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The terpene synthase gene family in maize – a clarification of existing community nomenclature

The Original Article was published on 27 January 2023

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Terpenes are important natural products functioning in both the primary and specialized metabolism of plants, bacteria, fungi, and other life forms. Core structural diversity is mainly determined by terpene synthases (TPS), enzymes that convert ubiquitous prenyl diphosphates such as geranyl diphosphate, farnesyl diphosphate, and geranylgeranyl diphosphate into the various terpene backbones.

Terpene synthases in the crop plant maize (Zea mays) have been the subject of active research since the 1990s. A majority of maize TPS enzymes have already been functionally described and characterized, many of them in the laboratories of the authors of this clarification effort (reviewed in [1, 2]; Table 1). A comprehensive analysis of the TPS genes in the maize inbred lines B73 and W22 showed that both contain about 40 TPS genes, although the number varies between the different lines (43 in B73 versus 38 in W22) [3, 4]. These numbers include apparent pseudogenes, as it has been shown that a pseudogene in one maize line can be functional in another line [3, 5, 6].

Table 1 Current existing nomenclature of the terpene synthase gene family in maize. The first column contains the names already assigned to functionally characterized maize TPS genes in the literature (for citations see last column). To fill the remaining gaps in the TPS numbering and to unify the nomenclature, we propose the names listed in the second column, mainly following the original names or the names already given in Ding et al. [4] (third column). Please note that this table also includes obvious pseudogenes, because it has been shown that a pseudogene in one maize line can be functional in another line [3, 5, 6]

The amazing quantitative and qualitative plasticity of the maize TPS gene family was confirmed in a recent paper by Sun and coworkers, who analyzed TPS genes in the genomes of 26 inbred lines [7]. However, only 31 gene loci were included in this analysis, resulting in one-third of the already characterized TPS genes being omitted by the authors. Furthermore, the authors did not address the extensive pre-existing literature on maize terpene synthases prior to proposing a new nomenclature that was both incomplete and inconsistent with previously published names. Our concern with this approach is that it could lead to massive confusion in this field as readers will be unable to compare the new names with the original names without extensive sequence comparisons.

With the goal of minimizing confusion, we provide an overview of the existing maize nomenclature(s) and cite the primary literature in which the maize TPSs were first described and enzyme products characterized (Table 1). In addition, following the previously published TPS names, we propose to designate all mono- and sesquiterpene synthase genes with the abbreviation “ZmTPS” and a sequential numbering (ZmTPS1 - ZmTPS36). Further we propose the continued designation of the class I diterpene synthase genes, namely kaurene synthase-like (KSL) genes, as ZmTPS42/KSL1 to ZmTPS47/KSL6. Similarly, the class II diterpene synthase genes, namely the five copalyl diphosphate synthase (CPS) genes, are abbreviated as ZmTPS37/CPS1 to ZmTPS41/CPS5 (Table 1). Those involved in biosynthesis of the gibberellin hormone also have been designated by the original mutant names – i.e., an1/2 and d5, with the latter further modified as KS(L3)/D5 to highlight its activity as an ent-kaurene synthase. Note that this nomenclature includes not only the 43 TPS gene loci found in the B73 reference genomes GRAMENE 4.0 and NAM 5.0 (www.maizegdb.org), but also four additional TPS genes not present in B73 but identified in other maize lines by Sun and coworkers [7]. The improvement of the already sequenced genomes and the sequencing of additional maize lines will lead to continued changes in the absolute number of known maize TPS genes in the future. Therefore, the nomenclature proposed here is itself evolving and merits periodic revision that builds upon existing knowledge.

The overview of the maize TPS gene family presented in this paper, together with the proposed nomenclature that includes all previously published names, is intended to help to minimize confusion about maize TPS names. In addition, the list of uncharacterized TPS genes presented in Table 1 can serve as a reference point to motivate future research on TPSs and their biological roles in maize.

Data Availability

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Abbreviations

TPS:

Terpene synthase

KSL:

Kaurene synthase/kaurene synthase-like

CPS:

Copalyl diphosphate synthase

References

  1. Degenhardt J, Köllner TG, Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry. 2009;70(15–16):1621–37.

    Article  CAS  PubMed  Google Scholar 

  2. Block AK, Vaughan MM, Schmelz EA, Christensen SA. Biosynthesis and function of terpenoid defense compounds in maize (Zea mays). Planta. 2019;249(1):21–30.

    Article  CAS  PubMed  Google Scholar 

  3. Springer NM, Anderson SN, Andorf CM, Ahern KR, Bai F, Barad O, Barbazuk WB, Bass HW, Baruch K, Ben-Zvi G, Buckler ES, Bukowski R, Campbell MS, Cannon EKS, Chomet P, Dawe RK, Davenport R, Dooner HK, Du LH, Du CG, Easterling KA, Gault C, Guan JC, Hunter CT, Jander G, Jiao YP, Koch KE, Kol G, Köllner TG, Kudo T, Li Q, Lu F, Mayfield-Jones D, Mei WB, McCarty DR, Noshay JM, Portwood JL, Ronen G, Settles AM, Shem-Tov D, Shi JH, Soifer I, Stein JC, Stitzer MC, Suzuki M, Vera DL, Vollbrecht E, Vrebalov JT, Ware D, Wei SR, Wimalanathan K, Woodhouse MR, Xiong WW, Brutnell TP. The maize W22 genome provides a foundation for functional genomics and transposon biology. Nat Genet. 2018;50(9):1282–.

