Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Two novel methylesterases from Olea europaea contribute to the catabolism of oleoside-type secoiridoid esters

Abstract

Main conclusion

Two newly identified phytohormone cleaving esterases from Olea europaea are responsible for the glucosidase-initiated activation of the specialized metabolites ligstroside and oleuropein.

Abstract

Biosynthetic routes leading to the formation of plant natural products are tightly orchestrated enzymatic sequences usually involving numerous specialized catalysts. After their accumulation in plant cells and tissues, otherwise non-reactive compounds can be enzymatically activated, e.g., in response to environmental threats, like pathogen attack. In olive (Olea europaea), secoiridoid-derived phenolics, such as oleuropein or ligstroside, can be converted by glucosidases and as yet unidentified esterases to oleoside aldehydes. These are not only involved in pathogen defense, but also bear considerable promise as pharmaceuticals or neutraceuticals. Making use of the available olive genomic data, we have identified four novel methylesterases that showed significant homology to the polyneuridine aldehyde esterase (PNAE) from Rauvolfia serpentina, an enzyme acting on a distantly related metabolite group (monoterpenoid indole alkaloids, MIAs) also featuring a secoiridoid structural component. The four olive enzymes belong to the α/ß-hydrolase fold family and showed variable in vitro activity against methyl esters of selected plant hormones, namely jasmonic acid (MeJA), indole acetic acid (MeIAA), as well as salicylic acid (MeSA). None of the identified catalysts were directly active against the olive metabolites oleuropein, ligstroside, or oleoside 11-methyl ester. When employed in a sequential reaction with an appropriate glucosidase, however, two were capable of hydrolyzing these specialized compounds yielding reactive dialdehydes. This suggests that the esterases play a pivotal role in the activation of the olive secoiridoid polyphenols. Finally, we show that several of the investigated methylesterases exhibit a concomitant in vitro transesterification capacity—a novel feature, yielding ethyl esters of jasmonic acid (JA) or indole-3-acetic acid (IAA).

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data availability

The sequences reported herein are deposited with GenBank under accession numbers MK23485, MK160486, MK236351, and MK236352.

Change history

  • 01 November 2019

    Page 5, paragraph 3, line 14, GenBank Accession Number which should read MK234850 instead of MK23485.

Abbreviations

JA:

Jasmonic acid

MeJA:

Methyl jasmonate

MeSA:

Methyl salicylate

PNAE:

Polyneuridine aldehyde esterase

SA:

Salicylic acid

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

  2. Amiot MJ, Fleuriet A, Macheix JJ (1986) Importance and evolution of phenolic compounds in olive during growth and maturation. J Agric Food Chem 34(5):823–826. https://doi.org/10.1021/jf00071a014

  3. Beauchamp GK, Keast RS, Morel D, Lin J, Pika J, Han Q, Lee CH, Smith AB, Breslin PA (2005) Phytochemistry: ibuprofen-like activity in extra-virgin olive oil. Nature 437(7055):45–46. https://doi.org/10.1038/437045a

  4. Bendini A, Cerretani L, Carrasco-Pancorbo A, Gomez-Caravaca AM, Segura-Carretero A, Fernandez-Gutierrez A, Lercker G (2007) Phenolic molecules in virgin olive oils: a survey of their sensory properties, health effects, antioxidant activity and analytical methods. An overview of the last decade. Molecules 12(8):1679–1719

  5. Bianco A, Uccella N (2000) Biophenolic components of olives. Food Res Int 33(6):475–485. https://doi.org/10.1016/S0963-9969(00)00072-7

  6. Cruz F, Julca I, Gomez-Garrido J, Loska D, Marcet-Houben M, Cano E, Galan B, Frias L, Ribeca P, Derdak S, Gut M, Sanchez-Fernandez M, Garcia JL, Gut IG, Vargas P, Alioto TS, Gabaldon T (2016) Genome sequence of the olive tree, Olea europaea. Gigascience 5:29. https://doi.org/10.1186/s13742-016-0134-5

