Skip to main content
Log in

Elevated CO2 and virus infection impacts wheat and aphid metabolism

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Introduction

The aphid Rhopalosiphum padi L. is a vector of Barley yellow dwarf virus (BYDV) in wheat and other economically important cereal crops. Increased atmospheric CO2 has been shown to alter plant growth and metabolism, enhancing BYDV disease in wheat. However, the biochemical influences on aphid metabolism are not known.

Objectives

This work aims to determine whether altered host-plant quality, influenced by virus infection and elevated CO2, impacts aphid weight and metabolism.

Methods

Untargeted 1H NMR metabolomics coupled with multivariate statistics were employed to profile the metabolism of R. padi reared on virus-infected and non-infected (sham-inoculated) wheat grown under ambient CO2 (aCO2, 400 µmol mol−1) and future, predicted elevated CO2 (eCO2, 650 µmol mol−1) concentrations. Un-colonised wheat was also profiled to observe changes to host-plant quality (i.e., amino acids and sugars).

Results

The direct impacts of virus or eCO2 were compared. Virus presence increased aphid weight under aCO2 but decreased weight under eCO2; whilst eCO2 increased non-viruliferous (sham) aphid weight but decreased viruliferous aphid weight. Discriminatory metabolites due to eCO2 were succinate and sucrose (in sham wheat), glucose, choline and betaine (in infected wheat), and threonine, lactate, alanine, GABA, glutamine, glutamate and asparagine (in aphids), irrespective of virus presence. Discriminatory metabolites due to virus presence were alanine, GABA, succinate and betaine (in wheat) and threonine and lactate (in aphids), irrespective of CO2 treatment.

Conclusion

This study confirms that virus and eCO2 alter host-plant quality, and these differences are reflected by aphid weight and metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ainsworth, E. A., & Long, S. P. (2005). What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist, 165(2), 351–372.

    Article  PubMed  Google Scholar 

  • Ajayi, B. O. (1986). The effect of barley yellow dwarf virus on the amino acid composition of spring wheat. Annals of Applied Biology, 108(1), 145–149.

    Article  CAS  Google Scholar 

  • Ali, K., Maltese, F., Toepfer, R., Choi, Y. H., & Verpoorte, R. (2011). Metabolic characterization of Palatinate German white wines according to sensory attributes, varieties, and vintages using NMR spectroscopy and multivariate data analyses. Journal of Biomolecular NMR, 49, 255–266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Awmack, C., Harrington, R., Leather, S., & Lawton, J. (1996). The impacts of elevated CO2 on aphid–plant interactions. In R. Froud-Williams, R. Harrington, T. Hocking, H. Smith & T. Thomas (Eds.), Implications of global environmental change for crops in Europe-aspects of applied biology (Vol. 45, pp. 317–322). Cambridge: AAB.

    Google Scholar 

  • Awmack, C., & Leather, S. (2002). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47(1), 817–844.

    Article  CAS  PubMed  Google Scholar 

  • Ball, A. (1997). Microbial decomposition at elevated CO2 levels: Effect of litter quality. Global Change Biology, 3(4), 379–386.

    Article  Google Scholar 

  • Barbehenn, R. V., Chen, Z., Karowe, D. N., & Spickard, A. (2004). C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2. Global Change Biology, 10(9), 1565–1575.

    Article  Google Scholar 

  • Bartelt, R. J., McGuire, M. R., & Black, D. A. (1990). Feeding stimulants for the European corn borer (Lepidoptera: Pyralidae): Additives to a starch-based formulation for Bacillus thuringiensis. Environmental Entomology, 19(1), 182–189.

    Article  Google Scholar 

  • Bosque-Pérez, N. A., & Eigenbrode, S. D. (2011). The influence of virus-induced changes in plants on aphid vectors: Insights from luteovirus pathosystems. Virus Research, 159(2), 201–205.

    Article  PubMed  Google Scholar 

  • Browne, R. A., & Brindle, K. M. (2007). 1H NMR-based metabolite profiling as a potential selection tool for breeding passive resistance against Fusarium head blight (FHB) in wheat. Molecular Plant Pathology, 8(4), 401–410.

