Abstract
Key message
Phloeomyzus passerinii can induce a pseudogall within the bark of susceptible poplar genotypes, while in resistant genotypes the induction seems to be impeded by lignification processes.
Abstract
Phloeomyzus passerinii is a major pest of poplar stands in Europe, North Africa and the Near East. This aphid feeds in the cortical parenchyma of different poplar species and hybrids, and can affect their growth and survival through unknown mechanisms. In some genotypes, however, resistance prevents either the settlement or the development of aphid colonies. For a better understanding of tree reactions to aphid probing, we compared the anatomical and biochemical modifications undergone within the bark of stem cuttings, after different delays of either aphid colonization or mechanical wounding. To assess how resistance may modulate tree reactions, the comparison was performed using three poplar genotypes exhibiting different resistance levels. In these three genotypes, mechanical wounding induced a similar, localized, wound periderm. In contrast, aphid colonization triggered more extended reactions, which differed among genotypes. In the susceptible genotype, aphids induced a reaction tissue, characterized after a month by thin-walled hypertrophied cells and a depletion of soluble phenolic compounds and starch. Anatomical features of this reaction tissue suggest that the aphid initiates a pseudogall in the cortical tissues of its susceptible host. In the resistant genotypes, however, the differentiation of the reaction tissue was totally or partially inhibited, probably because of extended lignification processes. The implications of a pseudogall induction on susceptible hosts’ physiology, and the impact of lignification on aphid development and behavior, are discussed.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Amman GD, Speers CF (1965) Balsam woolly aphid in the Southern Appalachians. J For 63:18–20
Arru GM (1974) Metodo per valutare la resistenza dei pioppi all’Afide lanigero (Phloeomyzus passerinii Sign). Cellulosa e Carta 25:45–49
Arzone A, Vidano C (1984) Indagini su Phloeomyzus passerinii (Sign.) in Piemonte. Ann Fac Sci Agrari Univ Stud Torino 13:337–356
Balch RE, Clark J, Bonga JM (1964) Hormonal action in production of tumours and compression wood by an aphid. Nature 22:721–722
Baubet O, Caroulle F (2009) Bilan de la Santé des Forêts en 2008. Peupleraie française: entre rouille et puceron lanigère, l’inquiétude demeure. Min. Agr. Pêche, Paris
Biggs AR (1984) Intracellular suberin occurrence and detection in tree bark. IAWA Bull 5:243–248
Biggs AR (1992) Anatomical and physiological responses of bark tissues to mechanical injuries. In: Blanchette RA, Biggs AR (eds) Defense mechanisms of woody plants against fungi. Springer-Verlag, Berlin, pp 13–40
Biggs AR, Merrill W, Davis DD (1984) Discussion: response of bark tissues to injury and infection. Can J For Res 14:351–356
Blackman RL, Eastop VF (1994) The Aphids. In: Blackman RL, Eastop VF (eds) Aphids on the world’s trees: an identification and information guide. CAB International in association with the Natural History Museum, London, pp 95–108
Bostock RM, Stermer BA (1989) Perspectives on wound healing in resistance to pathogens. Ann Rev Phytopathol 27:343–371
Bronner R (1992) The role of nutritive cells in the nutrition of Cynipids and Cecidomyiids. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 102–117
Brown MW, Glenn DM, Wisniewski ME (1991) Functional and anatomical disruption of apple roots by the woolly apple aphid (Homoptera: Aphididae). J Econ Entomol 84:1823–1826
Collins CM, Rosado RG, Leather SR (2001) The impact of aphids Tuberolachnus salignus and Pterocomma salicis on willow trees. Ann Appl Biol 138:133–140
Deysson G (1954) Eléments d’anatomie des plantes vasculaires. Sedes, Paris, p 266
Divol F, Vilaine F, Thibivilliers S, Kusiak C, Sauge MH, Dinant S (2007) Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environ 30:187–201
Dixon AFG (1971) The role of aphids in wood formation. I. The effect of the Sycamore aphid, Drepanosiphum platanoides (Schr.) (Aphididae), Acer pseudoplatanus (L.). J Appl Ecol 8:165–179
Eyles A, Bonello P, Ganley R, Mohammed C (2010) Induced resistance to pests and pathogens in trees. New Phytol 185:893–908
Fernandes GW, Negreiros D (2001) The occurrence and effectiveness of hypersusceptible reaction against galling herbivores across host taxa. Ecol Entomol 26:46–55
Forneck A, Kleinmann S, Blaich R, Anvari SF (2002) Histochemistry and anatomy of phylloxera (Daktulosphaira vitifoliae) nodosities on young roots of grapevine (Vitis spp.). Vitis 41:93–97
Höglund S, Larsson S, Wingsle G (2005) Both hypersusceptible and non-hypersusceptible responses are associated with resistance in Salix viminalis against the gall midge Dasineura marginemtorquens. J Exp Bot 56:3215–3222
Hollingsworth RG, Hain FP (1991) Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-fir decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Fla Entomol 74:179–187
Lieutier F, Berryman AA (1988) Preliminary histological investigations on the defense reactions of three pines to Ceratocystis clavigera and two chemical elicitors. Can J For Res 18:1243–1247
