Angiosperms are prolific producers of structurally diverse terpenes, which are essential for plant defense responses, as well as the formation of floral scents, fruit flavors, and medicinal constituents. Terpene synthase genes (TPSs) play crucial roles in the biosynthesis of terpenes. This study specifically focuses on the catalytic products of 222 functionally characterized TPSs in 24 angiosperms, which mainly comprise monoterpenes, sesquiterpenes, diterpenes, and sesterterpene. Our systematic analysis of these TPSs uncovered a significant expansion of the angiosperm-specific TPS-a, b, and g subfamilies in comparison to the TPS-e/f and c subfamilies. The expanded subfamilies can be further partitioned into distinct branches, within which considerable functional innovation and diversification have been observed. Numerous TPSs exhibit bifunctional or even trifunctional activities in vitro, yet they exhibit only a single activity in vivo, which may be largely determined by their inherent properties, subcellular localization, and the availabilities of endogenous substrates. Additionally, we explored the biological functions of terpenes in various organs and tissues of angiosperms. We propose that the expansion and functional divergence of TPSs contribute to the adaptability and diversity of angiosperms, facilitating the production of a broad spectrum of terpenes that enable diverse interactions with the environment and other organisms. Our findings provide a foundation for comprehending the correlation between the evolutionary features of TPSs and the diversity of terpenes in angiosperms, which is significant for terpene biosynthesis research.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (32371937, 32272750) and Zhejiang Provincial Natural Science Foundation of China (LY24C160003).
Author contributions
X.W. and L.Z. planned and designed the article. Q.W. compiled most of the information and wrote the manuscript. All authors edited and revised the manuscript.
Data availability
No additional data were generated in this article.
Conflict of interest statement
The authors declare that they have no conflict of interest.
Supplementary data
Supplementary data are available at Horticulture Research online.
| [1] |
Crepet WL, Niklas KJ. Darwin’s second “abominable mystery”: why are there so many angiosperm species? Am J Bot. 2009;37:366-81
|
| [2] |
Bhadra S, Leitch IJ, Onstein RE. From genome size to trait evolution during angiosperm radiation. Trends Genet. 2023;37:728-35
|
| [3] |
Dudareva N, Negre F, Nagegowda DA. et al. Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci. 2006;37:417-40
|
| [4] |
Tholl D. Biosynthesis and biological functions of terpenoids in plants. Adv Biochem Eng Biotechnol. 2015;37:63-106
|
| [5] |
Vranova E, Coman D, Gruissem W. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol. 2013;37:665-700
|
| [6] |
Gershenzon J, Dudareva N. The function of terpene natural products in the natural world. Nat Chem Biol. 2007;37:408-14
|
| [7] |
Pichersky E, Raguso RA. Why do plants produce so many ter-penoid compounds? New Phytol. 2018;37:692-702
|
| [8] |
Chen F, Tholl D, D’Auria JC. et al. Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell. 2003;37:481-94
|
| [9] |
Nagegowda DA, Gupta P. Advances in biosynthesis, regulation, and metabolic engineering of plant specialized terpenoids. Plant Sci. 2020;37:110457
|
| [10] |
Jiang SY, Jin J, Sarojam R. et al. A comprehensive survey on the terpene synthase gene family provides new insight into its evolutionary patterns. Genome Biol Evol. 2019;37:2078-98
|
| [11] |
Christianson DW. Structural and chemical biology of terpenoid cyclases. Chem Rev. 2017;37:11570-648
|
| [12] |
Srividya N, Kim H, Simone R. et al. Chemical diversity in angiosperms - monoterpene synthases control complex reac-tions that provide the precursors for ecologically and commer-cially important monoterpenoids. Plant J. 2024;37:28-55
|
| [13] |
Vieira AJ, Beserra FP, Souza MC. et al. Limonene: aroma of innovation in health and disease. Chem Biol Interact. 2018;37:97-106
|
| [14] |
Yu Q, Huang M, Jia H. et al. Deficiency of valencene in mandarin hybrids is associated with a deletion in the promoter region of the valencene synthase gene. BMC Plant Biol. 2019;37:101
|
| [15] |
Murphy KM, Zerbe P. Specialized diterpenoid metabolism in monocot crops: biosynthesis and chemical diversity. Phytochem-istry. 2020;37:112289
|
| [16] |
