties as available. The trial included the following unbalanced scion/rootstock combinations: ‘Hamlin/Kinkoji’, ‘Hamlin/Cleopatra’, ‘Temple/Cleopatra’, ‘Fallglo/Kinkoji’, ‘Sugar Belle/Sour Orange’, ‘Tango/Kuharske’, and ‘Ruby Red/Kinkoji’, with most comparisons based solely on scion/rootstock combinations. A randomized complete block experiment was established at Fort Pierce, FL, in Sept. 2010. All trees exhibited symptoms of HLB and tested positive for the Candidatus Liberibacter asiaticus (CLas) bacterium by Oct. 2012, with similar titers [directly assessed as cycle threshold (Ct) using quantitative polymerase chain reaction (qPCR)] measured for all scion/rootstocks at most sample dates, but early titer development in ‘Ruby Red/Kinkoji’ was significantly lower than several other scion/rootstocks. Across all time-points, ‘Fallglo/Kinkoji’ had the lowest rating of distinctive HLB mottling and ‘Ruby Red/Kinkoji’ had the highest rating, but ‘SugarBelle/Sour Orange’ had the highest percentage of leaves affected. After 5 years, ‘SugarBelle/Sour Orange’ and ‘Tango/Kuharske’ had the greatest overall increase in trunk diameter, and were among the healthiest in overall appearance. In Oct. 2015, ‘SugarBelle/Sour Orange’ and ‘Tango/Kuharske’ trees had significantly greater fruit load (80–88 fruit/tree) followed by ‘Temple/Cleopatra’ and ‘Fallglo/Kinkoji’ (31–35 fruit/tree) while ‘Hamlin/Kinkoji’, ‘Hamlin/Cleopatra’, and ‘Ruby Red/Kinkoji’ produced less than 20 fruit per tree. Despite becoming infected by CLas in less than 2 years after planting, the trees continued to grow and all scion/rootstocks displayed increasing fruit production, although very low in ‘Hamlin/Kinkoji’, ‘Hamlin/Cleopatra’, and ‘Ruby Red/Kinkoji’. Growth and fruit production in the highest performing scion/rootstocks were likely less than would be expected for healthy trees, but these results are promising, with markedly better response of some scion/rootstocks with mandarin hybrid scions compared with trees with sweet orange or grapefruit scions. Larger fully replicated trials are underway. It is noteworthy that the most pronounced HLB symptoms and higher early pathogen titer, which are the two criteria most widely used in assessing HLB resistance, were not associated with the lowest growth and cropping, and focus on early symptomatic traits when screening for resistance may obscure important disease tolerance.

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Abigail J. Walter, YongPing Duan, and David G. Hall

Huanglongbing, one of the most devastating diseases of citrus, is associated with the bacterium ‘Candidatus Liberibacter asiaticus’ vectored by the Asian citrus psyllid, Diaphorina citri, in North America. Murraya paniculata is a common ornamental plant that is an alternate host of both the psyllid and bacterium. We tested M. paniculata and Citrus sinensis grown together in the same field for their titer of ‘Ca. L. asiaticus’. We found the bacterium in both M. paniculata and C. sinensis, but the titer was four orders of magnitude lower in M. paniculata. We also assayed D. citri from laboratory colonies reared on either ‘Ca. L. asiaticus’-infected M. paniculata or infected Citrus spp. Psyllids reared on infected M. paniculata also carried bacterial titers five orders of magnitude lower than psyllids reared on infected Citrus spp. These observations imply resistance to huanglongbing in M. paniculata.

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David G. Hall, Tim R. Gottwald, Ed Stover, and G. Andrew C. Beattie

