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Survey of Poncirus trifoliata hybrids for resistance to colonization by Asian citrus psyllid.

Asiatic huanglongbing, also known as citrus greening or yellow shoot disease, is a serious citrus disease presumably caused by a bacterium ('Candidatus Liberibacter asiaticus'; Rhizobiaceae) transmitted by the Asian citrus psyllid, Diaphorinacitri Kuwayama (Hemiptera: Liviidae) (Bove 2006). Some Citrus species such as certain mandarins (Citrus reticulata Blanco; Rutaceae) exhibit various degrees of tolerance to the pathogen, but all Citrus (Rutaceae) species are susceptible to infection and some of the most economically important types of Citrus can quickly succumb to the disease, notably sweet oranges (Citrus sinensis [L.] Osbeck; Rutaceae) and grapefruit (Citrus paradisi Macfad.; Rutaceae). Citrus species highly susceptible to the disease decline in health and productivity to the point they lose their economic value. There is no cure for infection, and management programs aimed at the psyllid have ultimately been ineffective in preventing the introduction and spread of the pathogen in North America (Hall et al. 2013a, b).

Poncirus trifoliata (L.) Raf. (Rutaceae) is a close relative of and readily hybridizes with sweet oranges, grapefruit, and other Citrus species. Although genetically similar to Citrus, P. trifoliata is a deciduous relative that produces inedible fruit. The proven value of P. trifoliata in citrus production is its performance as a rootstock, increasing resistance to soil-borne pests, and conferring cold protection along with other desirable traits to the aboveground scion-portion of a tree. Citrus breeders have developed hybrids of P. trifoliata and Citrus spp. that are more broadly adapted than P. trifoliata, and are the primary rootstocks used in US citri-culture. Two traits of P. trifoliata are of interest in the pursuit of solutions to huanglongbing. One is tolerance to the pathogen, which has been noted in both pure P. trifoliata and some of its hybrids (Albrecht & Bowman 2012). The other trait of interest in pure P. trifoliata is resistance to colonization by the psyllid (Westbrook et al. 2011; Hall et al. 2015). Diaphorina citri sometimes oviposits on P. trifoliata, but lays significantly fewer eggs than on Citrus species, which are highly susceptible to ovi-position (Richardson & Hall 2013; Hall et al. 2017). Efforts continue to identify the trait (s) responsible for reduced oviposition on P. trifoliata, because these might be transferred to Citrus as a management tactic against D. citri. With this in mind, Hall et al. (2017) conducted a field survey to assess oviposition rates of D. citri on 4 citrange cultivars (hybrids between P. trifoliata and sweet orange). There was no evidence from this survey that traits conferring reduced oviposition on P. trifoliata were passed to these hybrids. However, many Poncirus hybrids have been and continue to be generated by breeders, and one cannot conclude from 4 hybrids alone that traits discouraging oviposition have not been passed to or expressed by other hybrids.

Presented here are the results of 3 field surveys of Poncirus hybrids looking for resistance to colonization by D. citri. The surveys were conducted in different plantings of trees located at a USDA grove near Fort Pierce, Florida, USA (27.4356833[degrees]N, 80.4309194[degrees]W). The plantings were subjected to routine fertilization and irrigation, herbicides, copper treatments for plant diseases, and occasional spray oil treatments, but no hard insecticides. The hybrids surveyed included citranges; citrandarins (hybrids with mandarin orange, C reticulata); citrumelos (hybrids with grapefruit, C. paradisi); citradias (hybrids with sour orange, Citrus aurantium L.; Rutaceae); citrangumas (hybrids between citrange and satsuma mandarin, Citrus unshiu Marcow.; Rutaceae); citremons (hybrids with lemon, Citrus limon [L.] Osbeck; Rutaceae); and hybrids between pomelo, Citrus maxima (Burm.) Merr. (Rutaceae), and Poncirus. The trees were periodically visited to collect 2 flush shoots appropriate for oviposition, although sometimes only 1 shoot could be found, and occasionally no flush was present on a tree. The shoots were transported to a laboratory and examined under a microscope to count eggs and nymphs, the latter of which were counted separately by instar. Combined egg + nymph counts per sample (converted to logs) and percentages of samples infested by fifth instar nymphs (arcsine transformed) were subjected to analyses of variance (ANOVA) (PROC GLM) (SAS Institute 2010), and results were reported with untransformed means.

