Diversification of petal monoterpene profiles during floral development and senescence in wild roses: relationships among geraniol content, petal colour, and floral lifespan

K G Srikanta Dani,Susanna Pollastri,Alice Trivellini,Silvia Fineschi,Marco Michelozzi,Francesco Loreto

doi:10.1007/s00442-020-04710-z

Abstract

Wild roses store and emit a large array of fragrant monoterpenes from their petals. Maximisation of fragrance coincides with floral maturation in many angiosperms, which enhances pollination efficiency, reduces floral predation, and improves plant fitness. We hypothesized that petal monoterpenes serve additional lifelong functions such as limiting metabolic damage from reactive oxygen species (ROS), and altering isoprenoid hormonal abundance to increase floral lifespan. Petal monoterpenes were quantified at three floral life-stages (unopened bud, open mature, and senescent) in 57 rose species and 16 subspecies originating from Asia, America, and Europe, and relationships among monoterpene richness, petal colour, ROS, hormones, and floral lifespan were analysed within a phylogenetic context. Three distinct types of petal monoterpene profiles, revealing significant developmental and functional differences, were identified: Type A, species where monoterpene abundance peaked in open mature flowers depleting thereafter; Type B, where monoterpenes peaked in senescing flowers increasing from bud stage, and a rare Type C (8 species) where monoterpenes depleted from bud stage to senescence. Cyclic monoterpenes peaked during early floral development, whereas acyclic monoterpenes (dominated by geraniol and its derivatives, often 100-fold more abundant than other monoterpenes) peaked during floral maturation in Type A and B roses. Early-diverging roses were geraniol-poor (often Type C) and white-petalled. Lifetime changes in hydrogen peroxide (H2O2) revealed a significant negative regression with the levels of petal geraniol at all floral life-stages. Geraniol-poor Type C roses also showed higher cytokinins (in buds) and abscisic acid (in mature petals), and significantly shorter floral lifespan compared with geraniol-rich Type A and B roses. We conclude that geraniol enrichment, intensification of petal colour, and lower potential for H2O2-related oxidative damage characterise and likely contribute to longer floral lifespan in monoterpene-rich wild roses.

Highlights

Floral fragrance in roses is largely made of volatile monoterpenes, isoprenoid alcohols, and their oxidised and glycosylated derivatives
Type C roses were significantly poorer of total monoterpenes (< 1000 nmol gFW−1 at any stage) and poorer of geraniol compared with Type A and B (Fig. 2a)
Linalool abundance was highest in Type C Asian rose (~ 150 nmol gFW−1; Fig. 2c)

Summary

Introduction

Floral fragrance in roses is largely made of volatile monoterpenes, isoprenoid alcohols, and their oxidised and glycosylated (non-volatile) derivatives. Hybrid roses show the highest monoterpene abundance in petals at floral maturity (Bergougnoux et al 2007; Rusanov et al 2011). Petal monoterpenes are under selection to deter floral herbivores (e.g., Schiestl 2010, Junker and Blüthgen 2010), which means that temporal changes in monoterpene abundance may not strictly reflect pollination needs of a species. It is unclear whether petal monoterpenes by themselves perform constitutive functions to influence floral health and lifespan. The capacity to store and emit monoterpenes is associated with longer leaf lifespan (Dani et al 2014), and potentially with longer floral lifespan (Rogers 2012; Dani et al 2016)

Methods

Results

Conclusion