Asiatic huanglongbing (HLB) is a devastating disease of citrus associated in North America with the bacterium ‘Candidatus Liberibacter asiaticus’ (LAS) vectored by the Asian citrus psyllid (ACP), Diaphorina citri Kuwayama. ACP management is considered a vital component of a program aimed at reducing the incidence and spread of HLB. Considerable research has been published comparing the efficacy of different insecticides for ACP control as well as on seasonal strategies for applying ACP insecticides. However, published information was largely lacking for even the most intense insecticide programs on their effectiveness for keeping HLB out of a new citrus planting in Florida citrus. We therefore conducted two replicated (individual plots 0.2 to 0.4 ha in size) experiments on protecting young citrus from HLB using different ACP management programs. An intensive insecticide program was evaluated in each experiment: eight annual calendar applications of traditional insecticides (hereafter referred to as the “complete” program). In one experiment, citrus was either planted alone and subjected to the complete program or citrus was interplanted with orange jasmine, Murraya exotica L. (a favored ACP host plant) and subjected to a reduced insecticide program (four calendar sprays of traditional insecticides). There was one set of plots in which both jasmine and citrus were treated with insecticides and one set in which jasmine was not treated at all. In the second experiment, citrus was either subjected to the complete program or to one of two other programs: a reduced insecticide program consisting of five calendar applications of traditional insecticides or a mineral oil program (oil applications every 3 weeks plus one dormant insecticide spray). The results of the two experiments were similar. Relatively good ACP control was achieved under each ACP management program during the first year but, as the experiments progressed and trees increased in size, ACP outbreaks occurred regardless of the psyllid management program. Little HLB developed under any ACP management program during the first year, but thereafter HLB increased and large percentages of the trees in each experiment became LAS-infected in less than two to three years. The combined results of the experiments indicated that up to eight monthly pesticide treatments per year applied on a calendar schedule were ineffective for preventing young citrus from becoming diseased. Of important significance is that the orchard within which the two experiments were conducted was subjected to a minimal psyllid management program and contained many older trees known to be infected by the HLB pathogen, a challenging situation for getting young trees into production without contracting the disease. Thus, the ACP management programs we evaluated might have been more effective if ACP in the surrounding areas had been more aggressively controlled and diseased trees in the surrounding areas removed to reduce inoculum loads. Also, the programs might have been more effective for slowing the spread of HLB if our research plots had been larger.

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Ed Stover, David G. Hall, Robert G. Shatters Jr., and Gloria A. Moore

Assessments of the resistance of citrus germplasm to huanglongbing (HLB) can be expedited by inoculating plants under laboratory or greenhouse settings with the HLB bacterium, Candidatus Liberibacter asiaticus (CLas). Consistent rapid screening is critical to efficiently assess disease resistance among plant materials; however, a number of factors may govern the efficacy of such inoculations. Despite the rapidity at which HLB can spread in a grove, it often takes 8 to 10 months for high levels of CLas and HLB symptoms to develop even in highly susceptible sweet orange. Therefore, two experiments were conducted to assess factors that might influence efficiency in screening for HLB resistance. In one experiment, three test citrus genotypes (‘Kuharske’, previously shown to be HLB resistant; rough lemon, previously shown to be HLB tolerant; and ‘Valencia’, HLB susceptible) were bud grafted using CLas-infected buds from four different source genotypes. All bud source genotypes had similar levels of CLas titer, but citron, rough lemon, and Volkamer lemon were hypothesized to be better bud inoculum sources as they are more tolerant of HLB than ‘Valencia’. Among the three test genotypes over all sources of infected buds, inoculations of ‘Kuharske’ resulted in lower CLas titers and fewer HLB symptoms than inoculations of rough lemon or ‘Valencia’. Inoculations of rough lemon resulted in higher CLas titers and more pronounced HLB symptoms when it was inoculated using infected buds from rough lemon or ‘Valencia’. Grafting ‘Valencia’ with infected buds from Volkamer lemon resulted in less disease than when ‘Valencia’ was grafted with infected citron, rough lemon, or ‘Valencia’ buds. Overall, these results suggest that the source of CLas-infected buds used to graft-inoculate some genotypes will influence disease development. Trunk cross-sectional area increase for the year following infection was 3× higher in ‘Kuharske’ and rough lemon, compared with ‘Valencia’. ‘Kuharske’ had very low levels of CLas (30 CLas/µg DNA), whereas ‘Valencia’ (43,000 CLas/µg DNA) and rough lemon (6700 CLas/ µg DNA) had relatively high levels. As an alternative to graft-inoculating plants with CLas-infected buds, plants can be subjected to infestations of CLas-infected Asian citrus psyllid (ACP) as occurs naturally. Of interest is if transmission rates of CLas and the development of HLB in a genotype are greater when the ACP have been feeding on the same host genotype. An experiment was therefore conducted to assess transmission of CLas by ACP reared on CLas-infected rough lemon to five different genotypes (‘Carrizo’, ‘Flame’ grapefruit, rough lemon, ‘Temple’, and ‘Valencia’). These assessments were made using a detached leaf assay recognized as a faster method of gauging transmission rates of CLas than using whole plants. Higher percentages of ACP died when they were transferred from infected rough lemon to healthy ‘Carrizo’, and lower percentages died when they were transferred to rough lemon or ‘Flame’. However, CLas transmission by infected ACP occurred to at least some leaves of each genotype in each of the five different assays, with 70% or more leaves of each genotype becoming infected in at least one assay. Over all assays, there was relatively little variation among genotypes in the percentage of leaves becoming CLas infected and in the titer of CLas developing in infected leaves. However, there were relatively large differences in transmission rates among individual assays unrelated to differences among test genotypes. Because of the rapidity of the detached leaf assay, efforts are merited to improve consistency of this inoculation method.

