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The reactions of plant hormones with reactive oxygen species: chemical insights at a molecular level

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Abstract

The reactions of two plant hormones, namely jasmonic acid (JA) and methyl jasmonate (MJ), with different reactive oxygen species (ROS) were investigated using the density functional theory. Different reaction sites and mechanisms were explored, as well as solvents of different polarity, and pH in aqueous solution. The thermochemical viability and kinetics of the investigated reaction pathways were found to be strongly influenced by the reacting ROS. All the investigated pathways were found to be exergonic, both in aqueous and lipid solution and for both JA and MJ, when the reactions involve •OH and •OCH3. On the contrary, for the reactions with peroxy radicals (•OOH and •OOCH2CHCH2) only a few hydrogen transfer pathways were found to be thermochemically viable. The reactions involving •OH were found to be diffusion-controlled, with both JA and MJ, regardless of the polarity of the solvent. This led to the hypothesis that the direct •OH scavenging activity of JA and MJ might play a role in the beneficial effects of the jasmonate family regarding the antioxidant defense of plants against metal-induced oxidative stress. The deprotonated fraction of JA is, to some extent, more reactive than the neutral fraction toward ROS. This, together with the acid-base equilibria inherent to some ROS, make the pH an influential environmental factor on the overall reactivity of JA toward ROS.

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References

  1. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  2. Wasternack C (2014) Action of jasmonates in plant stress responses and development - Applied aspects. Biotechnol Adv 32:31–39

    Article  CAS  PubMed  Google Scholar 

  3. Wasternack C, Hause B (2013) Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pieterse CMJ, Leon-Reyes A, Van Der Ent S et al (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  5. Sorokan AV, Burhanova GF, Maksimov IV (2018) Anionic peroxidase-mediated oxidative burst requirement for jasmonic acid-dependent Solanum tuberosum defence against Phytophthora infestans. Plant Pathol 67:349–357

    Article  CAS  Google Scholar 

  6. Dar TA, Uddin M, Khan MMA et al (2015) Jasmonates counter plant stress: A review. Environ Exp Bot 115:49–57

    Article  CAS  Google Scholar 

  7. Santino A, Taurino M, De Domenico S et al (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098

    Article  CAS  PubMed  Google Scholar 

  8. Kamal AHM, Komatsu S (2016) Jasmonic acid induced protein response to biophoton emissions and flooding stress in soybean. J Proteomics 133:33–47

    Article  CAS  PubMed  Google Scholar 

  9. Carvalhais LC, Schenk PM, Dennis PG (2017) Jasmonic acid signalling and the plant holobiont. Curr Opin Microbiol 37:42–47

    Article  CAS  PubMed  Google Scholar 

  10. Jacobo-Velázquez DA, González-Aguëro M, Cisneros-Zevallos L (2015) Cross-talk between signaling pathways: The link between plant secondary metabolite production and wounding stress response. Sci Rep 5:8608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Farooq MA, Islam F, Yang C et al (2018) Methyl jasmonate alleviates arsenic-induced oxidative damage and modulates the ascorbate–glutathione cycle in oilseed rape roots. Plant Growth Regul 84:135–148

    Article  CAS  Google Scholar 

  12. Sirhindi G, Mir MA, Abd-Allah EF et al (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in glycine max under nickel toxicity. Front Plant Sci 7:591

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yoon JY, Hamayun M, Lee S-K et al (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68

    Article  Google Scholar 

  14. Farmer EE (2007) Plant biology: Jasmonate perception machines. Nature 448:659–660

    Article  CAS  PubMed  Google Scholar 

  15. Shan C, Yang T (2017) Nitric oxide acts downstream of hydrogen peroxide in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Agropyron cristatum leaves. Biol Plantarum 61:779–784

    Article  CAS  Google Scholar 

  16. Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405

    Article  CAS  PubMed  Google Scholar 

  17. Sasaki-Sekimoto Y, Taki N, Obayashi T et al (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  CAS  PubMed  Google Scholar 

  18. Salimi F, Shekari F, Hamzei J (2016) Methyl jasmonate improves salinity resistance in German chamomile (Matricaria chamomilla L.) by increasing activity of antioxidant enzymes. Acta Physiol Plant 38:1–14