  7. Damtoft S, Franzyk H, Jensen SR (1993) Biosynthesis of secoiridoid glucosides in Oleaceae. Phytochemistry 34(5):1291–1299. https://doi.org/10.1016/0031-9422(91)80018-V

  8. Devamani T, Rauwerdink AM, Lunzer M, Jones BJ, Mooney JL, Tan MAO, Zhang ZJ, Xu JH, Dean AM, Kazlauskas RJ (2016) Catalytic promiscuity of ancestral esterases and hydroxynitrile lyases. J Am Chem Soc 138(3):1046–1056. https://doi.org/10.1021/jacs.5b12209

  9. Di Maio I, Esposto S, Taticchi A, Selvaggini R, Veneziani G, Urbani S, Servili M (2013) Characterization of 3,4-DHPEA–EDA oxidation products in virgin olive oil by high performance liquid chromatography coupled with mass spectrometry. Food Chem 138(2–3):1381–1391. https://doi.org/10.1016/j.foodchem.2012.10.097

  10. Dogru E, Warzecha H, Seibel F, Haebel S, Lottspeich F, Stockigt J (2000) The gene encoding polyneuridine aldehyde esterase of monoterpenoid indole alkaloid biosynthesis in plants is an ortholog of the alpha/betahydrolase super family. Eur J Biochem 267(5):1397–1406

  11. Fabiani R, De Bartolomeo A, Rosignoli P, Servili M, Selvaggini R, Montedoro GF, Di Saverio C, Morozzi G (2006) Virgin olive oil phenols inhibit proliferation of human promyelocytic leukemia cells (HL60) by inducing apoptosis and differentiation. J Nutr 136(3):614–619. https://doi.org/10.1093/jn/136.3.614

  12. Gentile L, Uccella NA (2014) Selected bioactives from callus cultures of olives (Olea europaea L. Var. Coratina) by LC-MS. Food Res Int 55:128–136. https://doi.org/10.1016/j.foodres.2013.10.046

  13. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923

  14. Green MR, Sambrook J (2012) Molecular cloning: a laboratory manual, vol 3, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

  15. Guirimand G, Courdavault V, Lanoue A, Mahroug S, Guihur A, Blanc N, Giglioli-Guivarc’h N, St-Pierre B, Burlat V (2010) Strictosidine activation in Apocynaceae: towards a “nuclear time bomb”? BMC Plant Biol 10:182. https://doi.org/10.1186/1471-2229-10-182

  16. Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89(6):2389–2393

  17. Gutierrez-Rosales F, Romero MP, Casanovas M, Motilva MJ, Minguez-Mosquera MI (2010) Metabolites involved in oleuropein accumulation and degradation in fruits of Olea europaea L.: Hojiblanca and Arbequina varieties. J Agric Food Chem 58(24):12924–12933. https://doi.org/10.1021/jf103083u

  18. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends in Plant Sci 13(6):264–272. https://doi.org/10.1016/j.tplants.2008.03.005

  19. Huang H, Liu B, Liu LY, Song SS (2017) Jasmonate action in plant growth and development. J Exp Biol 68(6):1349–1359. https://doi.org/10.1093/jxb/erw495

  20. Jackson RG, Lim EK, Li Y, Kowalczyk M, Sandberg G, Hoggett J, Ashford DA, Bowles DJ (2001) Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J Biol Chem 276(6):4350–4356. https://doi.org/10.1074/jbc.M006185200

  21. Jenik PD, Barton MK (2005) Surge and destroy: the role of auxin in plant embryogenesis. Development 132(16):3577–3585. https://doi.org/10.1242/dev.01952

  22. Jensen SR, Franzyk H, Wallander E (2002) Chemotaxonomy of the Oleaceae: iridoids as taxonomic markers. Phytochemistry 60(3):213–231

  23. Konno K, Hirayama C, Yasui H, Nakamura M (1999) Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc Natl Acad Sci USA 96(16):9159–9164

