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Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition?

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Abstract

Plants provide aphids with unbalanced and low concentrations of amino acids. Likely, intracellular symbionts improve the aphid nutrition by participating to the synthesis of essential amino acids. To compare the aphid amino acid uptakes from the host plant and the aphids amino acid excretion into the honeydew, host plant exudates (phloem + xylem) from infested and uninfested Vicia faba L. plants were compared to the honeydew produced by two aphid species (Acyrthosiphon pisum Harris and Megoura viciae Buckton) feeding on V. faba. Our results show that an aphid infestation modifies the amino acid composition of the infested broad bean plant since the global concentration of amino acids significantly increased in the host plant in response to aphid infestations. Specifically, the concentrations of the two amino acids glutamine and asparagine were strongly enhanced. The amino acid profiles from honeydews were similar for the two aphid species, but the concentrations found in the honeydews were generally lower than those measured in the exudates of infested plants (aphids uptakes). This work also highlights that aphids take large amounts of amino acids from the host plant, especially glutamine and asparagine, which are converted into glutamic and aspartic acids but also into other essential amino acids. The amino acid profiles differed between the host plant exudates and the aphid excretion product. Finally, this study highlights that the pea aphid, a “specialist” for the V. faba host plant, induced more important modifications into the host plant amino acid composition than the “generalist” aphid M. viciae.

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References

  • Arakaki N, Hattori M (1998) Difference in the quality of honeydew from first instar soldier nand ordinary morph nymphs of the bamboo aphid, Pseudoregma koshunensis (Takahashi) (Homoptera: Aphididae). Appl Entomol Zool 33:357–361

    Google Scholar 

  • Auclair JL (1963) Aphid feeding and nutrition. Ann Rev Entomol 8:439–490

    Article  Google Scholar 

  • Cloutier C (1986) Amino acid utilization in the aphid Acyrthosiphon pisum infected by the parasitoid Aphidius smithi. J Insect Physiol 32:263–267

    Article  CAS  Google Scholar 

  • Cull DC, van Emden HF (1977) The effect on Aphis fabae of diel changes in their food quality. Phys Ent 2:109–115

    Article  Google Scholar 

  • Dorschner KW, Ryan JD, Johnson RC, Eikenbary RD (1987) Modification of host nitrogen levels by the greenbug (Homoptera: Aphididae): its role in resistance of winter wheat to aphids. Env Entomol 16:1007–1011

    Google Scholar 

  • Douglas AE (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecol Entomol 18:31–38

    Article  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbal symbioses: aphids and their symbiotic bacteria Buchnera. Ann Rev Entomol 43:17–37

    Article  CAS  Google Scholar 

  • Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57(4):747–754

    Article  PubMed  CAS  Google Scholar 

  • Douglas AE, Prasser WA (1992) Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J Insect Physiol 38:565–568

    Article  CAS  Google Scholar 

  • Dreger-Jauffret F, Shorthouse JD (1992) Diversity of gall-inducing insects and their galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, Oxford, pp 8–33

    Google Scholar 

  • Faria CA, Wäckers FL, Turlings TCJ (2008) The nutritional value of aphid honeydew for non-aphid parasitoids. Basic and Appl Ecol 9(3):286–297

    Article  Google Scholar 

  • Febvay G, Rahbe Y, Rynkiewicz M et al (1999) Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. J Exp Biol 202:2639–2652

    PubMed  CAS  Google Scholar 

  • Fischer MK, Shingleton AW (2001) Host plant and ants influence the honeydew sugar composition of aphids. Funct Ecol 15:544–550

    Article  Google Scholar 

  • Fisher MK, Völkl W, Schopf R, Hoffmann KH (2002) Age-specific patterns in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant-attendance. J Insect Physiol 48:319–326

    Article  Google Scholar 

  • Girousse C, Bonnemain JL, Delrot S, Bournoville R (1991) Sugar and amino acid composition of phloem sap of Medicago sativa: a comparative study of two collecting methods. Plant Physiol Biochem 29:41–48

    CAS  Google Scholar 

  • Hawkins CDB, Whitecross MI, Aston MJ (1986) Interactions between aphid infestation and plant growth and uptake of nitrogen and phosphorus by three leguminous host plants. Can J Bot 64:2362–2367

    Article  CAS  Google Scholar 

  • Hendrix DL, Wie Y, Leggett JE (1992) Homopteran honeydew sugar composition is determined by both the insect and plant species. Comp Biochem Physiol A 101B:23–72

    CAS  Google Scholar 

  • Hogervorst P, Wäckers F, Romeis J (2007) Effects of honeydew sugar composition on the longevity of Aphidius ervi. Entomol Exp Appl 122:223–232

    Article  CAS  Google Scholar 

  • Karley AJ, Douglas AE, Parker WE (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for Aphids. J Exp Biol 205:3009–3018

    PubMed  CAS  Google Scholar 

  • Malcolm SB (1990) Chemical defence in chewing and sucking insect herbivores: plant-derived cardenolides in the monarch butterfly and oleander aphid. Chemoecology 1:12–21

    Article  CAS  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • Mittler TE (1958) Studies on the feeding and nutrition of Tuberolachnus salignus II the nitrogen and sugar composition of ingested phloem sap and excreted honeydew. J Exp Biol 35:74–84

    CAS  Google Scholar 

  • Olmstead KL, Denno RF, Morton TC, Romeo JT (1997) Influence of Prokelisia plant hoppers on amino acid composition and growth of Spartina alterniflora. J Chem Ecol 23:303–321

    Article  CAS  Google Scholar 

  • Petersen MK, Sandström JP (2001) Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Funct Ecol 15:525–534