    Article  CAS  PubMed  Google Scholar 

  • Ciepiela, A., & Sempruch, C. (1999). Effect of L-3, 4-dihydroxyphenylalanine, ornithine and γγ-aminobutyric acid on winter wheat resistance to grain aphid. Journal of Applied Entomology, 123(5), 285–288.

    Article  CAS  Google Scholar 

  • Colinet, H., & Renault, D. (2012). Metabolic effects of CO2 anaesthesia in Drosophila melanogaster. Biology Letters, 8(6), 1050–1054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conroy, J., & Hocking, P. (1993). Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiologia Plantarum, 89(3), 570–576.

    Article  CAS  Google Scholar 

  • Conroy, J., Seneweera, S., Basra, A., Rogers, G., & Nissen-Wooller, B. (1994). Influence of rising atmospheric CO2 concentrations and temperature on growth, yield and grain quality of cereal crops. Functional Plant Biology, 21(6), 741–758.

    Google Scholar 

  • Dadd, R. H. (1985). Nutrition: Organisms. In G. Kerkut & L. Gilbert (Eds.), Comprehensive insect physiology, biochemistry and phamracology (Vol. 4, pp. 313–390). Oxford: Pergamon Press.

    Google Scholar 

  • Dáder, B., Fereres, A., Moreno, A., & Trębicki, P. (2016). Elevated CO2 impacts bell pepper growth with consequences to Myzus persicae life history, feeding behaviour and virus transmission ability. Scientific Reports, 6, 19120.

    Article  PubMed  PubMed Central  Google Scholar 

  • De Barro, P. J. (1991). Attractiveness of four colours of traps to cereal aphids (Hemiptera: Aphididae) in South Australia. Australian Journal of Entomology, 30(4), 263–264.

    Article  Google Scholar 

  • Dean, G. (1978). Observations on the morphs of Macrosiphum avenae and Metopolophium dirhodum on cereals during the summer and autumn. Annals of Applied Biology, 89(1), 1–7.

    Article  Google Scholar 

  • Dossey, A. T., Walse, S. S., Rocca, J. R., & Edison, A. S. (2006). Single-insect NMR: A new tool to probe chemical biodiversity. ACS Chemical Biology, 1(8), 511–514.

    Article  CAS  PubMed  Google Scholar 

  • Douglas, A. (1998). Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43(1), 17–37.

    Article  CAS  PubMed  Google Scholar 

  • Douglas, A. (2003). The nutritional physiology of aphids. Advances in Insect Physiology, 31, 73–140.

    Article  CAS  Google Scholar 

  • Drake, B. G., Gonzàlez-Meler, M. A., & Long, S. P. (1997). More efficient plants: A consequence of rising atmospheric CO2? Annual Review of Plant Biology, 48(1), 609–639.

    Article  CAS  Google Scholar 

  • Febvay, G., Rahbé, Y., Rynkiewicz, M., Guillaud, J., & Bonnot, G. (1999). Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. Journal of Experimental Biology, 202(19), 2639–2652.

    CAS  PubMed  Google Scholar 

  • Fiebig, M., Poehling, H. M., & Borgemeister, C. (2004). Barley yellow dwarf virus, wheat, and Sitobion avenae: A case of trilateral interactions. Entomologia Experimentalis et Applicata, 110(1), 11–21.

    Article  Google Scholar 

  • Finlay, K., & Luck, J. (2011). Response of the bird cherry-oat aphid (Rhopalosiphum padi) to climate change in relation to its pest status, vectoring potential and function in a crop–vector–virus pathosystem. Agriculture, Ecosystems & Environment, 144(1), 405–421.

    Article  Google Scholar 

  • Fitzgerald, G., Tausz, M., O’Leary, G., Mollah, M., Tausz-Posch, S., Seneweera, S., et al. (2016). Elevated atmospheric [CO2] can dramatically increase wheat yields in semi-arid environments and buffer against heat waves. Global Change Biology, 22, 2269–2284.