In a 2017 survey, 27 genotypes were monitored for eggs and nymphs, including 20 new citranges from USDA and University of Florida breeders, 1 citrandarin, 3 complex hybrids, 2 Citrus species as susceptible checks, and 1 pure Poncirus resistant check. Five trees of each were sampled monthly from May to Sep. The 6-yr-old trees were in a large replicated planting (previously described by Hall et al. 2017) with conventional citrus cultivars, pure trifoliate cultivars, and many experimental hybrids. Significantly fewer immatures were observed on the pure Poncirus cultivar than on any other cultivar ([F.sub.25,474] = 5.9; P = < 0.0001) (Table 1). There were no significant differences between Citrus and any Poncirus hybrid with respect to infestation levels of immatures, but oviposition was somewhat reduced on 'Ftp646130,' the only hybrid tested with P. trifoliata in the pedigree of both parents. There was no obvious deterrence of nymphal development on any of the hybrids based on the frequency of fifth instar nymphs observed, and no significant differences ([F.sub.25,406] = 0.9; P = 0.58) were found among the cultivars with respect to percentages of samples with these nymphs.

In the second survey, oviposition rates were investigated on 6 different types of Poncirus hybrids. The seed source of the trees was the Citrus Research Center, Riverside, California, USA, and the specific CRC accession number was known for each cultivar. The trees were 5 yr old, and there were 4 trees of each cultivar (only 3 trees of 2 'Sacaton' accessions) in a replicated 0.25 ha planting of many selections along 3 rows (175 m long, 0.8 m tree spacing). Two pure Poncirus cultivars were sampled as resistant checks. No pure Citrus accessions were included in the planting, thus the citrange 'Uvalde' was surveyed as a susceptible check (Hall et al. 2017). The trees were sampled 9 times from Feb to Sep 2018. Infestation densities were relatively low throughout the survey, often with low percentages of flush shoots infested. Therefore, analyses were conducted on the maximum number of immature psyllids per flush shoot per tree. Significant differences among cultivars were found in infestation levels of D. citri ([F.sub.14,110] = 6.1; P = < 0.0001), but there was no evidence of resistance to D. citri ovi-position in any of the hybrids compared to the check (Table 2). Fifth instar nymphs were observed on all hybrids except 'Sacaton 2,' indicating that at least some nymphs fully developed on most hybrids. The data were too variable to declare any significant differences among cultivars with respect to percentages of samples with fifth instar nymphs ([F.sub.14,169] = 0.2; P = 0.99).

In the third survey, oviposition rates were assessed on a single tree of each of 6 different groups including 6 Poncirus hybrids. Two species of Severinia (Mantidae) (a close relative of Citrus) were included for comparison purposes. The 19-yr-old trees were scattered across 7 rows (140 m long, 4.6 m tree spacing) in a 0.7 ha planting of diverse germplasm maintained for breeding purposes. The trees were sampled 9 times from Mar to Sep 2018. As in the second survey, analyses were conducted on the maximum number of immature psyllids per flush shoot per tree. Significant differences were found among cultivars with respect to colonization by D. citri ([F.sub.14,102] = 13.2; P = < 0.0001). There was no evidence of reduced oviposition on the hybrids 'Cpb-40197,' 'Savage,' or 'Willits' (Table 2). Oviposition was reduced on 3 citrumelo hybrids ('Cpb-4481,' 'Sacaton,' and 'Yuma'; the latter was once considered a citrange but recent investigations indicate this is a citrumelo [M. Roose, unpublished]), but factors unrelated to resistance to oviposition may have been involved. This caution is provided primarily because only 1 tree of each cultivar was available for the survey. While in the second survey colonization on 3 of 6 citrumelo hybrids was not significantly different on 'Flying Dragon,' all 6 of these citrumelos, including 2 'Sacaton' cultivars, were as susceptible to colonization as a susceptible check. Tree age was 1 notable difference between the citrumelo cultivars in the 2 surveys. Fifth instar nymphs were frequently observed on 3 hybrids (1 citrandarin and 2 citranges). The 2 Severinia species were as susceptible to colonization as the Citrus hybrid accessions, although no fifth instars were observed during the limited observations of these 2 trees. Data on percentages of samples with fifth instars were too variable to declare any significant differences among cultivars ([F.sub.12, 40]= 0.8; P = 0.61).