Miles PW (1989) Specific responses and damage caused by Aphidoidea. In: Minks AK, Harrewijn P (eds) Aphids: their Biology, Natural Enemies and Control, vol 2C. Elsevier, Amsterdam, pp 23–47
Mullick DB (1977) The non-specific nature of defense in bark and wood during wounding, insect and pathogen attack. Rec Adv Phytochem 11:395–441
Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA 97:13184–13187
Orondo SBO, Day RK (1994) Cypress aphid (Cinara cupressi) damage to a cypress (Cupressus lusitanica) stand in Kenya. Int J Pest Manag 40:140–144
Pepin R, Boumendil J (1982) Préservation de l’ultrastructure du sclérote de Sclerotinia tuberosa (Champignon Discomycète); un modèle pour la préparation des échantillons imperméables et hétérogènes. Cytology 47:359–377
Philippe RN, Bohlmann J (2007) Poplar defence against insects herbivores. Can J Bot 85:1111–1126
Pointeau S, Sallé A, Lesieur V, Bankhead-Dronnet S, Bonnaffoux M, Lieutier F (2011) Estimating the effect of poplar resistance on the performance of the woolly poplar aphid, Phloeomyzus passerinii, in various experimental conditions. Can J For Res 41:1233–1241
Pointeau S, Ameline A, Laurans F, Sallé A, Rahbé Y, Bankhead-Dronnet S, Lieutier F (2012) Exceptional plant penetration and feeding upon cortical parenchyma cells by the woolly poplar aphid. J Insect Physiol 58:857–866
Pointeau S, Ameline A, Sallé A, Bankhead-Dronnet S, Lieutier F (2013) Characterization of antibiosis and antixenosis to the woolly poplar aphid (Hemiptera: Aphididae) in the bark of different poplar genotypes. J Econ Entomol 106:473–481
Pollard DC (1973) Plant penetration by feeding aphids (Hemiptera, Aphidoidea): a review. Bull Entomol Res 62:631–714
Price PW, Fernandes GW, Waring GL (1987) The adaptive nature of insect galls. Environ Entomol 16:15–24
Raman A, Beiderbeck R, Herth W (2009) Early subcellular responses of susceptible and resistant Vitis taxa to feeding by grape phylloxera Daktulosphaira vitifoliae. Bot Helv 119:31–39
Rangasamy M, Rathinasabapathi B, McAuslane HJ, Cherry RH, Nagata RT (2009) Role of leaf sheath lignification and anatomy in resistance against southern chinch bug (Hemiptera: Blissidae) in St. Augustinegrass. J Econ Entomol 102:432–439
Rey LA (1992) Developmental morphology of two types of Hymenopterous galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 87–101
Rohfritsch O (1992) Patterns in gall development. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 60–86
Rohfritsch O, Anthony M (1992) Strategies in gall induction by two groups of Homopterans. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 102–117
Sadeghi SE, Rajabi-Mazhar NA, Moharramipour S (2007) A study on the incidence of woolly poplar aphid, Phloeomyzus passerinii (Hom.: Aphididae) on poplar species and clones in Hamedan province. Iran J Entomol Soc 26:47–59
Saltzmann KD, Giovanini MP, Zheng C, Williams CE (2008) Virulent Hessian fly larvae manipulate the free amino acid content of host wheat plants. J Chem Ecol 34:1401–1410
Sauge MH, Kervella J, Pascal T (1998) Settling behaviour and reproductive potential of the green peach aphid Myzus persicae on peach varieties and a related wild Prunus. Entomol Exp Appl 89:233–242
Shannon RE, Brewer JW (1980) Starch and sugar levels in three coniferous insect galls. Z Angew Entomol 89:526–533
Straw NA, Fielding N, Green G, Price J, Williams D (2011) Defoliation and growth relationships for mid-rotation Sitka spruce attacked by the green spruce aphid, Elatobium abietinum (Walker) (Homoptera: Aphididae). For Ecol Manag 262:1223–1235
Suzuki D, Fukushi Y, Ashimoto SI (2009) Do aphid galls provide good nutrients for the aphids? Comparisons of amino acid concentrations in galls among Tetraneura species (Aphididae: Eriosomatinae). Arthropod Plant Interact 3:241–247
Tjallingii WF, HogenEsch TH (1993) Fine structure of aphid stylet routes in plant tissue in correlation with EPG signals. Physiol Entomol 18:317–328
van Emden HF (2007) Host-plant resistance. In: van Emdem HF, Harrington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 447–462
Wagner MR, Clancy KM, Lieutier F (2002) Mechanisms and deployment of resistance in trees to insects. Kluwer Academic Publishers, Dordrecht
Weiland JE, Stanosz GR (2007) The histology of hybrid poplar clones inoculated with Septoria musiva. Plant Dis 91:1524–1530
Wood BW, Tedders WL, Dutcher JD (1987) Energy drain of three pecan aphid species (Homoptera: Aphididae) and their influence on in-shell pecan production. Environ Entomol 16:1045–1056
Acknowledgments
This work was supported by a grant from the French Ministry of Agriculture, Food Processing and Forest. The PhD thesis of F. Dardeau is granted by the French Ministry of Higher Education and Research. We thank Cécile Montécot-Dubourg and Stéphane Mortaud for their technical assistance with autofluorescence, and Sophie Pointeau for her earlier comments on the manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U. Luettge.
Rights and permissions
About this article
Cite this article
Dardeau, F., Deprost, E., Laurans, F. et al. Resistant poplar genotypes inhibit pseudogall formation by the wooly poplar aphid, Phloeomyzus passerinii Sign. Trees 28, 1007–1019 (2014). https://doi.org/10.1007/s00468-014-1014-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-014-1014-1