    Article  PubMed  Google Scholar 

  • Fuhrer, J. (2003). Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change. Agriculture, Ecosystems & Environment, 97(1–3), 1–20.

    Article  CAS  Google Scholar 

  • Graham, S., Amigues, E., Migaud, M., & Browne, R. (2009a). Application of NMR based metabolomics for mapping metabolite variation in European wheat. Metabolomics, 5(3), 302–306.

    Article  CAS  Google Scholar 

  • Graham, S., Hollis, J., Migaud, M., & Browne, R. (2009b). Analysis of betaine and choline contents of aleurone, bran, and flour fractions of wheat (Triticum aestivum L.) using 1H nuclear magnetic resonance (NMR) spectroscopy. Journal of Agricultural and Food Chemistry, 57(5), 1948–1951.

    Article  CAS  PubMed  Google Scholar 

  • Gray, S., & Gildow, F. E. (2003). Luteovirus–aphid interactions. Annual Review of Phytopathology, 41(1), 539–566.

    Article  CAS  PubMed  Google Scholar 

  • Hawker, J. (1985). Sucrose. In P. M. Dey & R. Dixon (Eds.), Biochemistry of storage carbohydrates in green plants (pp. 1–51). London: Academic Press.

    Google Scholar 

  • Hikosaka, K., Onoda, Y., Kinugasa, T., Nagashima, H., Anten, N. P. R., & Hirose, T. (2005). Plant responses to elevated CO2 concentration at different scales: Leaf, whole plant, canopy, and population. Ecological Research, 20(3), 243–253.

    Article  CAS  Google Scholar 

  • Ingwell, L. L., Eigenbrode, S. D., & Bosque-Pérez, N. A. (2012). Plant viruses alter insect behavior to enhance their spread. Scientific Reports, 2, 1–6.

    Article  Google Scholar 

  • IPCC. (2013). Climate change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.

    Google Scholar 

  • Irwin, M. E., & Thresh, J. M. (1990). Epidemiology of barley yellow dwarf: A study in ecological complexity. Annual Review of Phytopathology, 28(1), 393–424.

    Article  Google Scholar 

  • Jensen, S. G., & D’Arcy, C. J. (1995). Effects of barley yellow dwarf on host plants. In C. J. D’Arcy & P. A. Burnett (Eds.), Barley yellow dwarf: 40 years of progress (Vol. 40, pp. 55–74). St Paul: The American Phytopathological Society.

    Google Scholar 

  • Jiménez-Martínez, E. S., Bosque-Pérez, N. A., Berger, P. H., Zemetra, R. S., Ding, H., & Eigenbrode, S. D. (2004). Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology, 33(5), 1207–1216.

    Article  Google Scholar 

  • Kimball, B., Kobayashi, K., & Bindi, M. (2002). Responses of agricultural crops to free-air CO2 enrichment. Advances in Agronomy, 77, 293–368.

    Article  Google Scholar 

  • Kimball, B., Pinter, P., Garcia, R., LaMorte, R., Wall, G., Hunsaker, D., et al. (1995). Productivity and water use of wheat under free-air CO2 enrichment. Global Change Biology, 1(6), 429–442.

    Article  Google Scholar 

  • Krumbein, A., Kläring, H. P., Schonhof, I., & Schreiner, M. (2010). Atmospheric carbon dioxide changes photochemical activity, soluble sugars and volatile levels in broccoli (Brassica oleracea var. italica). Journal of Agricultural and Food Chemistry, 58(6), 3747–3752.

    Article  CAS  PubMed  Google Scholar 

  • Leckstein, P., & Llewellyn, M. (1974). The role of amino acids in diet intake and selection and the utilization of dipeptides by Aphis fabae. Journal of Insect Physiology, 20(5), 877–885.

    Article  CAS  PubMed  Google Scholar 

  • Lenz, E., Hägele, B., Wilson, I., & Simpson, S. (2001). High resolution 1H NMR spectroscopic studies of the composition of the haemolymph of crowd-and solitary-reared nymphs of the desert locust, Schistocerca gregaria. Insect Biochemistry and Molecular Biology, 32(1), 51–56.

