Nutrient-rich plants emit a less intense blend of volatile isoprenoids

Abstract

The emission of isoprenoids (e.g. isoprene and monoterpenes) by plants plays an important defensive role against biotic and abiotic stresses. Little is known, however, about the functional traits linked to species-specific variability in the types and rates of isoprenoids emitted and about possible co-evolution of functional traits with isoprenoid emission type (isoprene emitter, monoterpene emitter or both). We combined data for isoprene and monoterpene emission rates per unit dry mass with key functional traits (foliar nitrogen (N) and phosphorus (P) concentrations, and leaf mass per area) and climate for 113 plant species, covering the boreal, wet temperate, Mediterranean and tropical biomes. Foliar N was positively correlated with isoprene emission, and foliar P was negatively correlated with both isoprene and monoterpene emission rate. Nonemitting plants generally had the highest nutrient concentrations, and those storing monoterpenes had the lowest concentrations. Our phylogenetic analyses found that the type of isoprenoid emission followed an adaptive, rather than a random model of evolution. Evolution of isoprenoids may be linked to nutrient availability. Foliar N and P are good predictors of the type of isoprenoid emission and the rate at which monoterpenes, and to a lesser extent isoprene, are emitted.

Keywords: monoterpenes; nitrogen (N); nutrient availability; phosphorus (P); phylogeny; volatile organic compounds (VOCs).

Figure 1

Average (± standard error) PC1 and PC2 scores per emission type: non-emitters (NE), monoterpene and isoprene emitters only (MTP and ISP, respectively), and emitters of monoterpenes and isoprene (TWO). MTPs and TWOs are the emission types that store monoterpenes. Different upper- and lowercase letters (e.g., AB – ab) indicate statistically significant differences at the 0.05 level amongst emission types for the PC1 and PC2 axes, respectively, following Tukey’s HSD test. Red arrows represent the loadings in the phylogenetic PCA. Factor loadings can be found in Table S3.

Figure 2

Partial-residual plots showing the relationships between foliar nutrient concentrations of nitrogen (N) and phosphorus (P) and their stoichiometry (N:P ratio) with the probability that a species stores monoterpenes (1) or not (0) (a, b), or that it emits either monoterpenes (0) or isoprene (1) (c, d), and with emission rates of isoprene (e, f) and monoterpenes (g, h). Results of the models are presented in Table 1. Ln indicates that the variable was log-transformed. Partial-residual plots show variation in the dependent variable in relation to a given predictor (the fitted line), while simultaneously controlling for all other predictors in the model. The blue-shaded area indicated the 95% confidence bands of the slope around the fitted line. Results of the models are presented in Table 1. DW, dry weight.

Figure 3

Phylogenetic tree including the probability of emission type of ancestor nodes (large circles) as pie charts. Small circles indicate the emission type of the species. The ancestral reconstruction was performed using 1000 stochastic character mapped trees (see Methods for further information). NE, non-emitters; MTP, monoterpene emitters only; ISP, isoprene emitters only; TWO, emitters of both monoterpenes and isoprene. MTPs and TWOs are the emission types that store monoterpenes.

Figure 4

Optimal values of the predictor variables for the six emission types estimated with OUMV models (Ornstein-Uhlenbeck assuming different optimal values and phenotypic variability for each emission type) for the 1000 stochastic character maps (in the graphs there is a point for every emission type and model). The results for MAT were calculated with OUM models (assuming different state means but equal multiple rates of evolution) due to lower AICc (see Table S4). N, foliar nitrogen concentration; P, foliar phosphorus concentration; LMA, leaf mass per area; MAT, mean annual temperature; MAP, mean annual precipitation; NE, non-emitters; ISP, isoprene emitters only; MTP, monoterpene emitters only; MTPs, monoterpene emitters only that store monoterpenes; TWO, emitters of both isoprene and monoterpenes; TWOs, emitters of both isoprene and monoterpenes that also store monoterpenes; DW, dry weight. Medians are presented in Table 2.