, Volume 249, Issue 1, pp 21–30 | Cite as

Biosynthesis and function of terpenoid defense compounds in maize (Zea mays)

  • Anna K. BlockEmail author
  • Martha M. Vaughan
  • Eric A. Schmelz
  • Shawn A. Christensen
Part of the following topical collections:
  1. Terpenes and Isoprenoids


Main conclusion

Maize produces an array of herbivore-induced terpene volatiles that attract parasitoids to infested plants and a suite of pathogen-induced non-volatile terpenoids with antimicrobial activity to defend against pests.

Plants rely on complex blends of constitutive and dynamically produced specialized metabolites to mediate beneficial ecological interactions and protect against biotic attack. One such class of metabolites are terpenoids, a large and structurally diverse class of molecules shown to play significant defensive and developmental roles in numerous plant species. Despite this, terpenoids have only recently been recognized as significant contributors to pest resistance in maize (Zea mays), a globally important agricultural crop. The current review details recent advances in our understanding of biochemical structures, pathways and functional roles of maize terpenoids. Dependent upon the lines examined, maize can harbor more than 30 terpene synthases, underlying the inherent diversity of maize terpene defense systems. Part of this defensive arsenal is the inducible production of volatile bouquets that include monoterpenes, homoterpenes and sesquiterpenes, which often function in indirect defense by enabling the attraction of parasitoids and predators. More recently discovered are a subset of sesquiterpene and diterpene hydrocarbon olefins modified by cytochrome P450s to produce non-volatile end-products such kauralexins, zealexins, dolabralexins and β-costic acid. These non-volatile terpenoid phytoalexins often provide effective defense against both microbial and insect pests via direct antimicrobial and anti-feedant activity. The diversity and promiscuity of maize terpene synthases, coupled with a variety of secondary modifications, results in elaborate defensive layers whose identities, regulation and precise functions are continuing to be elucidated.


Corn Insect Pathogen Phytoalexins Terpenes Volatiles 



The use of trade name, commercial product or corporation in this publication is for the information and convenience of the reader and does not imply an official recommendation, endorsement or approval by the U.S. Department of Agriculture or the Agricultural Research Service for any product or service to the exclusion of others that may be suitable. USDA is an equal opportunity provide and employer. This work was funded by United States Department of Agriculture-Agricultural Research Service projects 6036-11210-001-00D and 5010-42000-048-00-D and by United States Department of Agriculture-National Institute of Food and Agriculture Grant 2018-51181-28419.


