Research Article: Testing the optimal defense hypothesis in nature: Variation for glucosinolate profiles within plants

Date Published: July 21, 2017

Publisher: Public Library of Science

Author(s): Rose A. Keith, Thomas Mitchell-Olds, Cesar Rodriguez-Saona.

http://doi.org/10.1371/journal.pone.0180971

Abstract

Plants employ highly variable chemical defenses against a broad community of herbivores, which vary in their susceptibilities to specific compounds. Variation in chemical defenses within the plant has been found in many species; the ecological and evolutionary influences on this variation, however, are less well-understood. One central theory describing the allocation of defenses in the plant is the Optimal Defense Hypothesis (ODH), which predicts that defenses will be concentrated in tissues that are of high fitness value to the plant. Although the ODH has been repeatedly supported within vegetative tissues, few studies have compared vegetative and reproductive tissues, and the results have not been conclusive. We quantified variation in glucosinolate profile and tissue value between vegetative and reproductive tissues in Boechera stricta, a close relative of Arabidopsis. B. stricta manufactures glucosinolates, a set of defensive compounds that vary genetically and are straightforward to quantify. Genetic diversity in glucosinolate profile has been previously demonstrated to be important to both herbivory and fitness in B. stricta; however, the importance of glucosinolate variation among tissues has not. Here, we investigate whether allocation of glucosinolates within the plant is consistent with the ODH. We used both clipping experiments on endogenous plants and ambient herbivory in a large-scale transplant experiment at three sites to quantify fitness effects of loss of rosette leaves, cauline leaves, and flowers and fruits. We measured glucosinolate concentration in leaves and fruits in the transplant experiment, and asked whether more valuable tissues were more defended. We also investigated within-plant variation in other aspects of the glucosinolate profile. Our results indicated that damage to fruits had a significantly larger effect on overall fitness than damage to leaves, and that fruits had much higher concentrations of glucosinolates, supporting the ODH. This is, to the best of our knowledge, the first study to explicitly compare both tissue value and chemical defense concentrations between vegetative and reproductive tissues under natural conditions.

Partial Text

Plants manufacture a wide range of defenses against herbivores; variation in these defenses is common, both among individuals and within a single plant. Variation in physical defenses among plant tissues is often easily observable; many chemical defenses vary among tissues as well [1]. Studies of this variation have given rise to a number of general hypotheses regarding the evolution and allocation of defenses. The Optimal Defense Hypothesis (ODH) is one of the primary theories addressing the distribution of defenses within a plant. The ODH, which very broadly states that defenses will be allocated in any way that is adaptive to the plant, may be extended into a set of specific, testable predictions for defense allocation [2–4]. Within the plant, the ODH predicts that defenses will be concentrated in tissues that are at higher risk of herbivory and/or tissues that are more valuable; that is, tissues which if lost to herbivores cause greater loss of plant fitness [2–4].

Our results support the ODH. In both the clipping treatment and the ambient herbivory experiment, we found that damage to fruits was significantly more detrimental to fitness than loss of leaf tissue. Correspondingly, fruits had a much higher concentration of glucosinolates. These results support the commonly-made assumption that reproductive tissues are of higher fitness value than vegetative tissues. These results also unambiguously support the ODH; the tissue of higher value has a higher investment in defense.

 

Source:

http://doi.org/10.1371/journal.pone.0180971

 

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