The results of this study indicated that simple hybrids between Poncirus and Citrus species lack the marked resistance pure Poncirus exhibits to colonization by D. citri. This was true even during late spring and early summer when larger populations of D. citri are common in Florida citrus. Based on 'Ftp646130,' further investigations are warranted on the resistance of hybrids when both parents have Poncirus in their pedigree.


Genetic traits in Poncirus trifoliata (Rutaceae) are known to confer resistance to colonization by the Asian citrus psyllid, but field surveys indicated these traits were not expressed in any of 24 simple hybrids between P. trifoliata and sweet orange. No resistance to colonization by the psyllid was observed in 14 other types of P trifoliata hybrids. Three citrumelo hybrids appeared to be resistant in 1 survey, but in another survey, none of 6 citrumelos exhibited resistance. Interestingly, colonization was somewhat reduced on a hybrid with P. trifoliata in the pedigree of both parents, suggesting the possibility that traits suppressing oviposition may be recovered through similar crosses.

Key Words: citrus greening; huanglongbing; Diaphorina citri; Liberibacter


Se sabe que los rasgos geneticos en Poncirus trifoliata (Rutaceae) confieren resistencia a la colonizacion por parte del psflido asiatico de los cftricos, pero los sondeos de campo indicaron que estos rasgos no se expresaron en ninguno de los 24 hfbridos simples entre P. trifoliata y naranja dulce. No se observo resistencia a la colonizacion por el psflido en otros 14 tipos de hfbridos de P. trifoliata. Tres hfbridos de citrumelo parecieron ser resistentes en 1 sondeo, pero en otro sondeo, ninguno de los 6 citrumelos mostro resistencia. Curiosamente, la colonizacion se redujo algo en un hibrido con P. trifoliata en el pedigrf de ambos parientes, lo que sugiere la posibilidad de que los rasgos que suprimen la oviposicion puedan recuperarse a traves de cruces similares.

Palabras Clave: cftricos enverdecimiento; huanglongbing; Diaphorina citri; Liberibacter

References Cited

Albrecht U, Bowman KD. 2012. Tolerance of trifoliate citrus rootstock hybrids to Candidatus Liberibacter asiaticus. Scientia Horticulturae 147: 71-80.

BoveJM. 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88: 7-37.

Hall DG,Gottwald TR, Stover E, Beattie GAC. 2013a. Evaluation of management programs for protecting young citrus plantings from huanglongbing. HortScience 48: 330-337.

Hall DG, Richardson ML, Ammar ED, Halbert SE. 2013b. Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae), vector of citrus huanglongbing disease. Entomologia Experimentalis et Applicata 146: 207-223.

Hall DG,George J, Lapointe SL. 2015. Further investigations on colonization of Poncirus trifoliata by the Asian citrus psyllid. Crop Protection 72: 112-118.

Hall DG, Hentz MG, Stover E. 2017. Field survey of Asian citrus psyllid (Hemiptera: Liviidae) infestations associated with six cultivars of Poncirus trifoliata. Florida Entomologist 100: 667-668.

Richardson ML, Hall DG. 2013. Resistance of Poncirus and Citrus x Poncirus germplasm to the Asian citrus psyllid. Crop Science 53: 183-188.