    Article  CAS  PubMed  Google Scholar 

  • Li, F., Kang, S., & Zhang, J. (2004). Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat. Agricultural Water Management, 67(3), 221–233.

    Article  Google Scholar 

  • Malmström, C., & Field, C. (1997). Virus-induced differences in the response of oat plants to elevated carbon dioxide. Plant, Cell & Environment, 20(2), 178–188.

    Article  Google Scholar 

  • Moriwaki, N., Matsushita, K., Nishina, M., & Kono, Y. (2003). High concentrations of trehalose in aphid hemolymph. Applied Entomology and Zoology, 38(2), 241–248.

    Article  CAS  Google Scholar 

  • Nancarrow, N., Constable, F. E., Finlay, K. J., Freeman, A. J., Rodoni, B. C., Trębicki, P., et al. (2014). The effect of elevated temperature on Barley yellow dwarf virus-PAV in wheat. Virus Research, 186, 97–103.

    Article  CAS  PubMed  Google Scholar 

  • Oehme, V., Högy, P., Zebitz, C. P., & Fangmeier, A. (2013). Effects of elevated atmospheric CO2 concentrations on phloem sap composition of spring crops and aphid performance. Journal of Plant Interactions, 8(1), 74–84.

    Article  CAS  Google Scholar 

  • Phalaraksh, C., Reynolds, S. E., Wilson, I. D., Lenz, E. M., Nicholson, J. K., & Lindon, J. C. (2008). A metabonomic analysis of insect development: 1H-NMR spectroscopic characterization of changes in the composition of the haemolymph of larvae and pupae of the tobacco hornworm, Manduca sexta. ScienceAsia, 34(3), 279–286.

    Article  CAS  Google Scholar 

  • Reich, P. B., Hungate, B. A., & Luo, Y. (2006). Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecolology, Evolution and Systematics, 37, 611–636.

    Article  Google Scholar 

  • Sasaki, T., & Ishikawa, H. (1995). Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 41(1), 41–46.

    Article  CAS  Google Scholar 

  • Seneweera, S. P., Conroy, J. P., Ishunaru, K., Ghannoum, O., Okada, M., Lieffering, M., et al. (2002). Changes in source-sink relations during development influence photosynthetic acclimation of rice to free air CO2 enrichment (FACE). Functional Plant Biology, 29, 945–953.

    Article  CAS  Google Scholar 

  • Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., & Ishikawa, H. (2000). Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature, 407(6800), 81–86.

    Article  CAS  PubMed  Google Scholar 

  • Snart, C. J., Hardy, I. C., & Barrett, D. A. (2015). Entometabolomics: Applications of modern analytical techniques to insect studies. Entomologia Experimentalis et Applicata, 155(1), 1–17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stiling, P., & Cornelissen, T. (2007). How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biology, 13(9), 1823–1842.

    Article  Google Scholar 

  • Sumner, L. W., Amberg, A., Barrett, D., Beale, M. H., Beger, R., Daykin, C. A., et al. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics, 3(3), 211–221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, Y. C., & Ge, F. (2011). How do aphids respond to elevated CO2? Journal of Asia-Pacific Entomology, 14, 217–220.

    Article  Google Scholar 

  • Team, R. C. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, 2012. ISBN 3-900051-07-0.

    Google Scholar 

  • Thompson, S. (2001). Parasitism enhances the induction of glucogenesis by the insect, Manduca sexta L. The International Journal of Biochemistry & Cell Biology, 33(2), 163–173.

    Article  CAS  Google Scholar 

  • Thompson, S., Lee, R., & Beckage, N. (1990). Metabolism of parasitized Manduca sexta examined by nuclear magnetic resonance. Archives of Insect Biochemistry and Physiology, 13(1-2), 127–143.

    Article  CAS  Google Scholar 

  • Trębicki, P., Nancarrow, N., Cole, E., Bosque-Pérez, N. A., Constable, F. E., Freeman, A. J., et al. (2015). Virus disease in wheat predicted to increase with a changing climate. Global Change Biology, 21(9), 3511–3519.