    Article  CAS  PubMed  Google Scholar 

  4. Ding YZ, Weckwerth PR, Poretsky E, Murphy KM, Sims J, Saldivar E, Christensen SA, Char SN, Yang B, Tong AD, Shen ZX, Kremling KA, Buckler ES, Kono T, Nelson DR, Bohlmann J, Bakker MG, Vaughan MM, Khalil AS, Betsiashvili M, Dressano K, Kollner TG, Briggs SP, Zerbe P, Schmelz EA, Huffaker A. Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity. Nat Plants. 2020;6(11):1375–88.

    Article  CAS  PubMed  Google Scholar 

  5. Köllner TG, Schnee C, Gershenzon J, Degenhardt J. 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. 2004;16(5):1115–31.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J. A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell. 2008;20(2):482–94.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sun Y, Xiao WQ, Wang QN, Wang J, Kong XD, Ma WH, Liu SX, Ren P, Xu LN, Zhang YJ. Multiple variation patterns of terpene synthases in 26 maize genomes. BMC Genomics. 2023;24(1):46.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Schnee C, Köllner TG, Gershenzon J, Degenhardt J. 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. 2002;130(4):2049–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Richter A, Schaff C, Zhang ZW, Lipka AE, Tian F, Köllner TG, Schnee C, Preiss S, Irmisch S, Jander G, Boland W, Gershenzon J, Buckler ES, Degenhardt J. Characterization of Biosynthetic pathways for the production of the volatile Homoterpenes DMNT and TMTT in Zea mays. Plant Cell. 2016;28(10):2651–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J. 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. 2008;283(30):20779–88.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ren F, Mao HJ, Liang J, Liu J, Shu K, Wang Q. Functional characterization of ZmTPS7 reveals a maize tau-cadinol synthase involved in stress response. Planta. 2016;244(5):1065–74.

    Article  CAS  PubMed  Google Scholar 

  12. Saldivar EV, Ding YZ, Poretsky E, Bird S, Block AK, Huffaker A, Schmelz EA. Maize Terpene Synthase 8 (ZmTPS8) Contributes to a Complex Blend of Fungal-Elicited Antibiotics. Plants 2023, 12, (5).

  13. Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J. 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. 2006;103(4):1129–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Luck K, Chen XL, Norris AM, Chen F, Gershenzon J, Köllner TG. The reconstruction and biochemical characterization of ancestral genes furnish insights into the evolution of terpene synthase function in the Poaceae. Plant Mol Biol. 2020;104(1–2):203–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Liang J, Liu J, Brown R, Jia MR, Zhou K, Peters RJ, Wang Q. Direct production of dihydroxylated sesquiterpenoids by a maize terpene synthase. Plant J. 2018;94(5):847–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lin CF, Shen BZ, Xu ZN, Köllner TG, Degenhardt J, Dooner HK. Characterization of the monoterpene synthase gene tps26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiol. 2008;146(3):940–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ding YZ, Huffaker A, Köllner TG, Weckwerth P, Robert CAM, Spencer JL, Lipka AE, Schmelz EA. Selinene volatiles are essential precursors for Maize Defense promoting Fungal Pathogen Resistance. Plant Physiol. 2017;175(3):1455–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP. Cloning and characterization of the maize an1 gene. Plant Cell. 1995;7(1):75–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Harris LJ, Saparno A, Johnston A, Prisic S, Xu M, Allard S, Kathiresan A, Ouellet T, Peters RJ. The maize An2 gene is induced by Fusarium Attack and encodes an ent-copalyl diphosphate synthase. Plant Mol Biol. 2005;59(6):881–94.

    Article  CAS  PubMed  Google Scholar 

  20. Murphy KM, Ma LT, Ding YZ, Schmelz EA, Zerbe P. Functional characterization of two class II Diterpene synthases indicates additional Specialized Diterpenoid pathways in Maize (Zea mays). Front Plant Sci 2018, 9.

  21. Ding Y, Murphy KM, Poretsky E, Mafu S, Yang B, Char SN, Christensen SA, Saldivar E, Wu M, Wang Q, Ji L, Schmitz RJ, Kremling KA, Buckler ES, Shen Z, Briggs SP, Bohlmann J, Sher A, Castro-Falcon G, Hughes CC, Huffaker A, Zerbe P, Schmelz EA. Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Nature Plants 2019, 5, 1043–1056.

  22. Fu JY, Ren F, Lu X, Mao HJ, Xu MM, Degenhardt J, Peters RJ, Wang Q. A Tandem array of ent-kaurene synthases in Maize with roles in Gibberellin and more specialized metabolism. Plant Physiol. 2016;170(2):742–51.

    Article  CAS  PubMed  Google Scholar 

  23. Mafu S, Ding Y, Murphy KM, Yaacoobi O, Bennett Addison J, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA. Discovery, biosynthesis and stress-related Accumulation of Dolabradiene-Derived defenses in Maize. Plant Physiol. 2018;176:2677–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This research was supported by the Max Planck Society, grants from the NIH (GM131885) and USDA-NIFA (2020-67013-32557) to RJP, and grants from NSF (1758976) and the DOE-JGI (CSP2568) to PZ and EAS. The funders had no role in the experimental design, data collection and analysis or preparation of the manuscript.

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TGK, JG, RJP, PZ, and EAS analyzed data and literature. TGK wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Tobias G. Köllner.

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Köllner, T.G., Gershenzon, J., Peters, R.J. et al. The terpene synthase gene family in maize – a clarification of existing community nomenclature. BMC Genomics 24, 744 (2023). https://doi.org/10.1186/s12864-023-09856-7

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  • DOI: https://doi.org/10.1186/s12864-023-09856-7