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Intraspecific Variation in Aphid Resistance and Constitutive Phenolics Exhibited by the Wild Blueberry Vaccinium darrowi

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Abstract

Illinoia pepperi (MacGillivray) infests cultivated highbush blueberries, Vaccinium corymbosum L., in the Northeastern United States. Allopatric resistance to I. pepperi was examined in Vaccinium darrowi Camp, which evolved in the absence of I. pepperi in the Southeastern U.S. V. corymbosum cv. “Elliott”, was used as a susceptible control. Between population variability in I. pepperi resistance was assessed by measuring length of the prereproductive period, fecundity, and survivorship on 14 V. darrowi accessions representing 11 discrete wild populations. Length of I. pepperi’s prereproductive period and survivorship were not significantly affected. However, differences were detected in fecundity and the intrinsic rate of increase (r m ). Within population variability in resistance was measured by confining first instars to 24 accessions from a single wild population of V. darrowi (NJ88-06). Significant differences in the mean total number of aphids occurring after 20 d were only detected between 2 of the 24 V. darrowi accessions. A greater degree of diversity in I. pepperi resistance exists between populations of V. darrowi compared to within a population. Constitutive leaf and stem polyphenolics were identified by HPLC-MS and quantified from 14 of the V. darrowi accessions. The accessions varied in concentrations of five phenolic acids and seven flavonol glycosides, but a correlation was not found between individual or total phenolics and aphid performance. Overall, screening within and between populations of V. darrowi identified promising sources of aphid resistance, but phenolic acid and flavonol glycoside profiles did not predict resistance levels. The mechanism of resistance remains to be identified.

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References

  • Andersson, B. A., Holman, R. T., Lundgren, L, and Stenhagen, G. 1980. Capillary gas chromatograms of leaf volatiles. A possible aid to breeders for pest and disease resistance. J. Agric. Food Chem. 28:985–989.

    Article  CAS  Google Scholar 

  • Andrewartha, H. G. and Birch, L. C. 1954. The Distribution and Abundance of Animals. University of Chicago Press, Chicago, USA.

    Google Scholar 

  • Ayaz, F. A., Hayirlioglu-Ayaz, S., Gruz, J., Novak, O., and Strnad, M. 2005. Separation, characterization, and quantification of phenolic acids in a little-known blueberry (Vaccinium arctostaphylos L.) fruit by HPLC-MS. J. Agric. Food Chem. 53:8116–8122.

    Article  PubMed  CAS  Google Scholar 

  • Binns, S. E., Livesey, J. F., Arnason, J. T., and Baum, B. R. 2002. Phytochemical variation in Echinacea from roots and flowerheads of wild and cultivated populations. J. Agric. Food Chem. 50:3673–3687.

    Article  PubMed  CAS  Google Scholar 

  • Blackman, R. L. and Eastop, V. F. 2000. Aphids on the World’s Crops: An Identification and Information Guide. John Wiley and Sons, Ltd. New York, NY.

    Google Scholar 

  • Brennan, R. M., Robertson, G. W., McNicol, J. W., Fyfee, L., and Hall, J. E. 1992. The use of metabolic profiling in the identification of gall mite (Cecidophyopsis ribis Westw.)–resistant blackcurrant (Ribes nigrum L.) genotypes. Ann. Appl. Biol. 121:503–509.

    CAS  Google Scholar 

  • Brignolas, F., Lieutier, F., Sauvard, D., Christiansen, E., and Berryman, A. A. 1998. Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera: Scolytidae) and an associated fungus, Ceratocytsis polonica. Can. J. For. Res. 28:720–728.

    Article  CAS  Google Scholar 

  • Bristow, P. R., Martin, R. R., and Windom, G. E. 2000. Transmission, field spread, cultivar response, and impact on yield in highbush blueberry infected with Blueberry scorch virus. Phytopathology 90:474–479.

    PubMed  CAS  Google Scholar 

  • Bruederle, L. P. and Vorsa, N. 1994. Genetic differentiation of diploid blueberry, Vaccinium sect. Cyanococcus (Ericaceae). Syst. Bot. 19:337–349.

    Article  Google Scholar 

  • Camp, W. H. 1945. The North American blueberries with notes on other groups of Vacciniaceae. Brittonia 5:203–275.