    Article  CAS  Google Scholar 

  19. Zaragoza-Martínez F, Lucho-Constantino GG, Ponce-Noyola T et al (2016) Jasmonic acid stimulates the oxidative responses and triterpene production in Jatropha curcas cell suspension cultures through mevalonate as biosynthetic precursor. Plant Cell Tissue Organ Cult 127:47–56

    Article  CAS  Google Scholar 

  20. Aftab T, Khan MMA, Idrees M et al (2011) Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma 248:601–612

    Article  CAS  PubMed  Google Scholar 

  21. Złotek U, Michalak-Majewska M, Szymanowska U (2016) Effect of jasmonic acid elicitation on the yield, chemical composition, and antioxidant and anti-inflammatory properties of essential oil of lettuce leaf basil (Ocimum basilicum L.). Food Chem 213:1–7

    Article  CAS  PubMed  Google Scholar 

  22. Złotek U, Szymanowska U, Karaś M et al (2016) Antioxidative and anti-inflammatory potential of phenolics from purple basil (Ocimum basilicum L.) leaves induced by jasmonic, arachidonic and β-aminobutyric acid elicitation. Int J Food Sci Technol 51:163–170

    Article  CAS  Google Scholar 

  23. Zhang M, Su L, Xiao Z et al (2016) Methyl jasmonate induces apoptosis and pro-apoptotic autophagy via the ROS pathway in human non-small cell lung cancer. Am J Cancer Res 6:187–199

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Raviv Z, Cohen S, Reischer-Pelech D (2013) The anti-cancer activities of jasmonates. Cancer Chemother Pharmacol 71:275–285

    Article  CAS  PubMed  Google Scholar 

  25. Cohen S, Flescher E (2009) Methyl jasmonate: A plant stress hormone as an anti-cancer drug. Phytochemistry 70:1600–1609

    Article  CAS  PubMed  Google Scholar 

  26. Tong Q-s, Jiang G, Zheng L-d et al (2008) Natural jasmonates of different structures suppress the growth of human neuroblastoma cell line SH-SY5Y and its mechanisms. Acta Pharmacol Sin 29:861

    Article  CAS  PubMed  Google Scholar 

  27. Flescher E (2005) Jasmonates - A new family of anti-cancer agents. Anti-Cancer Drugs 16:911–916

    Article  CAS  PubMed  Google Scholar 

  28. Gunjegaonkar Shivshankar M, Shanmugarajan TS (2015) In vitro potential of plant stress hormone Methyl Jasmonate for anti arthritis, anti-inflammatory and free radical scavenging activity. Int J Pharmtech Res 8:161–165

    Google Scholar 

  29. Frisch MJ, Trucks GW, Schlegel HB et al (2009) Gaussian. Gaussian, Inc., Wallingford, CT, USA, p 09

    Google Scholar 

  30. Zhao Y, Schultz NE, Truhlar DG (2006) Design of density functionals by combining the method of constraint satisfaction with parametrization for thermochemistry, thermochemical kinetics. and noncovalent interactions. J Chem Theory Comput 2:364–382

    Article  CAS  PubMed  Google Scholar 

  31. Marenich AV, Cramer CJ, Truhlar DG (2009) Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J Phys Chem B 113:6378–6396

    Article  CAS  PubMed  Google Scholar 

  32. Altarawneh M, Dlugogorski BZ (2013) A mechanistic and kinetic study on the formation of PBDD/Fs from PBDEs. Environ Sci Technol 47:5118–5127

    Article  CAS  PubMed  Google Scholar 

  33. Dargiewicz M, Biczysko M, Improta R et al (2012) Solvent effects on electron-driven proton-transfer processes: Adenine-thymine base pairs. Phys Chem Chem Phys 14:8981–8989

    Article  CAS  PubMed  Google Scholar 

  34. Murillo J, Henao D, Vélez E et al (2012) Thermal decomposition of 4-hydroxy-2-butanone in m-xylene solution: Experimental and computational study. Int J Chem Kinet 44:407–413

