The reconstruction and biochemical characterization of ancestral genes furnish insights into the evolution of terpene synthase function in the Poaceae

Abstract

Key Message Distinct catalytic features of the Poaceae TPS-a subfamily arose early in grass evolution and the reactions catalyzed have become more complex with time. Abstract The structural diversity of terpenes found in nature is mainly determined by terpene synthases (TPS). TPS enzymes accept ubiquitous prenyl diphosphates as substrates and convert them into the various terpene skeletons by catalyzing a carbocation-driven reaction. Based on their sequence similarity, terpene synthases from land plants can be divided into different subfamilies, TPS-a to TPS-h. In this study, we aimed to understand the evolution and functional diversification of the TPS-a subfamily in the Poaceae (the grass family), a plant family that contains important crops such as maize, wheat, rice, and sorghum. Sequence comparisons showed that aside from one clade shared with other monocot plants, the Poaceae TPS-a subfamily consists of five well-defined clades I-V, the common ancestor of which probably originated very early in the evolution of the grasses. A survey of the TPS literature and the characterization of representative TPS enzymes from clades I-III revealed clade-specific substrate and product specificities. The enzymes in both clade I and II function as sesquiterpene synthases with clade I enzymes catalyzing initial C10-C1 or C11-C1 ring closures and clade II enzymes catalyzing C6-C1 closures. The enzymes of clade III mainly act as monoterpene synthases, forming cyclic and acyclic monoterpenes. The reconstruction and characterization of clade ancestors demonstrated that the differences among clades I-III were already present in their ancestors. However, the ancestors generally catalyzed simpler reactions with less double-bond isomerization and fewer cyclization steps. Overall, our data indicate an early origin of key enzymatic features of TPS-a enzymes in the Poaceae, and the development of more complex reactions over the course of evolution.

Overexpression of Terpenoid Biosynthesis Genes From Garden Sage (Salvia officinalis) Modulates Rhizobia Interaction and Nodulation in Soybean

“…Researchers recently identified a terpene synthase (TPS) that can convert one carbocation to a mixture of others through various cyclizations, rearrangements, or hydride shifts ( Luck et al, 2020 ). Thus, TPS enzymes have the unique catalysis ability to convert intermediate substrates into a single or several products during different reaction cycles ( Zhou and Pichersky, 2020 ).…”

Molecular and Functional Evolution of the Spermatophyte Sesquiterpene Synthases

“…Successive gene duplications and the subsequent accumulation of mutations led to the multitude of STSs, many of which catalyze more complex reactions than the ancestor. Although it is universally accepted that evolution of natural product biosynthesis has led to the formation of more and more complex structures, this process has rarely been documented at the level of a specific enzyme and plant group [45]. Overall, we speculated the early possible evolutionary process of spermatophyte STSs is from acyclic sesquiterpenes to cyclic sesquiterpenes, and the C6-C1 closure sesquiterpenes of 17 (small rings) may have formed earlier than C10-C1/C11-C1 closure sesquiterpenes.…”

Effect of Developmental Stages on Genes Involved in Middle and Downstream Pathway of Volatile Terpene Biosynthesis in Rose Petals

“…RcTPS39 was clustered with some genes that can catalyze monoterpenoid products, such as FvPINS (strawberry) [ 45 ], PcTPS2 and PcTPS5 ( P. campanulate ) [ 47 ], PdTPS1 ( Prunus dulcis ) [ 48 ], and MdPIN/CAM ( Malus domestica ) [ 49 ]. An evolutionary analysis on the TPS-a genes of Poaceae exhibited that some TPS-a members can convert GPP into monoterpenes derived from an initial C6-C1 closure [ 50 ]. Further studies will be conducted to investigate the ability of RcTPS39 to catalyze monoterpene products.…”