SAS Institute, Inc. 2010. SAS Procedures Guide. Version 9.3. SAS Institute, Cary, North Carolina, USA.

Westbrook a, Hall DG, Stover EW, Duan YP, Lee RF. 2011. Colonization of Citrus and Citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). Hort-Science 46: 997-1005.

David G. Hall (1,*), Chandrika Ramadugu (2), Matthew G. Hentz (1), Fred G. Gmitter Jr. (3), and Ed Stover (1)

(1) USDA-ARS, U.S. Horticultural Research Laboratory, 2001 South Rock Road, Ft. Pierce, Florida 34945, USA; E-mail: (D. G. H.); (M. G. H.); (E. S.)

(2) University of California, 900 University Avenue, Riverside, California 92521, USA; E-mail: (C. R.)

(3) University of Florida, Citrus Research & Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA; E-mail: (F. G. G.)

(*) Corresponding author; E-mail:
Table 1. Mean number of immature Asian citrus psyllid per flush shoot
in a 6-yr-old field planting of Citrus, Poncirus trifoliata, and their
hybrids (survey 1). All hybrids except 'Ftp646130' had 1 parent that
was either pure Poncirus or a Poncirus hybrid; both parents of
'Ftp646130' were Poncirus hybrids. (a)

                                        Mean number
Genotype group     Cultivar             immatures per flush shoot

Citrus             'Hamlin' C sinensis  40.9 ab
Citrus (Tangor)    'Temple'             40.7 ab
Citrandarin        'US-897'             26.0 ab
Citrange           'B11R1T22'           55.7ab
Citrange           'B11R1T34'           47.1 ab
Citrange           'B11R5T57'           35.3 ab
Citrange           'B6R18T3'            35.8 ab
Citrange           'B6R18T6'            38.6 ab
Citrange           'B6R18T7'            56.4 ab
Citrange           'FD-X-SHAM-#1'       48.8 ab
Citrange           'FD-X-SHAM-#4'       70.7 a
Citrange           'FD-X-SUCC-#15'      29.9 ab
Citrange           'FD-X-SUCC-#19'      24.5 ab
Citrange           'FD-X-SUCC-#5'       25.5 ab
Citrange           'SFB16R1T55'         45.5 ab
Citrange           'SFB16R2T54'         47.0 ab
Citrange           'SFB6R1T53'          48.4 ab
Citrange           'SFB7R1T44'          66.2 ab
Citrange           'SFB7R1T56'          45.5 ab
Citrange           'SFB7R1T58'          52.4 ab
Citrange           'SFB7R2T47'          42.3 ab
Citrange           'SFB7R2T59'          34.4 ab
Citrange           'SFB7R2T89'          33.7 ab
Complex citrumelo  'US-119'             35.9 ab
Complex citrumelo  '2610'               21.7 ab
Complex citrumelo  'Ftp646130' (b)      15.7 b
Poncirus           'Rubidoux'            6.9 c

                   Mean percentage of
Genotype group     infested samples with fifth instar nymphs

Citrus             61.1 a
Citrus (Tangor)    65.0 a
Citrandarin        52.4 a
Citrange           47.8 a
Citrange           31.3 a
Citrange           54.6 a
Citrange           57.9 a
Citrange           40.0 a
Citrange           54.2 a
Citrange           50.0 a
Citrange           60.0 a
Citrange           45.8 a
Citrange           33.3 a
Citrange           60.0 a
Citrange           27.3 a
Citrange           25.0 a
Citrange           38.1 a
Citrange           57.1 a
Citrange           41.2 a
Citrange           61.1 a
Citrange           44.4 a
Citrange           42.9 a
Citrange           34.8 a
Complex citrumelo  41.7 a
Complex citrumelo  60.9 a
Complex citrumelo  41.2 a
Poncirus           37.5 a

(a) Means in the same column followed by the same letter are not
significantly different (P > 0.05), Ryan-Einot-Gabriel-Welsch multiple
range test.
(b) Hybrid between '2610' and ([pummelo x Poncirus] x 'Succory' sweet