    Article  CAS  Google Scholar 

  35. Prasanthkumar KP, Alvarez-Idaboy JR (2014) An experimental and theoretical study of the kinetics and mechanism of hydroxyl radical reaction with 2-aminopyrimidine. RSC Adv 4:14157–14164

    Article  CAS  Google Scholar 

  36. Zhao Y, Truhlar DG (2008) How well can new-generation density functionals describe the energetics of bond-dissociation reactions producing radicals? J Phys Chem A 112:1095–1099

    Article  CAS  PubMed  Google Scholar 

  37. Galano A, Alvarez-Idaboy JR (2014) Kinetics of radical-molecule reactions in aqueous solution: A benchmark study of the performance of density functional methods. J Comput Chem 35:2019–2026

    Article  CAS  PubMed  Google Scholar 

  38. Galano A, Alvarez-Idaboy JR (2013) A computational methodology for accurate predictions of rate constants in solution: Application to the assessment of primary antioxidant activity. J Comput Chem 34:2430–2445

    Article  CAS  PubMed  Google Scholar 

  39. Eyring H (1935) The activated complex in chemical reactions. J Chem Phys 3:63–71

    Article  Google Scholar 

  40. Evans MG, Polanyi M (1935) Some applications of the transition state method to the calculation of reaction velocities. especially in solution. Trans Faraday Soc 31:875–894

    Article  CAS  Google Scholar 

  41. Truhlar DG, Garrett BC, Klippenstein SJ (1996) Current status of transition-state theory. J Phys Chem 100:12771–12800

    Article  CAS  Google Scholar 

  42. Kuppermann A, Truhlar DG (1971) Exact tunneling calculations. J Am Chem Soc 93:1840–1851

    Article  CAS  Google Scholar 

  43. Marcus RA (1997) Electron transfer reactions in chemistry. Theory and experiment. Pure Appl Chem 69:13–29

    Article  CAS  Google Scholar 

  44. Collins FC, Kimball GE (1949) Diffusion-controlled reaction rates. J Colloid Sci 4:425–437

    Article  CAS  Google Scholar 

  45. Smoluchowski M (1917) Mathematical theory of the kinetics of the coagulation of colloidal solutions. Z Phys Chem 92:129–168

    Google Scholar 

  46. Einstein A (1905) Über einen die Erzeugung und Verwandlung des Lichtes betreffenden heuristischen Gesichtspunkt. Ann Phys 17:549–560

    Article  CAS  Google Scholar 

  47. Stokes GG (1903) Mathematical and Physical Papers, vol 3. Cambridge University Press, Cambridge

    Google Scholar 

  48. Dathe W, Kramell HM, Daeter W et al (1993) Uptake of jasmonic acid and related compounds by mesophyll protoplasts of the barley leaf. J Plant Growth Regul 12:133–140

    Article  CAS  Google Scholar 

  49. De Grey ADNJ (2002) HO2·: The forgotten radical. DNA Cell Biol 21:251–257

    Article  PubMed  Google Scholar 

  50. Pryor WA (1988) Why is the hydroxyl radical the only radical that commonly adds to DNA? Hypothesis: It has a rare combination of high electrophilicity, high thermochemical reactivity, and a mode of production that can occur near DNA. Free Radical Bio Med 4:219–223

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the Laboratorio de Visualización y Cómputo Paralelo at Universidad Autónoma Metropolitana-Iztapalapa.

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Authors and Affiliations

  1. Instituto Politécnico Nacional- UPIICSA, Té 950, Col. Granjas México, C.P. 08400, México, D. F, Mexico

    Misaela Francisco-Marquez

  2. Departamento de Química, Universidad Autónoma Metropolitana-Iztapalapa, San Rafael Atlixco 186, Col. Vicentina. Iztapalapa, C. P. 09340, México, D. F, Mexico

    Annia Galano

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  1. Misaela Francisco-Marquez
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Correspondence to Annia Galano.

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Francisco-Marquez, M., Galano, A. The reactions of plant hormones with reactive oxygen species: chemical insights at a molecular level. J Mol Model 24, 255 (2018). https://doi.org/10.1007/s00894-018-3781-x

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