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Justin G. Gardner, David B. Eastwood, Charles R. Hall, and John R. Brooker

The University of Tennessee developed a flowering dogwood tree (Cornus florida) that is resistant to powdery mildew (Microspaera pulchra). A simulated cooperative game was created to estimate a university fee and predict the behavior of nursery growers and nursery product retailers. The simulation suggests a university fee of $3.51, leading to an average retail price premium for the resistant tree of $10.41. At this price level the simulation predicts that 62 percent of all retail dogwood trees sold would be powdery mildew resistant. Based on 1998 sales of 1.475 million dogwood trees nationwide, 914,500 were predicted to be the powdery mildew resistant varieties, resulting in $3.2 million in revenue for the university. Given this level of sales and markup pricing, the cost of the trees will rise in subsequent stages of the distribution channel, and revenues will increase as well. The simulation suggests nursery revenue will increase by nearly $4 million and costs by $3.2 million, resulting in a net nursery gain of $0.8 million. Similar computations for the retail level are $9.5 million in revenue and a net increase of $5.5 million.

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Ed Stover, David G. Hall, Jude Grosser, Barrett Gruber, and Gloria A. Moore

The primary objective of this experiment was to determine if the selection of rootstock (Citrus and hybrids) could enhance the development of huanglongbing (HLB)-related symptoms associated with the pathogen Candidatus Liberibacter asiaticus (CLas) in sweet orange (Citrus sinensis). If so, then it may permit more rapid identification of HLB-susceptible compared to HLB-resistant scion types. The secondary objective was to assess the impact of different rootstocks on plant growth parameters and health to determine if trees on any rootstocks displayed reduced sensitivity to HLB-influenced growth restriction. ‘Valencia’ sweet orange was budded on each of the following eight genotypes: Carrizo (C. sinensis × Poncirus trifoliata); Cleopatra (C. reshni); Green-7 {a complex allotetraploid from somatic hybrids [C. clementina × (C. paradisi × C. reticulata) + C. grandis] × [(C. aurantium + (C. sinensis × P. trifoliata)]}; UFR-2 (a complex allotetraploid from somatic hybrids {[C. clementina × (C. paradisi × C. reticulata)] + C. grandis} × (C. reticulata + P. trifoliata)); UFR-4 (same pedigree as UFR-2); rough lemon (C. jambhiri); sour orange (C. aurantium); and US-897 (C. reticulata × P. trifoliata). Half of the trees on each rootstock were bud-inoculated with CLas and half were inoculated with the asian citrus psyllid [ACP (Diaphorina citri)], which is the CLas vector. During both experiments, no rootstock conferred significantly greater HLB symptom severity compared to trees on Carrizo; however, trees on several rootstocks had reduced HLB severity compared to those on Carrizo. Regarding the bud-inoculated trees after 3 years, trees on UFR-4 displayed greater overall health than trees on Carrizo, Green-7, sour orange, and US897, and trees on UFR-4 had a higher percentage of plants with leaf cycle threshold (Ct) values >36 compared with trees on Cleopatra and rough lemon (62 vs. 26-29 respectively). Regarding the ACP-inoculated trees after 3 years, trees on UFR-4 had better overall health than trees on Carrizo, rough lemon, and US-897, and trees on sour orange had a higher percentage of plants with leaf Ct values greater than 36 only compared to Cleopatra and US-897. The percentage increase in the trunk diameter per month over the course of each entire experiment was significantly greater for UFR-2 in both trials than all rootstocks except UFR-4. Only root CLas titers were sometimes significantly higher for trees on other rootstocks compared to those on Carrizo. Although no rootstock provided acceleration of HLB symptom development compared with Carrizo, some rootstocks conferred significantly greater health compared to Carrizo. However, it is uncertain whether the modest differences in health and growth observed in these greenhouse trials would translate to economic benefits in the field.