Table 2. Maximum numbers of immature Asian citrus psyllid per flush
shoot observed in 5-yr-old (survey 2) and 9-yr-old (survey 3) field
plantings of Poncirus trifoliata hybrids. All hybrids had 1 parent that
was either pure Poncirus or a Poncirus hybrid. (a)

Genotype group     Genotype or cultivar                 CRC (b)

5-yr-old trees
Citrange           'Uvalde' (susceptible check)         2865
Citrange           'Carrizo'                            2863
Complex citrange   'Citrangor'                          1447
Citradia           Poncirus x C. aurantium              1436
Citranguma         'S-302'                              3415
Citremon           Poncirus x Citrus limon              1449
Pomelo hybrids     African shaddock x Poncirus          3969
Citrumelo          'C-190'                              3889
Citrumelo          C paradisi x Poncirus                3821
Citrumelo          Poncirus x C. paradisi               1452
Citrumelo          'Sacaton 1'                          3337
Citrumelo          'Sacaton 2'                          3414
Complex citrumelo  'US-119'                             3998
Poncirus           'Rubidoux'                           838
Poncirus           'Flying Dragon'                      3330
19-yr-old trees
Citrus             Citrus macrophylla Wester            -
Citrus             'Jackson' C. paradisi                -
Citrus             'Ridge Pineapple' C. sinensis        -
Citrus             'Triumph' C. paradisi                -
Citrus             'Volkamer' C. limon                  -
Citrandarin        'Cpb-40197'                          -
Citrange           'Savage'                             -
Citrange           'Willits'                            -
Citrumelo          'Yuma'                               -
Citrumelo          'Sacaton'                            -
Complex citrumelo  'cpb-4481'c                          -
Citrus relative    Severinia buxifolia (Poir.) Ten.     -
Citrus relative    Severinia disticha (Blanco) Swingle  -
Poncirus           'Yamaguchi'                          -
Poncirus           'Rubidoux'                           -

                   Maximum number        % samples
Genotype group     immatures per sample  with fifth instar nymphs

5-yr-old trees
Citrange           30.4 a                36.4 a
Citrange           44.3 a                30.8 a
Complex citrange   43.5 a                31.3 a
Citradia           32.4 a                35.0 a
Citranguma         49.9 a                30.0 a
Citremon           52.6 a                30.0 a
Pomelo hybrids     28.3 a                27.8 a
Citrumelo          49.4 a                33.3 a
Citrumelo          41.1 a                47.6 a
Citrumelo          23.1 ab               28.6 a
Citrumelo          17.7 ab               23.1 a
Citrumelo          29.2 ab                0.0 a
Complex citrumelo  20.2 a                26.3 a
Poncirus            2.2 c                33.3 a
Poncirus            9.1 bc               33.3 a
19-yr-old trees
Citrus             14.9 abc              42.9 a
Citrus             35.8 ab               50.0 a
Citrus             53.0 ab               40.0 a
Citrus             33.0 ab               42.9 a
Citrus             21.6 ab               33.3 a
Citrandarin        35.8 ab               16.7 a
Citrange           27.4 ab               83.3 a
Citrange           68.3 a                62.5 a
Citrumelo          3.3 cde                0.0 a
Citrumelo           1.6 de                0.0 a
Complex citrumelo   3.2 cde              50.0 a
Citrus relative    15.1 bcd               0.0 a
Citrus relative    20.4 ab                0.0 a
Poncirus            0.0 e                 -
Poncirus            0.0 e                 -

(a) Means in the same column followed by the same letter are not
significantly different (P > 0.05), Ryan-Einot-Gabriel-Welsch multiple
range test.
(b) Citrus Research Center accession number
(*) (Citrus paradisi x Poncirus) x open pollination

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Author:Hall, David G.; Ramadugu, Chandrika; Hentz, Matthew G.; Gmitter, Fred G., Jr.; Stover, Ed
Publication:Florida Entomologist
Date:Sep 1, 2019
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