Production of constitutive and induced secondary metabolites is coordinated with growth and storage in Norway spruce saplings.

Gerd Gleixner,Susan Trumbore,Alexander Rücker,Henrik Hartmann,Axel Schmidt,Jianbei Huang,Jonathan Gershenzon

doi:10.1093/treephys/tpaa040

Abstract

A mechanistic understanding of how trees balance the trade-offs between growth, storage and defense is limited but crucial for predicting tree responses to abiotic and biotic stresses. Here we investigated how trees allocate storage of non-structural carbohydrates (NSC) to growth and constitutive and induced secondary metabolites (SM). We exposed Norway spruce (Picea abies) saplings to 5 weeks of complete darkness to induce light and/or carbon limitation and then applied methyl jasmonate (MeJA) to simulate biotic attack. We measured changes in biomass, NSC (sum of soluble sugars and starches), and constitutive and induced SM (sum of phenolic compounds and terpenoids) in current-year developing and previous-year mature needles and branches, as well as volatiles emitted from the canopy. Under darkness, NSC storage was preferentially used for constitutive biosynthesis of monoterpenes rather than biosynthesis of stilbenes and growth of developing organs, while SM stored in mature organs cannot be remobilized and recycled. Furthermore, MeJA-induced production of SM was constrained by low NSC availability in developing organs but not in mature organs grown in the dark. Emissions of volatiles were suppressed in the dark but after 1 h of re-illumination, emissions of both constitutive and induced monoterpene hydrocarbons recovered rapidly, whereas emissions of linalool and sesquiterpene produced via de novo synthesis did not recover. Our results highlight that light and/or carbon limitation may constrain constitutive and JA-induced biosynthesis of SM in coordination with growth, NSC storage and mobilization.

Highlights

Increasing evidence suggests that trees are more susceptible to biotic attacks under abiotic stress (Seidl et al 2017, Goodsman et al 2018, Klein and Hartmann 2018)
Starch levels showed large within-treatment variability, and there were no significant differences in non-structural carbohydrate (NSC) concentrations across treatments (Figure 2g, h, k and l)
The NSC were preferentially used for constitutive biosynthesis of monoterpenes rather than of stilbenes and growth in developing organs, while secondary metabolites (SM) stored in mature organs cannot be remobilized and recycled

Summary

Introduction

Increasing evidence suggests that trees are more susceptible to biotic attacks under abiotic stress (Seidl et al 2017, Goodsman et al 2018, Klein and Hartmann 2018). Trees defend against biotic attacks through strategic allocation of resources to primary (e.g., growth and storage) and secondary metabolism (e.g., protection and defense). Understanding how trees balance trade-offs in resource allocation is of critical importance for understanding tree defense response under abiotic (e.g., drought and competition) and biotic stress (e.g., attack by insects and pathogenic microbes) (Huang et al 2020). Trees defend against insects and pathogens using a complex suite of biochemical mechanisms, including both constitutive secondary metabolites (SM) (e.g., always present) to avoid initial attack and induced SM to limit damage after attack. A number of studies have investigated SM response to elevated CO2 and ozone in trees over the Past two decades, dynamics of SM have rarely been addressed in the context of environmental stress (severe drought, shade and defoliation) that reduces carbon supply (Holopainen et al 2018)

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Conclusion