    Article  Google Scholar 

  • Poehling HM (1985) Einfluss von Aphis fabae Scop (Homoptera, Aphididae) auf den Protein und Aminosäurestoffwechsel von Vicia faba Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte. Entomol 4:366–369

    Google Scholar 

  • Prosser WA, Douglas AE (1991) The aposymbiotic aphid: an analysis of chlortetracycline-treated pea aphid, Acyrthosiphon pisum. J Insect Physiol 37:713–719

    Article  CAS  Google Scholar 

  • Rhodes JD, Croghan PC, Dixon AFG (1996) Uptake, excretion and respiration of sucrose and amino acids by the pea aphid Acyrthosiphon pisum. J Exp Biol 199:1269–1276

    PubMed  CAS  Google Scholar 

  • Riedell WE (1989) Effect of Russian wheat aphid infestation on barley plant response to drought stress. Physiol Plant 77:587–592

    Article  CAS  Google Scholar 

  • Saheed SA, Botha CEJ, Liu L, Jonsson L (2007) Comparison of structural damage caused by Russian wheat aphid (Diuraphis noxia) and Bird cherryoat aphid (Rhopalosiphum padi) in a susceptible barley cultivar, Hordeum vulgare cv. Clipper. Physiol Plant 129:429–435

    Article  CAS  Google Scholar 

  • Sandström J, Moran N (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91:203–210

    Article  Google Scholar 

  • Sandström J, Moran N (2001) Amino acid budgets in three aphid species using the same host plant. Physiol Entomol 26(3):202–211

    Article  Google Scholar 

  • Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947–955

    Article  Google Scholar 

  • Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J Insect Physiol 46:33–40

    Article  PubMed  Google Scholar 

  • Sasaki T, Ishikawa H (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 41:41–46

    Article  CAS  Google Scholar 

  • Sasaki T, Aoki T, Hayashi H, Ishikawa H (1990) Amino acid composition of the honeydew of symbiotic and aposymbiotic pea aphids Acyrthosiphon pisum. J Insect Physiol 36:35–40

    Article  CAS  Google Scholar 

  • Sasaki T, Fukuchi N, Ishikawa H (1993) Amino acid flow through aphid and its symbiont: studies with 15 N-labeled glutamine. Zool Sci 10:787–791

    CAS  Google Scholar 

  • Shigenobu S, Watanabe H, Hattori M et al (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86

    Article  PubMed  CAS  Google Scholar 

  • Smith KM (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plant. Ann Appl Biol 13:109–139

    Article  Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold London

  • Spiller NJ, Koenders L, Tjallingii WF (1990) Xylem ingestion by aphid–a strategy for maintaining water balance. Entomol Exp Appl 55:101–104

    Article  Google Scholar 

  • Tedders WL, Thompson JM (1981) Histological investigation of stylet penetration and feeding damage to pecan foliage by three aphids (Hemiptera (Homoptera): Aphididae). In: Johnson D (ed) Tree fruit and nut pest management in the Southeastern United States. Entomological Society of America, Lanham, pp 69–83

    Google Scholar 

  • Telang A, Sandström J, Dyreson E, Moran NA (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol Exp Appl 91:403–412

    Article  Google Scholar 

  • Tjallingii WF (1994) Regulation of phloem sap feeding by aphids. In: Chapman GF, De Beor G (eds) Regulatory mechanisms in insect feeding. Chapman and Hall, New York, pp 190–209

    Google Scholar 

  • Urich K (1994) Comparative animal biochemistry. Springer-Verlag, Berlin

    Google Scholar 

  • Wäckers FL (2000) Do oligosaccharides reduce the suitability of honeydew for predators and parasitoids? A further facet to the function of insect-synthesized honeydew sugars. Oikos 90:197–201

    Article  Google Scholar 

  • Wäckers FL (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 17–74

    Chapter  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Weibull J, Ronquist F, Brishammar S (1990) Free amino acid composition of leaf exudates and phloem sap. Plant Physiol 92:222–226

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson TL, Douglas AE (1995) Why pea aphids (Acyrthosiphon pisum) lacking symbiotic bacteria have elevated levels of the amino acid glutamine. J Insect Physiol 41(11):921–927

    Article  CAS  Google Scholar 

  • Wilkinson TL, Ashford DA, Pritchard J, Douglas AE (1997) Honeydew sugars and osmoregulation in the pea aphid Acyrthosiphon pisum. J Exp Biol 200:2137–2143

    PubMed  CAS  Google Scholar 

  • Woodring J, Wiedemann R, Fischer MK et al (2004) Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiol Entomol 29:311–319

    Article  CAS  Google Scholar 

  • Yao I, Akimoto SI (2001) Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola. Oecologia 128:36–43

    Article  Google Scholar 

  • Yao I, Akimoto SI (2002) Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola. Ecol Entomol 27:745–752

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded by the Walloon Region Ministry Grant (WALEO2: SOLAPHIDRW/FUSAGX 061/6287).

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Authors and Affiliations

  1. Department of Functional and Evolutionary Entomology, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2, 5030, Gembloux, Belgium

    Pascal D. Leroy, Frédéric Francis, François J. Verheggen, Quentin Capella & Eric Haubruge

  2. Industrial Biological Chemistry Unity, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2, 5030, Gembloux, Belgium

    Bernard Wathelet

  3. Walloon Center of Industrial Biology, University of Liege, B40, 4000, Sart-Tilman, Belgium

    Ahmed Sabri & Philippe Thonart

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  1. Pascal D. Leroy
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Correspondence to Pascal D. Leroy.

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Leroy, P.D., Wathelet, B., Sabri, A. et al. Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition?. Arthropod-Plant Interactions 5, 193–199 (2011). https://doi.org/10.1007/s11829-011-9128-5

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