Abstract

Trade-offs between plant growth and defense depend on environmental resource availability. Plants are predicted to prioritize growth when environmental resources are abundant and defense when environmental resources are scarce. Nevertheless, such predictions lack a whole-plant perspective—they do not account for potential differences in plant allocation above- and belowground. Such accounting is important because leaves and roots, though both critical to plant survival and fitness, differ in their resource-uptake roles and, often, in their vulnerability to herbivores. Here we aimed to determine how water availability affects plant allocation to multiple metabolic components of growth and defense in both leaves and roots. To do this, we conducted a meta-analysis of data from experimental studies in the literature. We assessed plant metabolic responses to experimentally reduced water availability, including changes in growth, nutrients, physical defenses, primary metabolites, hormones, and other secondary metabolites. Both above- and belowground, reduced water availability reduced plant biomass but increased the concentrations of primary metabolites and hormones. Importantly, however, reduced water had opposite effects in different organs on the concentrations of other secondary metabolites: reduced water increased carbon-based secondary metabolites in leaves but reduced them in roots. In addition, plants suffering from co-occurring drought and herbivory stresses exhibited dampened metabolic responses, suggesting a metabolic cost of multiple stresses. Our study highlights the needs for additional empirical studies of whole-plant metabolic responses under multiple stresses and for refinement of existing plant growth-defense theory in the context of whole plants.

Highlights

  • Plants experience many forms of stress, from both the abiotic and the biotic environment

  • The literature search resulted in 1,475 publications, of which 61 papers published between January 1992 and August 2017 met our criteria

  • Considering only the studies that experimentally manipulated water availability we found three types of experiments: (1) studies that reduced the percentage of moisture in the soil compared to the control (44%), (2) studies that reduced the amount of water given to the plant (28%), and (3) studies that deprived the plants of water for the length of the study (28%)

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Summary

Introduction

Plants experience many forms of stress, from both the abiotic and the biotic environment. Plants have evolved various physiologic and metabolic responses to individual stresses, but the nature of such responses strongly depends on whether and how stresses co-occur in the plant’s environment (Atkinson and Urwin, 2012; Suzuki et al, 2014; Nguyen et al, 2016). Roots are the first responders to many kinds of stress (Brunner et al, 2015; Weemstra et al, 2016), work to date on growth-defense trade-offs and optimal defense has focused mostly aboveground, on shoots and leaves, rather than on the whole plant (van Dam, 2009). There are still few predictions about how simultaneous abiotic and biotic stresses should drive whole-plant allocation strategies

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