Journal of Chemical Ecology

, Volume 45, Issue 1, pp 61–73 | Cite as

Mediation of Impacts of Elevated CO2 and Light Environment on Arabidopsis thaliana (L.) Chemical Defense against Insect Herbivory Via Photosynthesis

  • Linus Gog
  • May R. Berenbaum
  • Evan H. DeLuciaEmail author


Elevated CO2 alters C3 plant tolerance to insect herbivory, as well as the induction kinetics of defense hormones salicylic acid (SA) and jasmonic acid (JA), but the underlying physiological mechanism causing this response is not well understood. In principle, SA could be induced under elevated CO2 by reactive oxygen signals generated in photosynthesis, ultimately influencing chemical defense. To test whether the effects of elevated CO2 on C3 plant chemical defense against herbivorous insects are modulated by photosynthesis, Arabidopsis thaliana var. Col-0 plants were grown in two 2 × 2 × 2 nested factorial combinations of ambient (400 ppm) and elevated (800 ppm) CO2, and two dimensions of light regimes comprising intensity (‘mild’ 150 μmol E m−2 s−1 vs. ‘low’ light, 75 μmol E m−2 s−1) and periodicity (‘continuous’, 150 μmol E m−2 s−1 vs. ‘dynamic’, in which lights were turned off, then on, for 15 min every 2 h). Plants were challenged with herbivore damage from third instar Trichoplusia ni (cabbage looper). Consistent with experimental predictions, elevated CO2 interacted with light as well as herbivory to induce foliar concentration of SA, while JA was suppressed. Under dynamic light, foliar content of total glucosinolates was reduced. Under combination of elevated CO2 and dynamic light, T. ni removed significantly more leaf tissue relative to control plants. The observations that CO2 and light interactively modulate defense against T. ni in A. thaliana provide an empirical argument for a role of photosynthesis in C3 plant chemical defense.


Global change Photosynthesis Plant-insect interactions Chemical defense Salicylic acid Jasmonic acid 

Supplementary material

10886_2018_1035_MOESM1_ESM.pdf (75 kb)
ESM 1 (PDF 75 kb)


