Abstract
Dictyostelids, or social amoebae, have a unique life style in forming multicellular fruiting bodies from unicellular amoeboids upon starvation. Recently, dictyostelids were found to contain terpene synthase (TPS) genes, a gene type of secondary metabolism previously known to occur only in plants, fungi and bacteria. Here we report an evolutionary functional study of dictyostelid TPS genes. The number of TPS genes in six species of dictyostelids examined ranges from 1 to 19; and the model species Dictyostelium purpureum contains 12 genes. Using in vitro enzyme assays, the 12 TPS genes from D. purpureum were shown to encode functional enzymes with distinct product profiles. The expression of the 12 TPS genes in D. purpureum is developmentally regulated. During multicellular development, D. purpureum releases a mixture of volatile terpenes dominated by sesquiterpenes that are the in vitro products of a subset of the 12 TPS genes. The quality and quantity of the terpenes released from D. purpureum, however, bear little resemblance to those of D. discoideum, a closely related dictyostelid. Despite these variations, the conserved clade of dictyostelid TPSs, which have an evolutionary distance of more than 600 million years, has the same biochemical function, catalyzing the formation of a sesquiterpene protoillud-7-ene. Taken together, our results indicate that the dynamic evolution of dictyostelid TPS genes includes both purifying selection of an orthologous group and species-specific expansion with functional divergence. Consequently, the terpenes produced by these TPSs most likely have conserved as well as species-adaptive biological functions as chemical languages in dictyostelids.
Highlights
terpene synthase (TPS) genes encode enzymes that catalyze the conversion of oligoprenyl diphosphates of various chain lengths to terpene hydrocarbons or alcohols of enormous structural diversity[11,12]
Such variation in the number of TPS genes poses intriguing questions: do paralogs in each species have similar or different catalytic functions? do paralogs and orthologs have similar or diverging expression patterns? how do the in vitro enzyme activities and gene expression patterns determine the chemical diversity of volatile terpenes produced by each dictyostelid species? what biological functions do these TPS genes and their terpene products have? Towards answering these questions, in this report, we investigate the functional evolution of the TPS family in dictyostelids using D. purpureum as the main model species
This study has led to new insights into the diversity and functional evolution of the TPS gene family in dictyostelid social amoebae
Summary
TPS genes encode enzymes that catalyze the conversion of oligoprenyl diphosphates of various chain lengths to terpene hydrocarbons or alcohols of enormous structural diversity[11,12]. The finding that dictyostelids contain TPS genes is significant in a number of ways It indicates a wider distribution of TPS genes, which were previously observed only in plants and fungi among the eukaryotes. It raises an intriguing question about the function of TPS genes in dictyostelids. Dictyostelium discoideum has been used as a model species for functional characterization of TPS genes This species contains 9 TPS genes, all of which were shown to be expressed and active for the in vitro production of sesquiterpenes, while some of them produce monoterpenes and diterpenes. How do the in vitro enzyme activities and gene expression patterns determine the chemical diversity of volatile terpenes produced by each dictyostelid species? Such variation in the number of TPS genes poses intriguing questions: do paralogs in each species have similar or different catalytic functions? do paralogs and orthologs have similar or diverging expression patterns? how do the in vitro enzyme activities and gene expression patterns determine the chemical diversity of volatile terpenes produced by each dictyostelid species? what biological functions do these TPS genes and their terpene products have? Towards answering these questions, in this report, we investigate the functional evolution of the TPS family in dictyostelids using D. purpureum as the main model species
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