Increased insect herbivore performance under elevated CO2 is associated with lower plant defence signalling and minimal declines in nutritional quality


  • 1.

    Gregory, P. J., Johnson, S. N., Newton, A. C. & Ingram, J. S. I. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827–2838 (2009).

    CAS 
    Article 

    Google Scholar
     

  • 2.

    Birch, A. N. E., Begg, G. S. & Squire, G. R. How agro-ecological research helps to address food security issues under new IPM and pesticide reduction policies for global crop production systems. J. Exp. Bot. 62, 3251–3261 (2011).

    CAS 
    Article 

    Google Scholar
     

  • 3.

    Johnson, S. N. & Jones, T. H. Global Climate Change and Terrestrial Invertebrates (John Wiley & Son Ltd., New York, 2017).


    Google Scholar
     

  • 4.

    Robinson, E. A., Ryan, G. D. & Newman, J. A. A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol. 194, 321–336 (2012).

    CAS 
    Article 

    Google Scholar
     

  • 5.

    Zavala, J. A., Nabity, P. D. & DeLucia, E. H. An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu. Rev. Entomol. 58, 79–97 (2013).

    CAS 
    Article 

    Google Scholar
     

  • 6.

    Ode, P. J., Johnson, S. N. & Moore, B. D. Atmospheric change and induced plant secondary metabolites—Are we reshaping the building blocks of multi-trophic interactions? Curr. Opin. Ins. Sci. 5, 57–65 (2014).

    Article 

    Google Scholar
     

  • 7.

    DeLucia, E. H., Nabity, P. D., Zavala, J. A. & Berenbaum, M. R. Climage change: Resetting plant–insect interactions. Plant Physiol. 160, 1677–1685 (2012).

    CAS 
    Article 

    Google Scholar
     

  • 8.

    Facey, S. L., Ellsworth, D. S., Staley, J. T., Wright, D. J. & Johnson, S. N. Upsetting the order: How climate and atmospheric change affects herbivore–enemy interactions. Curr. Opin. Insect Sci. 5, 66–74 (2014).

    Article 

    Google Scholar
     

  • 9.

    Newman, J. A., Anand, M., Henry, H. A. L., Hunt, S. & Gedalof, Z. Climate Change Biology (CABI, 2011).

  • 10.

    Mattson, W. J. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11, 119–161 (1980).

    Article 

    Google Scholar
     

  • 11.

    Drake, B. G., Gonzalez-Meler, M. A. & Long, S. P. More efficient plants: A consequence of rising atmospheric CO2Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 609–639 (1997).

    CAS 
    Article 

    Google Scholar
     

  • 12.

    Stiling, P. & Cornelissen, T. 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. Glob. Change Biol. 13, 1823–1842 (2007).

    ADS 
    Article 

    Google Scholar
     

  • 13.

    Pang, J. et al. A new explanation of the N concentration decrease in tissues of rice (Oryza sativa L.) exposed to elevated atmospheric pCO2. Environ. Exp. Bot. 57, 98–105 (2006).

  • 14.

    Taub, D. R. & Wang, X. Z. Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J. Integr. Plant Biol. 50, 1365–1374 (2008).

    CAS 
    Article 

    Google Scholar
     

  • 15.

    Howe, G. A. & Jander, G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59, 41–66 (2008).

    CAS 
    Article 

    Google Scholar
     

  • 16.

    Wu, J. Q. & Baldwin, I. T. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44, 1–24 (2010).

    CAS 
    Article 

    Google Scholar
     

  • 17.

    Erb, M., Meldau, S. & Howe, G. A. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17, 250–259 (2012).

    CAS 
    Article 

    Google Scholar
     

  • 18.

    Anderson, C. J. et al. Hybridization and gene flow in the mega-pest lineage of moth, Helicoverpa. Proc. Natl. Acad. Sci. U.S.A. 115, 5034–5039 (2018).

    CAS 
    Article 

    Google Scholar
     

  • 19.