  1. Balmer D, de Papajewski DV, Planchamp C, Glauser G, Mauch-Mani B (2013) Induced resistance in maize is based on organ-specific defence responses. Plant J 74(2):213–225. CrossRefGoogle Scholar
  2. Becker EM, Herrfurth C, Irmisch S, Kollner 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. CrossRefGoogle Scholar
  3. 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. CrossRefGoogle Scholar
  4. Block A, Vaughan MM, Christensen SA, Alborn HT, Tumlinson JH (2017) Elevated carbon dioxide reduces emission of herbivore-induced volatiles in Zea mays. Plant Cell Environ 40(9):1725–1734. CrossRefGoogle Scholar
  5. Block AK, Hunter CT, Rering C, Christensen SA, Meagher RL (2018) Contrasting insect attraction and herbivore-induced plant volatile production in maize. Planta 248(1):105–116. CrossRefGoogle Scholar
  6. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95(8):4126–4133. CrossRefGoogle Scholar
  7. Casas MI, Falcone-Ferreyra ML, Jiang N, Mejia-Guerra MK, Rodriguez E, Wilson T, Engelmeier J, Casati P, Grotewold E (2016) Identification and characterization of maize salmon silks genes involved in insecticidal maysin biosynthesis. Plant Cell 28(6):1297–1309. CrossRefGoogle Scholar
  8. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66(1):212–229. CrossRefGoogle Scholar
  9. Christensen SA, Huffaker A, Sims J, Hunter CT, Block A, Vaughan MM, Willett D, Romero M, Mylroie JE, Williams WP, Schmelz EA (2017) Fungal and herbivore elicitation of the novel maize sesquiterpenoid, zealexin A4, is attenuated by elevated CO2. Planta. Google Scholar
  10. Christensen SA, Sims J, Vaughan M, Hunter C, Block A, Willett D, Alborn HT, Huffaker A, Schmelz EA (2018) Commercial hybrids and mutant genotypes reveal complex protective roles for inducible terpenoid defenses. J Exp Bot. Google Scholar
  11. Christianson DW (2006) Structural biology and chemistry of the terpenoid cyclases. Chem Rev 106(8):3412–3442. CrossRefGoogle Scholar
  12. Christianson DW (2008) Unearthing the roots of the terpenome. Curr Opin Chem Biol 12(2):141–150. CrossRefGoogle Scholar
  13. Davis EM, Croteau R (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Top Curr Chem 209:53–95CrossRefGoogle Scholar
  14. Degenhardt J (2009) Indirect defense responses to herbivory in grasses. Plant Physiol 149(1):96–102. CrossRefGoogle Scholar
  15. Degenhardt J, Hiltpold I, Kollner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (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. CrossRefGoogle Scholar
  16. Ding YZ, Huffaker A, Kollner TG, Weckwerth P, Robert CAM, Spencer JL, Lipka AE, Schmelz EA (2017) Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol 175(3):1455–1468. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. Gouinguene SP, Turlings TC (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129(3):1296–1307. CrossRefGoogle Scholar
  20. Gouinguene S, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11(1):9–16. CrossRefGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. Huffaker A, Kaplan F, Vaughan MM, Dafoe NJ, Ni XZ, Rocca JR, Alborn HT, Teal PEA, Schmelz EA (2011) Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol 156(4):2082–2097. CrossRefGoogle Scholar
  23. Kollner TG, Schnee C, Gershenzon J, Degenhardt J (2004a) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65(13):1895–1902. CrossRefGoogle Scholar
  24. Kollner TG, Schnee C, Gershenzon J, Degenhardt J (2004b) 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. CrossRefGoogle Scholar
  25. Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008a) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494. CrossRefGoogle Scholar
  26. Kollner 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. CrossRefGoogle Scholar
  27. Liang J, Liu J, Brown R, Jia M, Zhou K, Peters RJ, Wang Q (2018) Direct production of dihydroxylated sesquiterpenoids by a maize terpene synthase. Plant J. Google Scholar
  28. Lin CF, Shen BZ, Xu ZN, Koellner 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. CrossRefGoogle Scholar
  29. Mafu S, Ding Y, Murphy KM, Yaacoobi O, Addison JB, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA, Zerbe P (2018) Discovery, biosynthesis and stress-related accumulation of dolabradiene-derived defenses in maize. Plant Physiol 176(4):2677–2690. CrossRefGoogle Scholar
  30. Mao HJ, Liu J, Ren F, Peters RJ, Wang Q (2016) Characterization of CYP71Z18 indicates a role in maize zealexin biosynthesis. Phytochemistry 121:4–10. CrossRefGoogle Scholar