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Ed Stover, Randall Driggers, Matthew L. Richardson, David G. Hall, Yongping Duan, and Richard F. Lee

Xanthomonas citri ssp. citri (Xcc) is the causal agent of Asiatic citrus canker (ACC), a commercially important disease in Florida citrus as well as in many other regions. In this study we evaluated occurrence of foliar lesions from ACC on progenies of 94 seed-source genotypes (hereafter called “parent genotypes”) of Citrus and Citrus relatives in the field in east–central Florida to identify the relative susceptibility to ACC. Eight seedlings per parent genotype were planted in a randomized complete block planting, but the number of plants assessed in some genotype groups was reduced by mortality at some or all sampling dates. Plants experienced ambient exposure to high Xcc inoculum pressure and plants were assessed in Sept. 2010, July 2011, Oct. 2011, May 2012, and Sept. 2012. The incidence and severity of ACC lesions were assessed and evaluated using non-parametric analyses to compare progeny from the 94 parent genotypes. Progeny of 14 parent genotypes did not exhibit ACC symptoms at any date. All were in genera other than Citrus with only Microcitrus and Eremocitrus being cross-compatible with Citrus. The kumquat hybrid C. halimii, two accessions of C. reticulata, C. nobilis, and C. sunki were the only Citrus species in the group that had a low severity (percent total leaf area showing symptoms) on each date of assessment. The aforementioned accessions had an average incidence and severity of ACC lesions of less than 4% in 2011 and 2012, but 26% to 38% in 2010 when no chemical control for ACC was applied in the adjoining citrus groves at our field site. Fourteen of the 16 progeny of C. reticulata and related parent genotypes were in the group with the lowest incidence and severity of ACC on two or more assessment dates. However, for analysis of only the most symptomatic leaves on each plant, 10 C. reticulata parent genotype progenies were in the most resistant category on the Sept. 2012 assessment despite having a low incidence and severity of ACC symptoms overall. Progeny of Poncirus and its hybrids as well as those of C. maxima, C. limon, and related species were the most severely diseased at all assessment dates. There were few instances in which progeny of different accessions of the same species had markedly different responses to ACC: progeny of C. reticulata ‘Fremont’ displayed more severe ACC compared with several other C. reticulata groups and C. aurantium ‘Zhuluan’ displayed much lower incidence and severity of ACC compared with several other accessions designated C. aurantium. Information on ACC susceptibility in diverse Citrus and Citrus relatives may prove useful for breeding programs aimed at reducing ACC susceptibility and will be of value to researchers interested in mechanisms of ACC resistance and susceptibility.

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Catherine J. Westbrook, David G. Hall, Ed Stover, Yong Ping Duan, and Richard F. Lee

Huanglongbing (HLB) is a serious and devastating disease of citrus caused by Candidatus Liberibacter spp. and vectored by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae). The disease has the potential to greatly limit the production of citrus in Florida and other citrus-growing regions worldwide. Current control of D. citri and HLB is inadequate, but the identification and incorporation of D. citri resistance traits from uncultivated Citrus spp. and Citrus relatives is seen as a potential disease management strategy. In this study, seedlings of 87 Rutaceae seed-source genotypes, primarily in the orange subfamily Aurantioideae, were assessed in the field for their propensity in a free-choice situation for infestations of natural south Florida populations of D. citri. The majority of test populations surveyed hosted all three life stages of D. citri; however, there were significant differences among the test populations in the mean ranks for D. citri eggs (F = 3.13, df = 86, P < 0.0001), nymphs (F = 9.01, df = 86, P < 0.0001), and adults (F = 4.21, df = 86, P < 0.0001). The only sampled test population that was completely avoided by all life stages of D. citri was seedlings of Casimiroa edulis Llave et Lex, commonly known as white sapote, which was one of the few plants included in the study belonging to the Rutaceae subfamily Toddalioideae. Although not completely avoided, very low levels of D. citri were found on two surveyed test populations of Poncirus trifoliata (L.) Raf, seedlings of ‘Simmon's trifoliate’ and ‘Little-Leaf’. Poncirus trifoliata, the trifoliate orange, readily forms hybrids with Citrus spp., is commonly incorporated into rootstock varieties, and has been used in breeding-advanced scion material. The identification of partial resistance in P. trifoliata to D. citri could prove useful in future citrus breeding efforts aimed at reducing the incidence and spread of HLB. Determining if there is true resistance to D. citri in this and other germplasm sources with a low propensity for infestations in free-choice situations will require no-choice experiments.