Classification, biosynthesis, and biological functions of triterpene esters in plants

Abstract

Triterpene esters comprise a class of secondary metabolites that are synthesized by decorating triterpene skeletons with a series of oxidation, glycosylation, and acylation modifications. Many triterpene esters with important bioactivities have been isolated and identified, including those with applications in the pesticide, pharmaceutical, and cosmetic industries. They also play essential roles in plant defense against pests, diseases, physical damage (as part of the cuticle), and regulation of root microorganisms. However, there has been no recent summary of the biosynthetic pathways and biological functions of plant triterpene esters. Here, we classify triterpene esters into five categories based on their skeletons and find that C-3 oxidation may have a significant effect on triterpenoid acylation. Fatty acid and aromatic moieties are common ligands present in triterpene esters. We further analyze triterpene ester synthesis-related acyltransferases (TEsACTs) in the triterpene biosynthetic pathway. Using an evolutionary classification of BAHD acyltransferases (BAHD-ATs) and serine carboxypeptidase-like acyltransferases (SCPL-ATs) in Arabidopsis thaliana and Oryza sativa, we classify 18 TEsACTs with identified functions from 11 species. All the triterpene-skeleton-related TEsACTs belong to BAHD-AT clades IIIa and I, and the only identified TEsACT from the SCPL-AT family belongs to the CP-I subfamily. This comprehensive review of the biosynthetic pathways and bioactivities of triterpene esters provides a foundation for further study of their bioactivities and applications in industry, agricultural production, and human health.

Keywords: acyltransferases; biological functions; biosynthesis; classification; triterpene esters.

Figure 1

The diverse structures of triterpene esters. Different triterpene skeletons form triterpene esters with different types of acyl donors. Triterpene skeletons in plants can be divided into monocyclic, bicyclic, tricyclic, tetracyclic, and pentacyclic triterpenes according to the number of rings. The tetracylic and pentacyclic triterpenes have various characteristic types of triterpene skeletons (top). Acyl donors can also be divided into aromatic compounds (blue), sugars (pink), and aliphatic compounds (green) (middle). Triterpenes of different skeleton types form triterpenes with different acyl donors that have different characteristics (bottom).

Figure 2

Different acyl donors and acylation sites of triterpene esters. (A) Numbers of different types of acyl donors. (B) Fatty acid acyl donors. (C) Different acylation positions of triterpene esters. (D) Acyl donors at the C-3 position.

Figure 3

Acylation mechanisms and the structure of BAHD and SCPL acyltransferases. (A) In the cytoplasm, 2,3-oxidosqualene is catalyzed by OSCs and CYPs to synthesize triterpenoid skeletons, which are then modified by different enzymes. BAHD-ATs are located in the cytoplasm. SCPL-ATs are located in the vacuole, to which both the acyl donor and receptor are transported by tonoplastic transporters. (B) Acylation mechanisms of BAHD-ATs and SCPL-ATs. The structure of a BAHD-AT (THAA1, C) and an SCPL-AT (AsSCPL1, D) were predicted using AlphaFold2.

Figure 4

Biosynthetic pathways of triterpene esters involving BAHD acyltransferases. (A) Full-length amino acid sequences were aligned using ClustalX and used to build a neighbor-joining phylogenetic tree with MEGA 7.0. (B) Acyltransferases in clade I and the reactions they catalyze. (C) Acyltransferases in clade IIIa and the reactions they catalyze. βC, 3-O-3′,4′-diacetyl-β-D-xylopyranosyl-6-O-β-D-glucopyranosyl-cycloastragenol; CuC, Cucurbitacin C; CuB, Cucurbitacin B; T7,3β,7β-dihydroxy-16-keto-thalian-15-yl acetate; T17, 7β-hydroxy-16-keto-thalian-3β-15-yl diacetate.

Figure 5

Biosynthetic pathways of triterpene esters involving SCPL acyltransferases. (A) Full-length amino acid sequences were aligned using ClustalX and used to build a neighbor-joining phylogenetic tree with MEGA 7.0. (B) Acyltransferases in clade I and the reactions they catalyze. DAA, Des-acyl avenacin A; DMA, Des-methyl avenacin A; Anth-Glc, anthraniloyl-O-glucose; NMA-Glc, N-methyl anthraniloyl-O-glucose; DAB, Des-acyl avenacin B; Benz-Glc, benzoyl-O-glucose.

Figure 6

Potential functions of triterpene esters in plant growth, development, and environmental interactions. Triterpene esters in Bowellia bark, oat roots, and Cucurbitaceae plants have roles in defense against pests and diseases. Triterpene esters in pollen coats, leaves, and apple peels prevent water loss. Triterpene esters in roots can be secreted and regulate rhizosphere microorganisms, thus affecting plant growth and development. Triterpene esters in roots of Codonopsis pilosula exhibit autotoxicity. CuC, Cucurbitacin C; CuB, Cucurbitacin B; T7, 3β,7β-dihydroxy-16-keto-thalian-15-yl acetate; T17, 7β-hydroxy-16-keto-thalian-3β-15-yl diacetate.