    Article  Google Scholar 

  • Calatayud, P. A., Rahbé, Delobel, B., Khuong-Huu, F., Tertuliano, M., and Le Ru, B. 1994. Influence of secondary compounds in the phloem sap of cassava on expression of antibiosis towards the mealybug Phenacoccus manihoti. Entomol. Exp. Appl. 72:47–57.

    Article  CAS  Google Scholar 

  • Chandler, C. K., Draper, A. D., Galletta, G. J., and Bouwkamp, J. C. 1985. Combining ability of blueberry interspecific hybrids for growth on upland soils. HortScience 20:257–258.

    Google Scholar 

  • Cho, M. J., Howard, R., Prior, R. L., and Clark, J. R. 2004. Flavonoid glycosides and antioxidant capacity of various blackberry, blueberry and red grape genotypes determined by high-performance liquid chromatography/mass spectrometry. J. Sci. Food Agric. 84:1771–1782.

    Article  CAS  Google Scholar 

  • Clifford, M. N., Kelly, L. J., Susan, K., and Nicholai, K. 2003. Hierarchical scheme for LC-MS identification of chlorogenic acids. J. Agric.Food Chem. 51:2900–2911.

    Article  PubMed  CAS  Google Scholar 

  • Cole, R. A. 1987. Intensity of radicle fluorescence as related to the resistance of seedlings of lettuce to the lettuce root aphid and carrot the carrot fly. Ann. Appl. Biol. 111:629–639.

    Article  Google Scholar 

  • DeLoach, C. J. 1974. Rate of increase of populations of cabbage, green peach and turnip aphids at constant temperatures. Ann. Entomol. Soc. Am. 67:332–340.

    Google Scholar 

  • Draper, A. D. 1995. In search of the perfect blueberry variety. J. Small Fruit Vitic. 3:17–20.

    Article  Google Scholar 

  • Dreyer, D. L. and Jones, K. C. 1981. Feeding deterrency of flavonoids and related phenolics towards Schizaphis graminum and Myzus persicae: aphid feeding deterrents in wheat. Phytochemistry 11:2489–2493.

    Article  Google Scholar 

  • Dreyer, D. L., Reese, J. C., and Jones, K. C. 1981. Aphid feeding deterrents in sorghum. Bioassay, isolation and characterization. J. Chem. Ecol. 7:273:283.

    Article  CAS  Google Scholar 

  • Elsner, E. A. and Kriegel, R. D. 1989. Distribution and seasonal phenology of blueberry aphids (Illinoia pepperi (Macg.)) in Michigan. Acta Hortic. 241:330–332.

    Google Scholar 

  • Erb, W. A., Draper, A. D., Galletta, G. J., and Swartz, H. J. 1990. Combining ability for plant and fruit traits of interspecific blueberry progenies on mineral soil. J. Am. Soc. Hortic. Sci. 115:1025–1028.

    Google Scholar 

  • Etzel, R. W. and Meyer, J. R. 1986. Resistance in blueberries to feeding and oviposition by the sharpnosed leafhopper, Scaphytopius magdalensis Provancher. J. Econ. Entomol. 79:1513–1515.

    Google Scholar 

  • Fraenkel, G. 1959. Evaluation of our thoughts on secondary plant substances. Science 129:1466–1470.

    Article  PubMed  CAS  Google Scholar 

  • Fritz, R. S. 1992. Community structure and species interactions of phytophagous insects on resistant and susceptible host plants, pp. 240–277. in R. S. Fritz and E. L. Simms (eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. The University of Chicago Press, Chicago, IL.

    Google Scholar 

  • Givovich, A., Morse, S., Cerda, H., Niemeyer, H. M., Wraten, S. D., and Edwards, P. J. 1992. Hydroxamic acid glucosides in honeydew of aphids feeding on wheat. J. Chem. Ecol. 18:841–846.

    Article  CAS  Google Scholar 

  • Hakulinen, J., Julkunen-Tiitto, R., and Tahvanainen, J. 1995. Does nitrogen fertilization have an impact on the trade-off between willow growth and defensive secondary metabolism? Trees 9:235–240.

    Article  Google Scholar 

  • Häkkinen, S. H. and Törrönen, A. R. 2000. Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: influence of cultivar, cultivation site and technique. Food Res. Int. 32:345–353.

