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Functional characterization of ZmTPS7 reveals a maize τ-cadinol synthase involved in stress response

Abstract

Main conclusion

Maize ( Zea mays ) terpene synthase 7 (ZmTPS7) was characterized as a τ-cadinol synthase, which exhibited constitutive and inducible gene expression patterns, suggesting involvement in stress response.

Maize produces a variety of terpenoids involved in defense response. Despite some terpene synthases (TPSs) responsible for these terpenoids have been characterized, biosynthesis of many terpenes, particularly sesquiterpenes, which were produced in response to biotic or abiotic stress, remains largely unknown. Here, we characterized ZmTPS7 biochemically through recombinant expression in Escherichia coli and detected that it catalyzed formation of a blend of sesquiterpenes and sesquiterpenoid alcohols as the sesquiterpene synthase through GC–MS analysis. Subsequently, the major product was purified and identified as τ-cadinol through nuclear magnetic resonance spectroscopy (NMR) analysis, which was also detected in maize tissues infected by pathogen fungus for the first time. ZmTPS7 constitutively expressed in aerial tissues while with trace amount of transcript in roots. Fungus spore inoculation and methyl jasmonate (MeJA) treatment induced gene expression of ZmTPS7 in leaves, while exogenous ABA induced ZmTPS7 dramatically in roots, suggesting that ZmTPS7 might be involved in stress response. τ-cadinol was quantified in infected maize tissues with the concentration of ~200 ng/g fresh weight, however, which was much lower than the inhibitory one on two tested necrotrophic fungi. Such evidences indicate that anti-fungal activity of τ-cadinol is not physiologically relevant, and further investigation is needed to clarify its biological functions in maize. Taken together, ZmTPS7 was characterized as the τ-cadinol synthase and suggested to be involved in stress response, which also increased the diversity of maize terpenoid profile.

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Abbreviations

FPP:

Farnesyl pyrophosphate

GGPP:

Geranylgeranyl pyrophosphate

MeJA:

Methyl jasmonate

NMR:

Nuclear magnetic resonance spectroscopy

TPS:

Terpene synthases

ZmTPS7:

Maize terpene synthase 7

References

  1. Becker EM, Herrfurth C, Irmisch S, Köllner TG, Feussner I, Karlovsky P, Splivallo R (2014) Infection of corn ears by Fusarium spp. induces the emission of volatile sesquiterpenes. J Agric Food Chem 62(22):5226–5236

  2. Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7(1):75–84

  3. Bordoloi M, Shukla VS, Nath SC, Sharma RP (1989) Naturally occuring cadinenes. Phytochemistry 28:2007–2037

  4. Chen X, Chen Y, Heinstein P, Davisson V (1995) Cloning, expression, and characterization of (+)-delta-cadinene synthase a catalyst for cotton phytoalexin biosynthesis. Arch Biochem Biophys 324(2):255–266

  5. Cheng SS, Wu CL, Chang HT, Kao YT, Chang ST (2004) Antitermitic and antifungal activities of essential oil of Calocedrus formosana leaf and its composition. J Chem Ecol 30(10):1957–1967

  6. Cyr A, Wilderman PR, Determan M, Peters RJ (2007) A modular approach for facile biosynthesis of labdane-related diterpenes. J Am Chem Soc 129(21):6684–6685

  7. Degen T (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135(4):1928–1938

  8. Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TC (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106(32):13213–13218

  9. Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150(4):1750–1761

  10. Fontana A, Held M, Fantaye CA, Turlings TC, Degenhardt J, Gershenzon J (2011) Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). J Chem Ecol 37(6):582–591

  11. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10(6):490–498

  12. Fu J, Ren F, Lu X, Mao H, Xu M, Degenhardt J, Peters RJ, Wang Q (2016) A tandem array of ent-kaurene synthases in maize with roles in gibberellin and more specialized metabolism. Plant Physiol 170(2):742–751

  13. Gennadios HA, Gonzalez V, Di Costanzo L, Li A, Yu F, Miller DJ, Allemann RK, Christianson DW (2009) Crystal structure of (+)-δ-cadinene synthase from Gossypium arboreum and evolutionary divergence of metal binding motifs for catalysis. Biochemistry 48(26):6175–6183