    Jones, C. M., Parry, H., Tay, W. T., Reynolds, D. R. & Chapman, J. W. Movement ecology of pest Helicoverpa: Implications for ongoing spread. Annu. Rev. Entomol. 64, 277–295 (2019).

    CAS 
    Article 

    Google Scholar
     

  • 20.

    Sharma, H. C. et al. Elevated CO2 influences host plant defense response in chickpea against Helicoverpa armigera. Arthropod-Plant Interact. 10, 171–181 (2016).

    Article 

    Google Scholar
     

  • 21.

    Khadar, B. A., Prabhuraj, A., Rao, M. S., Sreenivas, A. G. & Naganagoud, A. Influence of elevated CO2 associated with chickpea on growth performance of gram caterpillar, Helicoverpa armigera (Hüb.). Appl. Ecol. Environ. Res. 12, 345–353 (2014).

  • 22.

    Chen, F., Wu, G., Parajulee, M. N. & Ge, F. Long-term impacts of elevated carbon dioxide and transgenic Bt cotton on performance and feeding of three generations of cotton bollworm. Entomol. Exp. Appl. 124, 27–35 (2007).

    Article 

    Google Scholar
     

  • 23.

    Chen, F. J., Wu, G., Ge, F., Parajulee, M. N. & Shrestha, R. B. Effects of elevated CO2 and transgenic Bt cotton on plant chemistry, performance, and feeding of an insect herbivore, the cotton bollworm. Entomol. Exp. Appl. 115, 341–350 (2005).

    CAS 
    Article 

    Google Scholar
     

  • 24.

    Coll, M. & Hughes, L. Effects of elevated CO2 on an insect omnivore: A test for nutritional effects mediated by host plants and prey. Agric. Ecosyst. Environ. 123, 271–279 (2008).

    CAS 
    Article 

    Google Scholar
     

  • 25.

    Gang, W., Chen, F. J., Sun, Y. C. & Feng, G. Response of successive three generations of cotton bollworm, Helicoverpa armigera (Hübner), fed on cotton bolls under elevated CO2. J. Environ. Sci. 19, 1318–1325 (2007).

    Article 

    Google Scholar
     

  • 26.

    Yin, J., Sun, Y. C., Wu, G. & Ge, F. Effects of elevated CO2 associated with maize on multiple generations of the cotton bollworm, Helicoverpa armigera. Entomol. Exp. Appl. 136, 12–20 (2010).

    CAS 
    Article 

    Google Scholar
     

  • 27.

    Wu, G., Chen, F. J. & Ge, F. Response of multiple generations of cotton bollworm Helicoverpa armigera Hübner, feeding on spring wheat, to elevated CO2. J. Appl. Entomol. 130, 2–9 (2006).

    Article 

    Google Scholar
     

  • 28.

    Hall, C. R., Mikhael, M., Hartley, S. E. & Johnson, S. N. Elevated atmospheric CO2 suppresses jasmonate and silicon-based defences without affecting herbivores. Funct. Ecol. 34, 993–1002 (2020).

    Article 

    Google Scholar
     

  • 29.

    Guo, H. J. et al. Elevated CO2 reduces the resistance and tolerance of tomato plants to Helicoverpa armigera by suppressing the JA signaling pathway. PloS One 7, e41426, https://doi.org/10.1371/journal.pone.0041426 (2012).

  • 30.

    Soussana, J. F. & Hartwig, U. A. The effects of elevated CO2 on symbiotic N2 fixation: A link between the carbon and nitrogen cycles in grassland ecosystems. Plant Soil 187, 321–332 (1996).

    CAS 
    Article 

    Google Scholar
     

  • 31.

    Johnson, S. N., Gherlenda, A. N., Frew, A. & Ryalls, J. M. W. The importance of testing multiple environmental factors in legume-insect research: Replication, reviewers and rebuttal. Front. Plant Sci. 7, 489, https://doi.org/10.3389/fpls.2016.00489 (2016).