    Article  Google Scholar 

  • Hancock, J. F., Haghighi, K., Krebs, S. L., Flore, J. A., and Draper, A. D. 1992. Photosynthetic heat stability in highbush blueberries and the possibility of genetic improvement. HortScience 27:1111–1113.

    Google Scholar 

  • Harborne, J. B. 1967. Function of flavonoids, pp. 280–303, in J. B. Harborne (ed.). Comparative Biochemistry of Flavonoids. Plenum Press, New York, NY.

    Google Scholar 

  • Harborne, J. B. and Grayer, R. J. 1993. Flavonoids and insects, pp. 589–618, in J. B. Harborne (ed.). The Flavonoids: Advances in Research since 1986. Chapman and Hall, London.

    Google Scholar 

  • Harris, M. K. 1975. Allopatric resistance: searching for sources of insect resistance for use in agriculture. Environ. Entomol. 4:661–669.

    Google Scholar 

  • Hedin, P. A., Parrott, W. L., and Jenkins, J. N. 1991. Effects of cotton plant allelochemicals and nutrients on behavior and development of tobacco budworm. J. Chem. Ecol. 32:262–267.

    Google Scholar 

  • Hedin, P. A. and Waage, S. K. 1986. Roles of flavonoids in plant resistance to insects, pp. 87–100, in V. Cody, E. Middleton, and J. B Harborne (eds.). Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological, and Structure–Activity Relationships. Liss, New York, NY.

    Google Scholar 

  • Hillman, B. I., Lawrence, D. M., and Halpern, B. T. 1996. Characterization and detection of blueberry scorch carlavirus and red ringspot caulimovirus, pp. 83–93, in R. E. Gough and R. F. Korcak (eds.). Blueberries: A Century of Research. Food Products Press. Binghamton, NY.

    Google Scholar 

  • Joerdens-Roettger, D. 1979. The role of phenolic substances for host-selection behaviour of the black bean aphid, Aphis fabae. Entomol. Exp. Appl. 26:49–54.

    CAS  Google Scholar 

  • Karban, R. 1992. Plant variation: its effects on populations of herbivorous insects, pp. 195–215, in R. S. Fritz and E. L. Simms (eds.). Ecology and Evolution of Plant Resistance. University of Chicago Press, Chicago, IL.

    Google Scholar 

  • Kennedy, G. G. and Barbour, J. D. 1992. Resistance variation in natural and managed systems, pp. 13–41, in R. S. Fritz and E. L. Simms (eds.). Ecology and Evolution of Plant Resistance. University of Chicago Press, Chicago, IL.

    Google Scholar 

  • Lattanzio, V., Arpaia, S., Cardinali, A., Di Venere, D., and Linsalata, V. 2000. Role of endogenous flavonoids in resistance mechanism of Vigna to aphids. J. Agric. Food Chem. 48:5316–5320.

    Article  PubMed  CAS  Google Scholar 

  • Lockhart, C. N. and Hall, I. V. 1962. Note on an indication of shoestring virus in the lowbush blueberry, Vaccinium angustifolium Ait. Can. J. Bot. 40:1561–1562.

    Google Scholar 

  • Lyrene, P. M. 1997. Value of various taxa in breeding tetraploid blueberries in Florida. Euphytica. 94:15–22.

    Article  Google Scholar 

  • Lyrene, P. M. and Sherman, W. B. 1980. Horticultural characteristics of native Vaccinium darrowi, V. elliottii, V. fuscatum, and V. myrsinites in Alachua County Florida. J. Am. Soc. Hortic. Sci. 105:393–396.

    Google Scholar 

  • Macleod, A. J. and Pridham, J. B. 1965. Observations on the translocation of phenolic compounds. Phytochemistry 5:777.

    Article  Google Scholar 

  • Maia, A., Luiz, A. J. B., and Campanhola, C. 2000. Statistical inference on associated fertility life table parameters using jackknife technique: computational aspects. J. Econ. Entomol. 93:511–518.

    Google Scholar 

  • Martin, R. R. and Bristow, P. R. 1995. Diseases caused by viruses and mycoplasma like organisms: scorch, pp. 51–53, in F. L. Caruso and D. C. Ramsdell (eds.). Compendium of Blueberry and Cranberry Diseases. American Phytopathological Society Press, St. Paul, MN.