    Article  PubMed  Google Scholar 

  • Trębicki, P., Vandegeer, R. K., Bosque-Pérez, N. A., Powell, K. S., Dader, B., Freeman, A. J., et al. (2016). Virus infection mediates the effects of elevated CO2 on plants and vectors. Scientific Reports, 6, 22785.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vassiliadis, S., Plummer, K., Powell, K., Trębicki, P., Luck, J., & Rochfort, S. (2016). The effect of elevated CO2 and virus infection on the primary metabolism of wheat. Functional Plant Biology, 43, 892–902.

    CAS  Google Scholar 

  • Verberk, W., Sommer, U., Davidson, R., & Viant, M. (2013). Anaerobic metabolism at thermal extremes: A metabolomic test of the oxygen limitation hypothesis in an aquatic insect. Integrative and Comparative Biology, 53(4), 609–619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Carolan, J. C., Hao, F., Nicholson, J. K., Wilkinson, T. L., & Douglas, A. E. (2010). Integrated metabonomic-proteomic analysis of an insect-bacterial symbiotic system. Journal of Proteome Research, 9(3), 1257–1267.

    Article  CAS  PubMed  Google Scholar 

  • Watt, A., Whittaker, J., Docherty, M., Brooks, G., Lindsay, E., & Salt, D. (1995). The impact of elevated atmospheric CO2 on insect herbivores. Insects in a Changing Environment, 1, 197–217.

    Google Scholar 

  • Wilcoxon, F. (1945). Individual comparisons by ranking methods. Biometrics Bulletin, 1, 80–83.

    Article  Google Scholar 

  • Williams, C. (1995). Effects of plant age and condition on the population dynamics of Myzus persicae Sulz. on sugar beet in field plots. Bulletin of Entomological Research, 85, 557–567.

    Article  Google Scholar 

  • Wishart, D. S., Jewison, T., Guo, A. C., Wilson, M., Knox, C., Liu, Y., et al. (2013). HMDB 3.0—The human metabolome database in 2013. Nucleic Acids Research, 41, D801–D807.

    Article  CAS  PubMed  Google Scholar 

  • Wu, R., Wu, Z., Wang, X., Yang, P., Yu, D., Zhao, C., et al. (2012). Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts. Proceedings of the National Academy of Sciences, 109(9), 3259–3263.

    Google Scholar 

  • Wyatt, G. (1967). The biochemistry of sugars and polysaccharides in insects. Advances in Insect Physiology, 4, 287–360.

    Article  CAS  Google Scholar 

  • Zhang, F., Dossey, A. T., Zachariah, C., Edison, A. S., & Brüschweiler, R. (2007). Strategy for automated analysis of dynamic metabolic mixtures by NMR. Application to an insect venom. Analytical Chemistry, 79(20), 7748–7752.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr Piotr Trębicki (DEDJTR, Horsham) for supplying wheat seeds, virus strain and aphid colonies, and Dr Myrna Deseo (DEDJTR, Bundoora) for assistance with 1H NMR protocol and metabolite identification. We would also like to thank Dr Rebecca Vandegeer for assisting with the maintenance of plants and aphid colonies.

Funding

This work was supported by La Trobe University and the Department of Economic Development, Jobs, Transport and Resources (DEDJTR), Victoria.

Author information

Authors and Affiliations

Authors

Contributions

SV designed the work, performed the experiments, analysed the data and drafted the manuscript. KP and KP supervised the study and edited the manuscript. SR helped provide financial support, supervised the study, assisted in data analysis and edited the manuscript.

Corresponding author

Correspondence to Simone Vassiliadis.

Ethics declarations

Conflict of interest

S. Vassiliadis, K. Plummer, K. Powell and S. Rochfort have no conflict of interest to declare.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent and ethical approval was not required for this study.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vassiliadis, S., Plummer, K.M., Powell, K.S. et al. Elevated CO2 and virus infection impacts wheat and aphid metabolism. Metabolomics 14, 133 (2018). https://doi.org/10.1007/s11306-018-1425-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11306-018-1425-x

Keywords

Navigation