  • 32.

    Guo, H. et al. Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Global Change Biol. 19, 3210–3223 (2013).

    ADS 
    Article 

    Google Scholar
     

  • 33.

    Johnson, S. N., Ryalls, J. M. W. & Karley, A. J. Global climate change and crop resistance to aphids: contrasting responses of lucerne genotypes to elevated atmospheric carbon dioxide. Ann. Appl. Biol. 165, 62–72 (2014).

    CAS 
    Article 

    Google Scholar
     

  • 34.

    Deng, Y. & Lu, S. Biosynthesis and regulation of phenylpropanoids in plants. Crit. Rev. Plant Sci. 36, 257–290 (2017).

    Article 

    Google Scholar
     

  • 35.

    Winter, G., Todd, C. D., Trovato, M., Forlani, G. & Funck, D. Physiological implications of arginine metabolism in plants. Front. Plant Sci. 6, 534, https://doi.org/10.3389/fpls.2015.00534 (2015).

  • 36.

    Schortemeyer, M., Hartwig, U. A., Hendrey, G. R. & Sadowsky, M. J. Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to Free Air Carbon dioxide Enrichment (FACE). Soil Biol. Biochem. 28, 1717–1724 (1996).

    CAS 
    Article 

    Google Scholar
     

  • 37.

    Ryle, G. J. A. & Powell, C. E. The influence of elevated CO2 and temperature on biomass production of continuously defoliated white clover. Plant Cell Environ. 15, 593–599 (1992).

    CAS 
    Article 

    Google Scholar
     

  • 38.

    Norby, R. J. Nodulation and nitrogenase activity in nitrogen-fixing woody plants stimulated by CO2 enrichment of the atmosphere. Physiol. Plantarum 71, 77–82 (1987).

    CAS 
    Article 

    Google Scholar
     

  • 39.

    Edwards, E. J., McCaffery, S. & Evans, J. R. Phosphorus availability and elevated CO2 affect biological nitrogen fixation and nutrient fluxes in a clover-dominated sward. New Phytol. 169, 157–167 (2006).

    CAS 
    Article 

    Google Scholar
     

  • 40.

    Goodspeed, D., Chehab, E. W., Min-Venditti, A., Braam, J. & Covington, M. F. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc. Natl. Acad. Sci. U.S.A. 109, 4674–4677 (2012).

    ADS 
    CAS 
    Article 

    Google Scholar
     

  • 41.

    Thaler, J. S., Humphrey, P. T. & Whiteman, N. K. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260–270 (2012).

    CAS 
    Article 

    Google Scholar
     

  • 42.

    IPCC. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC, 2014).

  • 43.

    Teakle, R. E. & Jensen, J. M. in Handbook of Insect Rearing, Vol. 2 (eds R. Singh & R.F. Moore) 312–322 (Elsevier, London, 1985).

  • 44.

    Jones, C. G., Hare, J. D. & Compton, S. J. Measuring plant protein with the Bradford assay. 1. Evaluation and standard method. J. Chem. Ecol. 15, 979–992 (1989).

  • 45.

    Bradford, M. M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

    CAS 
    Article 

    Google Scholar
     

  • 46.

    Furota, S., Ogawa, N. O., Takano, Y., Yoshimura, T. & Ohkouchi, N. Quantitative analysis of underivatized amino acids in the sub- to several-nanomolar range by ion-pair HPLC using a corona-charged aerosol detector (HPLC-CAD). J. Chromatogr. B 1095, 191–197 (2018).

    CAS 
    Article 

    Google Scholar
     

  • 47.

    Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).

    CAS 
    Article 

    Google Scholar
     

  • 48.

    Viechtbauer, W. Conducting meta-analyses in R with the metafor Package. J. Stat. Softw. 36, 1–48 (2010).

    Article 

    Google Scholar
     

  • 49.

    Hedges, L. V. & Olkin, I. Statistical Methods for Meta-Analysis (Academic Press, New York, 1985).



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