  24. Koudounas K, Banilas G, Michaelidis C, Demoliou C, Rigas S, Hatzopoulos P (2015) A defence-related Olea europaea beta-glucosidase hydrolyses and activates oleuropein into a potent protein cross-linking agent. J Exp Bot 66(7):2093–2106. https://doi.org/10.1093/jxb/erv002

  25. Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100(26):16101–16106. https://doi.org/10.1073/pnas.0307162100

  26. Lavallie ER, Diblasio EA, Kovacic S, Grant KL, Schendel PF, Mccoy JM (1993) A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Nat Biotechnol 11(2):187–193. https://doi.org/10.1038/nbt0293-187

  27. Letutour B, Guedon D (1992) Antioxidative activities of Olea europaea leaves and related phenolic compounds. Phytochemistry 31(4):1173–1178. https://doi.org/10.1016/0031-9422(92)80255-D

  28. Li W, Sperry JB, Crowe A, Trojanowski JQ, Smith AB 3rd, Lee VM (2009) Inhibition of tau fibrillization by oleocanthal via reaction with the amino groups of tau. J Neurochem 110(4):1339–1351. https://doi.org/10.1111/j.1471-4159.2009.06224.x

  29. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 50(2):309–332. https://doi.org/10.1023/A:1016024017872

  30. Martin-Pelaez S, Covas MI, Fito M, Kusar A, Pravst I (2013) Health effects of olive oil polyphenols: recent advances and possibilities for the use of health claims. Mol Nutr Food Res 57(5):760–771. https://doi.org/10.1002/mnfr.201200421

  31. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL–EBI. Nucleic Acids Res 41:W597–600. https://doi.org/10.1093/nar/gkt376(Web Server issue)

  32. Melliou E, Diamantakos P, Magiatis P (2017) New analytical trends for the measurement of phenolic substances of olive oil and olives with significant biological and functional importance related to health claims. In: Shahidi F, Kiritsakis A (eds) Olives and olive oil as functional foods. Wiley, pp 569–585. https://doi.org/10.1002/9781119135340.ch31

  33. Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, Verpoorte R, Oksman-Caldentey KM, Martinoia E, Bouwmeester H, Goossens A, Memelink J, Werck-Reichhart D (2014) The secoiridoid pathway from Catharanthus roseus. Nat Commun 5:3606. https://doi.org/10.1038/ncomms4606

  34. Morant AV, Jorgensen K, Jorgensen C, Paquette SM, Sanchez-Perez R, Moller BL, Bak S (2008) beta-Glucosidases as detonators of plant chemical defense. Phytochemistry 69(9):1795–1813. https://doi.org/10.1016/j.phytochem.2008.03.006

  35. Mueller-Roeber B, Balazadeh S (2014) Auxin and its role in plant senescence. J Plant Growth Regul 33(1):21–33. https://doi.org/10.1007/s00344-013-9398-5

  36. Nardi M, Bonacci S, De Luca G, Maiuolo J, Oliverio M, Sindona G, Procopio A (2014) Biomimetic synthesis and antioxidant evaluation of 3,4-DHPEA-EDA [2-(3,4-hydroxyphenyl) ethyl (3S,4E)-4-formyl-3-(2-oxoethyl) hex-4-enoate]. Food Chem 162:89–93. https://doi.org/10.1016/j.foodchem.2014.04.015

  37. Nardini M, Dijkstra BW (1999) Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9(6):732–737

  38. Obied HK, Bedgood DR Jr, Prenzler PD, Robards K (2007) Chemical screening of olive biophenol extracts by hyphenated liquid chromatography. Anal Chim Acta 603(2):176–189. https://doi.org/10.1016/j.aca.2007.09.044

  39. Obied HK, Prenzler PD, Ryan D, Servili M, Taticchi A, Esposto S, Robards K (2008) Biosynthesis and biotransformations of phenol-conjugated oleosidic secoiridoids from Olea europaea L. Nat Prod Rep 25(6):1167–1179. https://doi.org/10.1039/b719736e