    Google Scholar 

  • Massonie, G. and Maison, P. T1986. Investigations on the resistance of peach varieties to aphid transmission of plum pox virus. Acta Hortic. 193:207–211.

    Google Scholar 

  • Meyer, J. R. and Ballington, J. R. 1990. Resistance of Vaccinium spp. to the leafhopper Scaphytopius magdalensis (Homoptera: Cicadellidae). Ann. Entomol. Soc. Am. 83:515–520.

    Google Scholar 

  • Meyer, J. S., Ingersoll, C. G., McDonald, L. L., and Boyce, M. S. 1986. Estimating uncertainty in population growth rates, jacknife vs. bootstrap techniques. Ecology 67:1156–1166.

    Article  Google Scholar 

  • Montgomery, M. E. and Arn, H. 1974. Feeding response of Aphis pomi, Myzus persicae, and Amphorophora agathonica to phlorizin. J. Insect Physiol. 20:413–421.

    Article  CAS  Google Scholar 

  • Morimoto, K. M. and Ramsdell, D. C. 1985. Aphid vector population dynamics and movement relative to field transmission of blueberry shoestring virus. Phytopathology 75:1217–1222.

    Google Scholar 

  • Mullin, C. A. 1986. Adaptive Divergence of Chewing and Sucking Arthropods to Plant Allelochemicals. Plenum Press, New York.

    Google Scholar 

  • Nichols-Orians, C. M., Frtiz, R. S., and Clausen, T. P. 1993. The genetic basis for variation in the concentration of phenolic glycosides in Salix sericea: Clonal variation and sex-based differences. Biochem. Syst. Ecol. 21:535–542.

    Article  CAS  Google Scholar 

  • Ortiz, R., Vorsa, N., Bruederle, L. P., and Laverty, T. 1999. Pollen viability in natural populations of three North American diploid species of blueberry (Vaccinium, section Cyanococcus). Sci. Hortic. 80:39–48.

    Article  Google Scholar 

  • Peng, Z. and Miles, P. W. 1991. Oxidases in the gut of an aphid, Macrosiphum rosae (L.), and their relation to dietary phenolics. J. Insect Physiol. 37:779–787.

    Article  CAS  Google Scholar 

  • Petitt, F. L., Loader, C. A., and Schon, M. K. 1994. Reduction of nitrogen concentration in the hydroponic solution on population growth rate of the aphids (Homoptera: Aphididae) Aphis gossyppi on cucumber and Myzus persicae on pepper. Environ. Entomol. 23:930–936.

    Google Scholar 

  • Qu, L. and Hancock, J. F. 1997. RAPD-based genetic linkage map of blueberry derived from an interspecific cross between diploid Vaccinium darrowi and tetraploid V. corymbosum. J. Am. Soc. Hortic. Sci. 122:69–73.

    CAS  Google Scholar 

  • Qu, L. and Vorsa, N. 1999. Desynapsis and spindle abnormalities leading to 2n pollen formation in Vaccinium darrowi. Genome 42:35–40.

    Article  Google Scholar 

  • Ranger, C. M., Johnson-Cicalese, J., Polavarapu, S., and Vorsa, N. 2006. Evaluation of Vaccinium spp. for Illinoia pepperi (Hemiptera: Aphididae) performance and phenolic content. J. Econ. Entomol. 99:1474–1482.

    Article  PubMed  CAS  Google Scholar 

  • R Project for Statistical Computing, 2005. Version 2.1.1. http://www.r-project.org/

  • Ramsdell, D. C. 1979. Physical and chemical properties of blueberry shoestring virus. Phytopathology 69:1087–1091.

    Article  CAS  Google Scholar 

  • Raworth, D. A. 2004. Ecology and management of Ericaphis fimbriata (Hemiptera: Aphididae) in relation to the potential for spread of Blueberry scorch virus. Can. Entomol. 136:711–718.

    Google Scholar 

  • SAS Institute. 1996. SAS/STAT Software, Changes and Enhancements through Release 6.11. SAS Institute, Cory, North Carolina, USA.

  • Smith, C. M. 2005. Plant Resistance to Arthropods: Molecular and Conventional Approaches. Springer, Netherlands.