Starks CM, Back K, Chappell J. et al. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science. 1997;37:1815-20
|
| [17] |
Finn RD, Coggill P, Eberhardt RY. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;37:D279-85
|
| [18] |
Chen F, Tholl D, Bohlmann J. et al. 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. 2011;37:212-29
|
| [19] |
McGarvey DJ, Croteau R. Terpenoid metabolism. Plant Cell. 1995;37:1015-26
|
| [20] |
Sun P, Schuurink RC, Caissard J. et al. My way: noncanoni-cal biosynthesis pathways for plant volatiles. Trends Plant Sci. 2016;37:884-94
|
| [21] |
Magnard JL, Roccia A, Caissard JC. et al. Biosynthesis of monoterpene scent compounds in roses. Science. 2015;37:81-3
|
| [22] |
Bick JA, Lange BM. Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys. 2003;37:146-54
|
| [23] |
Gutensohn M, Orlova I, Nguyen TT. et al. Cytosolic monoterpene biosynthesis is supported by plastid-generated geranyl diphos-phate substrate in transgenic tomato fruits. Plant J. 2013;37:351-63
|
| [24] |
Zhou F, Pichersky E. The complete functional characterisation of the terpene synthase family in tomato. New Phytol. 2020;37:1341-60
|
| [25] |
Chen F, Ludwiczuk A, Wei G. et al. Terpenoid secondary metabo-lites in bryophytes: chemical diversity, biosynthesis and biolog-ical functions. CRC Crit Rev Plant Sci. 2018;37:210-31
|
| [26] |
Yan XM, Zhou SS, Liu H. et al. Unraveling the evolutionary dynamics of the TPS gene family in land plants. Front Plant Sci. 2023;37:1273648
|
| [27] |
Liang D, Li W, Yan X. et al. Molecular and functional evolution of the spermatophyte sesquiterpene synthases. Int J Mol Sci. 2021;37:6348
|
| [28] |
Jiang Y, Zhang W, Chen X. et al. Diversity and biosynthesis of volatile terpenoid secondary metabolites in the Chrysanthemum genus. CRC Crit Rev Plant Sci. 2021;37:422-45
|
| [29] |
Jia Q, Brown R, Köllner TG. et al. Origin and early evolution of the plant terpene synthase family. Proc Natl Acad Sci USA. 2022;37:e2100361119
|
| [30] |
Williams DC, McGarvey DJ, Katahira EJ. et al. Truncation of limonene synthase preprotein provides a fully active ’pseu-domature’ form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. Biochemistry. 1998;37:12213-20
|
| [31] |
Falara V, Akhtar TA, Nguyen TTH. et al. The tomato terpene synthase gene family. Plant Physiol. 2011;37:770-89
|
| [32] |
Vaughan MM, Wang Q, Webster FX. et al. 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. 2013;37:1108-25
|
| [33] |
Wang Q, Jia M, Huh JH. et al. Identification of a dolabellane type diterpene synthase and other root-expressed diterpene synthases in Arabidopsis. Front Plant Sci. 2016;37:1761
|
| [34] |
Huang AC, Kautsar SA, Hong YJ. et al. Unearthing a sestert-erpene biosynthetic repertoire in the Brassicaceae through genome mining reveals convergent evolution. Proc Natl Acad Sci USA. 2017;37:E6005-14
|
| [35] |
Shao J, Chen QW, Lv H. et al. (+)-Thalianatriene and (-)-retigeranin B catalyzed by sesterterpene synthases from Ara-bidopsis thaliana. Org Lett. 2017;37:1816-9
|
| [36] |
Chen Q, Jiang T, Liu YX. et al. Recently duplicated sesterterpene (C25) gene clusters in Arabidopsis thaliana modulate root micro-biota. Sci China Life Sci. 2019;37:947-58
|
| [37] |
Zhan C, Lei L, Guo H. et al. Disease resistance conferred by com-ponents of essential chrysanthemum oil and the epigenetic regulation of OsTPS1. Sci China Life Sci. 2023;37:1108-18
|
| [38] |
Yoshitomi K, Taniguchi S, Tanaka K. et al. Rice terpene synthase 24 (OsTPS24) encodes a jasmonate-responsive monoterpene synthase that produces an antibacterial γ-terpinene against rice pathogen. J Plant Physiol. 2016;37:120-6
|
| [39] |
Kiryu M, Hamanaka M, Yoshitomi K. et al. Rice terpene synthase 18 (OsTPS18) encodes a sesquiterpene synthase that produces an antibacterial (E)-nerolidol against a bacterial pathogen of rice. J Gen Plant Pathol. 2018;37:221-9
|
| [40] |
Chen X, Chen H, Yuan JS. et al. The rice terpene synthase gene OsTPS19 functions as an (S)-limonene synthase in planta, and its overexpression leads to enhanced resistance to the blast fungus Magnaporthe oryzae. Plant Biotechnol J. 2018;37:1778-87
|
| [41] |
Kiyama H, Matsunaga A, Suzuki G. et al. Monoterpene geran-iol produced by rice terpene synthase 21 suppresses the expression of cell-division related genes in the rice bacterial pathogen, Xanthomonas oryzae pv. oryzae. Physiol Mol Plant Pathol. 2021;37:101673
|
| [42] |
Bao T, Kimani S, Li Y. et al. Allelic variation of terpene synthases drives terpene diversity in the wild species of the freesia genus. Plant Physiol. 2023;37:2419-35