  14. Harris LJ, Saparno A, Johnston A, Prisic S, Xu M, Allard S, Kathiresan A, Ouellet T, Peters RJ (2005) The maize An2 gene is induced by Fusarium attack and encodes an ent-copalyl diphosphate synthase. Plant Mol Biol 59(6):881–894

  15. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104(13):5467–5472

  16. Huffaker A, Kaplan F, Vaughan MM, Dafoe NJ, Ni X, Rocca JR, Alborn HT, Teal PE, Schmelz EA (2011) Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol 156(4):2082–2097

  17. Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E (2004) The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol 136(3):3724–3736

  18. Jullien F, Moja S, Bony A, Legrand S, Petit C, Benabdelkader T, Poirot K, Fiorucci S, Guitton Y, Nicole F, Baudino S, Magnard JL (2014) Isolation and functional characterization of a τ-cadinol synthase, a new sesquiterpene synthase from Lavandula angustifolia. Plant Mol Biol 84(1–2):227–241

  19. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004a) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16(5):1115–1131

  20. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004b) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry 65(13):1895–1902

  21. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008a) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494

  22. Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J (2008b) Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)-beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283(30):20779–20788

  23. Köllner TG, Gershenzon J, Degenhardt J (2009) Molecular and biochemical evolution of maize terpene synthase 10, an enzyme of indirect defense. Phytochemistry 70(9):1139–1145

  24. Köllner TG, Lenk C, Schnee C, Kopke S, Lindemann P, Gershenzon J, Degenhardt J (2013) Localization of sesquiterpene formation and emission in maize leaves after herbivore damage. BMC Plant Biol 13:15

  25. Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell Environ 35(1):53–60

  26. Lin C, Shen B, Xu Z, Köllner TG, Degenhardt J, Dooner HK (2008) Characterization of the monoterpene synthase gene tps26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiol 146(3):940–951

  27. Maag D, Erb M, Köllner TG, Gershenzon J (2015) Defensive weapons and defense signals in plants: some metabolites serve both roles. BioEssays 37(2):167–174

  28. Mao H, Liu J, Ren F, Peters RJ, Wang Q (2016) Characterization of CYP71Z18 indicates a role in maize zealexin biosynthesis. Phytochemistry 121:4–10

  29. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TC (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434(7034):732–737

  30. Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni X, Rocca JR, Alborn HT, Teal PE (2011) Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc Natl Acad Sci USA 108(13):5455–5460

  31. Schmelz EA, Huffaker A, Sims JW, Christensen SA, Lu X, Okada K, Peters RJ (2014) Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins. Plant J 79(4):659–678

  32. Schnee C, Köllner TG, Held M, Turlings TC, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103(4):1129–1134

  33. Sun S, Du GJ, Qi LW, Williams S, Wang CZ, Yuan CS (2010) Hydrophobic constituents and their potential anticancer activities from Devil’s Club Oplopanax horridus. J Ethnopharmacol 132(1):280–285

  34. Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. Adv Biochem Eng Biotechnol 148:63–106

  35. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42(5):757–771

  36. Vaughan M, Wang Q, Webster FX et al (2013) Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell 25(3):1108–1125

  37. Vaughan MM, Christensen S, Schmelz EA, Huffaker A, McAuslane HJ, Alborn HT, Romero M, Allen LH, Teal PE (2015) Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance. Plant, Cell Environ 38(11):2195–2207

  38. Wang Q, Hillwig ML, Peters RJ (2011) CYP99A3: functional identification of a diterpene oxidase from the momilactone biosynthetic gene cluster in rice. Plant J 65(1):87–95

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Acknowledgments

This work was supported by the fund for distinguished young scientists of Sichuan Province (2014JQ0038) and start-up fund from Sichuan Agricultural University to Q.W. We appreciate the help of Dr. Reuben Peters at Iowa State University for providing the plasmid pGG.

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Correspondence to Qiang Wang.

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Ren, F., Mao, H., Liang, J. et al. Functional characterization of ZmTPS7 reveals a maize τ-cadinol synthase involved in stress response. Planta 244, 1065–1074 (2016). https://doi.org/10.1007/s00425-016-2570-y

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Keywords

  • ABA
  • Sesquiterpene
  • Terpene synthase
  • Terpenoid
  • Zea mays