  40. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318(5847):113–116. https://doi.org/10.1126/science.1147113

  41. Perez JA, Trujillo JM, Lopez H, Aragon Z, Boluda C (2009) Regioselective enzymatic acylation and deacetylation of secoiridoid glucosides. Chem Pharm Bull 57(8):882–884. https://doi.org/10.1248/cpb.57.882

  42. Pfitzner A, Stockigt J (1983) Characterization of polyneuridine aldehyde esterase, a key enzyme in the biosynthesis of sarpagine/ajmaline type alkaloids. Planta Med 48(8):221–227. https://doi.org/10.1055/s-2007-969924

  43. Poulton JE (1990) Cyanogenesis in plants. Plant Physiol 94(2):401–405. https://doi.org/10.1104/pp.94.2.401

  44. Romero C, Medina E, Vargas J, Brenes M, De Castro A (2007) In vitro activity of olive oil polyphenols against Helicobacter pylori. J Agric Food Chem 55(3):680–686. https://doi.org/10.1021/jf0630217

  45. Rugini E, Mencuccini M, Biasi R, Altamura MM (2005) Protocol for somatic embryogenesis in woody plants. Forestry sciences, vol 77. Springer, Dordrecht, pp 345–360

  46. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17(2):616–627. https://doi.org/10.1105/tpc.104.026690

  47. Stockigt J, Panjikar S (2007) Structural biology in plant natural product biosynthesis—architecture of enzymes from monoterpenoid indole and tropane alkaloid biosynthesis. Nat Prod Rep 24(6):1382–1400. https://doi.org/10.1039/b711935f

  48. Villeneuve P (2007) Lipases in lipophilization reactions. Biotechnol Adv 25(6):515–536. https://doi.org/10.1016/j.biotechadv.2007.06.001

  49. Vlot AC, Liu PP, Cameron RK, Park SW, Yang Y, Kumar D, Zhou FS, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56(3):445–456. https://doi.org/10.1111/j.1365-313X.2008.03618.x

  50. Vulcano I, Halabalaki M, Skaltsounis L, Ganzera M (2015) Quantitative analysis of pungent and anti-inflammatory phenolic compounds in olive oil by capillary electrophoresis. Food Chem 169:381–386. https://doi.org/10.1016/j.foodchem.2014.08.007

  51. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS–MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46(W1):W296–W303. https://doi.org/10.1093/nar/gky427

  52. Yang Y, Xu R, Ma CJ, Vlot AC, Klessig DF, Pichersky E (2008) Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol 147(3):1034–1045. https://doi.org/10.1104/pp.108.118224

  53. Zhao N, Lin H, Lan SQ, Jia QD, Chen XL, Guo H, Chen F (2016) VvMJE1 of the grapevine (Vitis vinifera) VvMES methylesterase family encodes for methyl jasmonate esterase and has a role in stress response. Plant Physiol Biochem 102:125–132. https://doi.org/10.1016/j.plaphy.2016.02.027

Download references

Acknowledgements

This work was funded through a collaborative research grant from BMBF (NeurOliv, Förderkennzeichen 031A590B). The contribution of reference substances by Christopher Fuchs and Renate Kirsch is greatly appreciated. The authors also acknowledge the support of the COST Action FA1006, PlantEngine). Further, our thanks are due to Agata Staniek, ProofEdScience, for language editing.

Author information

Correspondence to Heribert Warzecha.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2148 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Volk, J., Sarafeddinov, A., Unver, T. et al. Two novel methylesterases from Olea europaea contribute to the catabolism of oleoside-type secoiridoid esters. Planta 250, 2083–2097 (2019). https://doi.org/10.1007/s00425-019-03286-0

Download citation

Keywords

  • Secoiridoid
  • α/β-Hydrolase
  • Methylesterase
  • Ligstroside aglycone
  • Oleuropein aglycone
  • Phytohormone