    Book  Google Scholar 

  • Stretch, A. W., Ehlenfeldt, M. K., Brewster, V., Vorsa, N., and Polashock, J. 2001. Resistance of diploid Vaccinium spp. to the fruit rot stage of mummy berry disease. Plant Dis. 85:27–30.

    Google Scholar 

  • Takemura, M., Yasumasa, K., and Nishida, R. 2006. Feeding responses of an oligophagous bean aphid, Megoura crassicauda, to primary and secondary substances in Vicia angustifolia. Entomol. Exp. Appl. 121:51–57.

    Article  Google Scholar 

  • Taruscio, T. G., Barney, D. L., and Exon, J. 2004. Content and profile of flavonoid and phenolic acid compounds in conjunction with the antioxidant capacity for a variety of northwest Vaccinium berries. J. Agric. Food Chem. 52:3169–3176.

    Article  PubMed  CAS  Google Scholar 

  • Terhune, B. T., Ramsdell, D. C., Klomparens, K. L., and Hancock, J. F. 1991. Quantification of blueberry shoestring virus RNA and antigen in its aphid vector, Illinoia pepperi, during acquisition, retention, and transmission. Phytopathology 81:1096–1101.

    CAS  Google Scholar 

  • Vander Kloet, S. P. 1977. Potential and actual gene exchange among three sympatric species of Vaccinium subgenus Cyanococcus in Highlands County, Florida. Can. J. Bot. 55:2668–2672.

    Google Scholar 

  • Van Heerden, F. R., Van Wyk, B. E., Viljoen, A. M., and Steenkamp, P. A. 2003. Phenolic variation in wild populations of Aspalathus linearis (rooibos tea). Biochem. Syst. Ecol. 8:885–895.

    Google Scholar 

  • Vvedenskaya, I. O., Rosen, R. T., Guido, J. E., Russel, D. J., Mills, K. A., and Vorsa, N. 2004. Characterization of flavonols in cranberry (Vaccinium macrocarpon) powder. J. Agric. Food Chem. 52:188–195.

    Article  PubMed  CAS  Google Scholar 

  • Witzell, J., Gref, R., and Näsholm, T. 2003. Plant-part specific and temporal variation in phenolic compounds of boreal bilberry (Vaccinium myrtillus) plants. Biochem. Syst. Ecol. 31:115–127.

    Article  CAS  Google Scholar 

  • Wyatt, I. J. and White, P. R. 1977. Simple estimation of intrinsic increase rates for aphids and tetrancychid mites. J. Appl. Ecol. 14:757–766.

    Article  Google Scholar 

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Acknowledgments

This paper is dedicated to Professor Sridhar Polavarapu (1961–2004), who served as Extension Entomologist for the Philip E. Marucci Center for Blueberry and Cranberry Research and Extension, Rutgers-The State University of New Jersey for 10 years. We thank Michael Reding (Horticultural Insects Research Lab, USDA-ARS, Wooster, OH) and Cesar Rodriguez-Saona (Marucci Center, Rutgers University, Chatsworth, NJ) for reviewing earlier drafts of this manuscript. This work was supported in part by USDA-CSREES 2005-34155-15749 and the New Jersey Agri. Exp. Station project # NJ31912.

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  1. C. M. Ranger

    Present address: Horticultural Insects Research Lab, USDA-ARS, 1680 Madison Ave, Wooster, OH, 44691, USA

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  1. Philip E. Marucci Center for Blueberry and Cranberry Research and Extension, Rutgers-The State University of New Jersey, 125A Lake Oswego Rd., Chatsworth, NJ, 08019, USA

    C. M. Ranger, A. P. Singh, J. Johnson-Cicalese, S. Polavarapu & N. Vorsa

  2. Department of Plant Biology and Pathology, Rutgers-The State University of New Jersey, New Brunswick, NJ, 08901, USA

    A. P. Singh

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Ranger, C.M., Singh, A.P., Johnson-Cicalese, J. et al. Intraspecific Variation in Aphid Resistance and Constitutive Phenolics Exhibited by the Wild Blueberry Vaccinium darrowi . J Chem Ecol 33, 711–729 (2007). https://doi.org/10.1007/s10886-007-9258-5

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