Abstract
The development of flower scents was a crucial event in biological evolution, providing olfactory signals by which plants can attract pollinators. In this study, bioinformatics, metabolomics, and biochemical and molecular methodologies were integrated to investigate the candidate genes involved in the biosynthesis of volatile components in two cultivars of Freesia x hybrida, Red River® and Ambiance, which release different categories of compounds. We found that terpene synthase (TPS) genes were the pivotal genes determining spatiotemporal release of volatile compounds in both cultivars. Eight FhTPS genes were isolated and six were found to be functional: FhTPS1 was a single-product enzyme catalyzing the formation of linalool, whereas the other four FhTPS proteins were multi-product enzymes, among which FhTPS4, FhTPS6, and FhTPS7 could recognize geranyl diphosphate and farnesyl diphosphate simultaneously. The FhTPS enzymatic products closely matched the volatile terpenes emitted from flowers, and significant correlations were found between release of volatile terpenes and FhTPS gene expression. Graphical models based on these results are proposed that summarize the biosynthesis of Freesia floral volatile terpenes. The characterization of FhTPS genes paves the way to decipher their roles in the speciation and fitness of Freesia, and this knowledge could also be used to introduce or enhance scent in other plants.
Highlights
The emergence of the specialized secondary metabolic pathways improved the adaptive ability of plants during their evolution (Waters,2003).In particular,the widespread biosynthesis of volatile organic compounds (VOCs) in plant tissues has served multiple biological functions, including defense against pathogens, parasites, and herbivores (Holopainen and Gershenzon, 2010).The evolutionary emergence of angiosperms led to further exploitation of volatile compounds in flowers in order to attract pollinators (Filella et al, 2013; Byers et al, 2014).VOCs can be divided according to their independent origins into three categories, terpenes, benzenoid aromatics, and fatty acid derivatives (Dudareva et al, 2013), among which terpenes with relatively low molecular weight account for the largest proportion (Chen et al, 2011; Dudareva et al, 2013).The metabolic pathways of volatile terpenes have been well characterized in the plant kingdom
In the past two decades, terpene synthases have been extensively examined in terrestrial plants, and are usually divided into seven clades, designated as TPS-a, TPS-b, TPS-c, TPS-d, TPS-e/f,TPS-g, and TPS-h.TPS-a,TPS-b, and TPS-g are recognized as angiosperm-specific clades (Chen et al, 2011)
FhTPS1, FhTPS2, FhTPS3, and FhTPS5 were grouped in the TPS-b clade, containing the RRX8W motif in the N-terminal region for monoterpene cyclization, which is commonly found in angiosperm-specific monoterpene synthases (Hyatt et al, 2007; Chen et al, 2011)
Summary
The emergence of the specialized secondary metabolic pathways improved the adaptive ability of plants during their evolution (Waters,2003).In particular,the widespread biosynthesis of volatile organic compounds (VOCs) in plant tissues has served multiple biological functions, including defense against pathogens, parasites, and herbivores (Holopainen and Gershenzon, 2010).The evolutionary emergence of angiosperms led to further exploitation of volatile compounds in flowers in order to attract pollinators (Filella et al, 2013; Byers et al, 2014).VOCs can be divided according to their independent origins into three categories, terpenes, benzenoid aromatics, and fatty acid derivatives (Dudareva et al, 2013), among which terpenes with relatively low molecular weight (such as 10-carbon monoterpenes and 15-carbon sesquiterpenes) account for the largest proportion (Chen et al, 2011; Dudareva et al, 2013).The metabolic pathways of volatile terpenes have been well characterized in the plant kingdom. In maize, TPS10 was induced in herbivore-damaged leaves and TPS23 was responsible for attracting natural enemies of herbivores through controlling (E)-β-caryophyllene emissions (Köllner et al, 2009; Capra et al, 2015). Their role in the biosynthesis of flower scents might be important from the perspective of plant evolution and speciation, as they perform crucial roles in attracting pollinators and, in combination with other floral traits, determine plant pollination syndromes (Ojeda et al, 2013). Given the importance of floral scent in evolution and speciation (Parachnowitsch et al, 2012; Adler and Irwin, 2012), more TPS genes should be isolated from poorly studied clades of plants with diverse animal pollinators, especially petaloid monocots
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