Biosynthesis and function of terpenoid defense compounds in maize (Zea mays)
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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.
KeywordsCorn 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.
- 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. https://doi.org/10.1105/tpc.16.00003 CrossRefGoogle Scholar
- 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. https://doi.org/10.1007/s00425-017-2830-5 Google Scholar
- 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. https://doi.org/10.1073/pnas.0906365106 CrossRefGoogle Scholar
- 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. https://doi.org/10.1007/s10886-011-9967-7 CrossRefGoogle Scholar
- 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. https://doi.org/10.1105/tpc.019877 CrossRefGoogle Scholar
- 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. https://doi.org/10.1105/tpc.107.051672 CrossRefGoogle Scholar
- 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. https://doi.org/10.1074/jbc.M802682200 CrossRefGoogle Scholar
- 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. https://doi.org/10.1104/pp.17.01351 CrossRefGoogle Scholar
- 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. https://doi.org/10.1094/PHP-RS-16-0030 CrossRefGoogle Scholar
- 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. https://doi.org/10.1105/tpc.15.00919 CrossRefGoogle Scholar
- 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. https://doi.org/10.1104/pp.008326 CrossRefGoogle Scholar
- 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. https://doi.org/10.1073/pnas.0508027103 CrossRefGoogle Scholar
- 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. https://doi.org/10.1002/ece3.2893 CrossRefGoogle Scholar
- 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. https://doi.org/10.1007/BF00988004 CrossRefGoogle Scholar
- 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. https://doi.org/10.1104/pp.15.01039 Google Scholar
- 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. https://doi.org/10.1111/j.1469-8137.2010.03474.x CrossRefGoogle Scholar