  31. Meihls LN, Kaur H, Jander G (2012) Natural variation in maize defense against insect herbivores. Cold Spring Harb Symp Quant Biol 77:269–283. CrossRefGoogle Scholar
  32. Mueller DS, Wise KA, Sisson AJ, Allen TW, Bergstrom GC, Bosley DB, Bradley CA, Broders KD, Byamukama E, Chilvers MI, Collins A, Faske TR, Friskop AJ, Heiniger RW, Hollier CA, Hooker DC, Isakeit T, Jackson-Ziems TA, Jardine DJ, Kinzer K, Koenning SR, Malvick DK, McMullen M, Meyer RF, Paul PA, Robertson AE, Roth GW, Smith DL, Tande CA, Tenuta AU, Vincelli P, Warner F (2016) Corn yield loss estimates due to diseases in the United States and Ontario, Canada from 2012 to 2015. Plant Health Prog 17:211–222. CrossRefGoogle Scholar
  33. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43. CrossRefGoogle Scholar
  34. Rasmann S, Kollner 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. CrossRefGoogle Scholar
  35. Ren F, Mao H, Liang J, Liu J, Shu K, Wang Q (2016) Functional characterization of ZmTPS7 reveals a maize tau-cadinol synthase involved in stress response. Planta 244(5):1065–1074. CrossRefGoogle Scholar
  36. Richter A, Schaff C, Zhang Z, Lipka AE, Tian F, Kollner TG, Schnee C, Preiss S, Irmisch S, Jander G, Boland W, Gershenzon J, Buckler ES, Degenhardt J (2016) Characterization of biosynthetic pathways for the production of the volatile homoterpenes DMNT and TMTT in Zea mays. Plant Cell 28(10):2651–2665. CrossRefGoogle Scholar
  37. Robert CA, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings TC (2012) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194(4):1061–1069. CrossRefGoogle Scholar
  38. Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni XZ, 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. CrossRefGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. Schnee C, Kollner TG, Gershenzon J, Degenhardt J (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-beta-farnesene, (E)-nerolidol, and (E, E)-farnesol after herbivore damage. Plant Physiol 130(4):2049–2060. CrossRefGoogle Scholar
  41. Schnee C, Kollner 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. CrossRefGoogle Scholar
  42. Tamiru A, Bruce TJA, Richter A, Woodcock CM, Midega CAO, Degenhardt J, Kelemu S, Pickett JA, Khan ZR (2017) A maize landrace that emits defense volatiles in response to herbivore eggs possesses a strongly inducible terpene synthase gene. Ecol Evol 7(8):2835–2845. CrossRefGoogle Scholar
  43. Tarkowska D, Strnad M (2018) Isoprenoid-derived plant signaling molecules: biosynthesis and biological importance. Planta 247(5):1051–1066. CrossRefGoogle Scholar
  44. Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. Adv Biochem Eng Biot 148:63–106. Google Scholar
  45. Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250(4985):1251–1253. CrossRefGoogle Scholar
  46. Turlings TC, Tumlinson JH, Heath RR, Proveaux AT, Doolittle RE (1991) Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J Chem Ecol 17(11):2235–2251. CrossRefGoogle Scholar
  47. Tzin V, Fernandez-Pozo N, Richter A, Schmelz EA, Schoettner M, Schafer M, Ahern KR, Meihls LN, Kaur H, Huffaker A, Mori N, Degenhardt J, Mueller LA, Jander G (2015) Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays. Plant Physiol 169(3):1727–1743. Google Scholar
  48. van der Linde K, Kastner C, Kumlehn J, Kahmann R, Doehlemann G (2011) Systemic virus-induced gene silencing allows functional characterization of maize genes during biotrophic interaction with Ustilago maydis. New Phytol 189(2):471–483. CrossRefGoogle Scholar
  49. Vaughan MM, Christensen S, Schmelz EA, Huffaker A, Mcauslane HJ, Alborn HT, Romero M, Allen LH, Teal PEA (2015) Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance. Plant Cell Environ 38(11):2195–2207. CrossRefGoogle Scholar
  50. Wouters FC, Blanchette B, Gershenzon J, Vassao DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev 15(6):1127–1151. CrossRefGoogle Scholar
  51. Yan ZG, Wang CZ (2006) Identification of Mythmna separata-induced maize volatile synomones that attract the parasitoid Campoletis chlorideae. J Appl Entomol 130(4):213–219. CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  1. 1.Center for Medical, Agricultural and Veterinary EntomologyU.S. Department of Agriculture-Agricultural Research ServiceGainesvilleUSA
  2. 2.National Center for Agricultural Utilization ResearchU.S. Department of Agriculture-Agricultural Research ServicePeoriaUSA
  3. 3.Section of Cell and Developmental BiologyUniversity of California San DiegoLa JollaUSA

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