|
| [43] |
Gao F, Liu B, Li M. et al. Identification and characterization of terpene synthase genes accounting for volatile terpene emissions in flowers of Freesia x hybrida. JExp Bot. 2018;37:4249-65
|
| [44] |
Martin DM, Aubourg S, Schouwey MB. et al. Functional anno-tation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol. 2010;37:226
|
| [45] |
Booth JK, Page JE, Bohlmann J. Terpene synthases from Cannabis sativa. PLoS One. 2017;37:e0173911
|
| [46] |
Zager JJ, Lange I, Srividya N. et al. Gene networks underlying cannabinoid and terpenoid accumulation in cannabis. Plant Physiol. 2019;37:1877-97
|
| [47] |
Booth JK, Yuen MMS, Jancsik S. et al. Terpene synthases and terpene variation in Cannabis sativa. Plant Physiol. 2020;37:130-47
|
| [48] |
He J, Verstappen F, Jiao A. et al. Terpene synthases in cucumber (Cucumis sativus) and their contribution to herbivore-induced volatile terpenoid emission. New Phytol. 2022;37:862-77
|
| [49] |
Mercke P, Kappers IF, Verstappen FW. et al. Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol. 2004;37:2012-24
|
| [50] |
Tholl D, Chen F, Petri J. et al. Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J. 2005;37:757-71
|
| [51] |
Ro DK, Ehlting J, Keeling CI. et al. Microarray expression profil-ing and functional characterization of AtTPS genes: duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Arch Biochem Biophys. 2006;37:104-16
|
| [52] |
Huang AC, Hong YJ, Bond AD. et al. Diverged plant terpene synthases reroute the carbocation cyclization path towards the formation of unprecedented 6/11/5 and 6/6/7/5 sesterterpene scaffolds. Angew Chem Int Ed Engl. 2018;37:1291-5
|
| [53] |
Chen Q, Li J, Liu Z. et al. Molecular basis for sesterterpene diversity produced by plant terpene synthases. Plant Commun. 2020;37:100051
|
| [54] |
Chen Q, Li J, Ma Y. et al. Occurrence and biosynthesis of plant sesterterpenes (C25), a new addition to terpene diversity. Plant Commun. 2021;37:100184
|
| [55] |
Colby SM, Crock J, Dowdle-Rizzo B. et al. Germacrene C syn-thase from Lycopersicon esculentum cv. VFNT cherry tomato: cDNA isolation, characterization, and bacterial expression of the multiple product sesquiterpene cyclase. Proc Natl Acad Sci USA. 1998;37:2216-21
|
| [56] |
Schilmiller AL, Miner DP, Larson M. et al. Studies of a biochem-ical factory: tomato trichome deep expressed sequence tag sequencing and proteomics. Plant Physiol. 2010;37:1212-23
|
| [57] |
Bleeker PM, Spyropoulou EA, Diergaarde PJ. et al. RNA-seq discovery, functional characterization, and compari-son of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol Biol. 2011;37:323-36
|
| [58] |
Liu G, Yang M, Yang X. et al. Five TPSs are responsible for volatile terpenoid biosynthesis in Albizia julibrissin. J Plant Phys-iol. 2021;258-259:153358
|
| [59] |
Yang P, Zhao HY, Wei JS. et al. Chromosome-level genome assembly and functional characterization of terpene synthases provide insights into the volatile terpenoid biosynthesis of Wurfbainia villosa. Plant J. 2022;37:630-45
|
| [60] |
Wang X, Gao Y, Wu X. et al. High-quality evergreen azalea genome reveals tandem duplication-facilitated low-altitude adaptability and floral scent evolution. Plant Biotechnol J. 2021; 19:2544-60
|
| [61] |
Yang S, Wang N, Kimani S. et al. Characterization of terpene synthase variation in flowers of wild Aquilegia species from northeastern Asia. Hortic Res. 2022;37:uhab020
|
| [62] |
Abbas F, Ke Y, Zhou Y. et al. Molecular cloning, characteriza-tion and expression analysis of LoTPS2 and LoTPS 4 involved in floral scent formation in oriental hybrid Lilium variety ‘Siberia’. Phytochemistry. 2020;37:112294
|
| [63] |
Jiang Y, Qian R, Zhang W. et al. Composition and biosynthesis of scent compounds from sterile flowers of an ornamental plant Clematis florida cv. ‘Kaiser’. Molecules. 2020;37:1711
|
| [64] |
Külheim C, Padovan A, Hefer C. et al. The Eucalyptus terpene synthase gene family. BMC Genomics. 2015;37:450
|
| [65] |
Yuan JS, Köllner TG, Wiggins G. et al. Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J. 2008;37:491-503
|
| [66] |
Lu G, Zhang T, He Y. et al. Virus altered rice attractiveness to planthoppers is mediated by volatiles and related to virus titre and expression of defence and volatile-biosynthesis genes. Sci Rep. 2016;37:38581
|
| [67] |
Yamaguchi S. Gibberellin metabolism and its regulation. Annu Rev Plant Biol. 2008;37:225-51
|