  1. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Bio 50(1):601–639CrossRefGoogle Scholar
  2. Ballaré CL (2014) Light regulation of plant defense. Ann Rev Plant Bio 65Google Scholar
  3. Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21(10):1511–1530CrossRefGoogle Scholar
  4. Bidart-Bouzat MG, Mithen R, Berenbaum MR (2005) Elevated CO2 influences herbivory-induced defense responses of Arabidopsis thaliana. Oecologia145(3), 415–424Google Scholar
  5. Bilgin DD, Zavala JA, Zhu JIN, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33(10):1597–1613CrossRefGoogle Scholar
  6. Casteel CL (2010) Impacts of climate change on herbivore induced plant signaling and defenses. Dissertation. In: University of Illinois at Urbana-ChampaignGoogle Scholar
  7. Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A 96(7):4198–4203CrossRefGoogle Scholar
  8. DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160(4):1677–1685CrossRefGoogle Scholar
  9. Demmig-Adams B, Stewart JJ, Adams III WW (2014) Chloroplast photoprotection and the trade-off between abiotic and biotic defense. In: Demmig-Adams B, Garab G, Adams III WW (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria Springer Netherlands, The Netherlands, pp 631–643Google Scholar
  10. Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM (2017) Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat Commun 8:49CrossRefGoogle Scholar
  11. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18CrossRefGoogle Scholar
  12. Frenkel M, Külheim C, Jänkänpää HJ, Skogström O, Dall'Osto L, Ågren J, Bassi R, Moritz T, Moen J, Jansson S (2009) Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming. BMC Plant Biol 9(1):12CrossRefGoogle Scholar
  13. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. The Plant J 33(4):691–705CrossRefGoogle Scholar
  14. Gog L (2018) Reactive oxygen from photosynthesis: theory and experiments linking elevated atmospheric CO2 with C3 plant chemical defense. Dissertation. In: University of Illinois at Urbana-ChampaignGoogle Scholar
  15. Gog L, Zavala JA, DeLucia EH (2018) Linking primary and secondary metabolism; a mechanistic hypothesis for how elevated CO2 modulates defenses. In: Emani C (ed) The Biology of Plant-Insect Interactions: A Compendium for the Plant Biotechnologist.. CRC press. USA, Boca Raton, pp 93–112CrossRefGoogle Scholar
  16. Kaiser E, Zhou D, Heuvelink E, Harbinson J, Morales A, Marcelis LF (2017) Elevated CO2 increases photosynthesis in fluctuating irradiance regardless of photosynthetic induction state. J Exp Bot 68(20):5629–5640CrossRefGoogle Scholar
  17. Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci U S A 99(20):12789–12794Google Scholar
  18. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284(5414):654–657CrossRefGoogle Scholar
  19. Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6(4):390–396CrossRefGoogle Scholar
  20. Kliebenstein D, Kroymann J, Mitchell-Olds T (2005) The glucosinolate–myrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol 8(3):264–271CrossRefGoogle Scholar
  21. Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297(5578):91–93CrossRefGoogle Scholar
  22. Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein D, Gershenzon J (2001) The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13(12):2793–2807CrossRefGoogle Scholar
  23. Leakey ADB, Press MC, Scholes JD, Watling JR (2002) Relative enhancement of photosynthesis and growth at elevated CO2 is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling. Plant Cell Environ 25(12):1701–1714CrossRefGoogle Scholar
  24. Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108(4):1673–1678CrossRefGoogle Scholar
  25. Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57(8):1795–1807CrossRefGoogle Scholar
  26. Mawlong I, Sujith Kumar MS, Gurung B, Singh KH, Singh D (2017) A simple spectrophotometric method for estimating total glucosinolates in mustard de-oiled cake. Int J F Prop 20(12):3274–3281CrossRefGoogle Scholar
  27. Mewis I, Tokuhisa J, Schultz J, Appel H, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67(22):2450–2462CrossRefGoogle Scholar
  28. Mhamdi A, Noctor G (2016) High CO2 primes plant biotic stress defences through redox-linked pathways. Plant Physiol DOI:, pp.01129.2016
  29. Mockler M, Yang T, Yu HX, Parikh D, Cheng YC, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci U S A 100(4):2140–2145CrossRefGoogle Scholar
  30. Moreno JE, Ballaré CL (2014) Phytochrome regulation of plant immunity in vegetation canopies. J Chem Ecol 40(7):848–857CrossRefGoogle Scholar
  31. Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 gene. Mol Plant Microbe In 23(3):340–351CrossRefGoogle Scholar
  32. Müller R, De Vos M, Sun J, Sønderby I, Halkier B, Wittstock U, Jander G (2010) Differential effects of indole and aliphatic glucosinolates on lepidopteran herbivores. J Chem Ecol 36(8):905–913CrossRefGoogle Scholar
  33. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64(13):3983–3998CrossRefGoogle Scholar
  34. Noctor G, Mhamdi A (2017) Climate change, CO2, and defense: the metabolic, redox, and signaling perspectives. Trends Plant Sci 22(10):857–870CrossRefGoogle Scholar
  35. Ort DR, Baker NR (2002) A photoprotective role for O 2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5(3):193–198CrossRefGoogle Scholar
  36. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat Protoc 5(6):986–992Google Scholar
  37. Pohlert T (2016) Calculate pairwise multiple comparisons of mean rank sums. R statistical packageGoogle Scholar
  38. Rasband WS, ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA,, 1997-2016
  39. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296(5566):285–289CrossRefGoogle Scholar
  40. Szechyńska-Hebda M, Karpiński S (2013) Light intensity-dependent retrograde signalling in higher plants. J Plant Physiol 170(17):1501–1516CrossRefGoogle Scholar
  41. Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172(1):92–103CrossRefGoogle Scholar
  42. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17(5):260–270CrossRefGoogle Scholar
  43. de Torres-Zabala M, Littlejohn G, Jayaraman S, Studholme D, Bailey T, Lawson T, Tillich M, Licht D, Bölter B, Delfino L, Truman W, Mansfield J, Smirnoff N, Grant M (2015) Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat Plant 1(6):15074CrossRefGoogle Scholar
  44. Trębicki P, Dáder B, Vassiliadis S, Fereres A (2017) Insect–plant–pathogen interactions as shaped by future climate: effects on biology, distribution and implications for agriculture. Ins Sci 00:1–15Google Scholar
  45. Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127(2):426–435CrossRefGoogle Scholar
  46. Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz KJ (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26(3):1151–1165CrossRefGoogle Scholar
  47. Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant Cell Environ 20(2):254–260CrossRefGoogle Scholar
  48. Wit M, Spoel SH, Sanchez-Perez GF, Gommers CM, Pieterse CM, Voesenek LA, Pierik R (2013) Perception of low red: far-red ratio compromises both salicylic acid-and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75(1):90–103CrossRefGoogle Scholar
  49. Wittstock U, Halkier B (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7(6):263–270CrossRefGoogle Scholar
  50. Zavala JA, Casteel CL, DeLucia EH, Berenbaum MR (2008) Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects. Proc Natl Acad Sci U S A 105(13):5129–5133CrossRefGoogle Scholar
  51. Zavala JA, Nabity PD, DeLucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97CrossRefGoogle Scholar
  52. Zavala JA, Gog L, Giacometti R (2016) Anthropogenic increase in carbon dioxide modifies plant–insect interactions. Ann Appl Bot 170(1):68–77CrossRefGoogle Scholar
  53. Zhang S, Li X, Sun Z, Shao S, Hu L, Ye M, Zhou Y, Xia X, Yu J, Shi K (2015) Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J Exp Bot 66(7):1951–1963CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Plant BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Department of EntomologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  3. 3.Carl R. Woese Institute for Genomic BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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