The information landscape of plant constitutive and induced secondary metabolite production

Highlights

• Function and evolution of inducibility of resistance still remain unclear.

• Most basic function of plant secondary metabolite production is information transfer.

• Constitutive production of secondary metabolites determines herbivore host choice.

• Inducibility: plants can use expanded interaction arena to cope with herbivore attack.

Resistance against antagonist organisms, such as herbivores, has been identified as a major function of constitutive and stress-inducible production of plant secondary metabolites (PSMs). The mechanism through which constitutive expression and inducibility mediate resistance and, hence physiological and ecological factors that affect their evolution are still little understood. Here I propose information transfer as the least common denominator function of PSM production. In this framework constitutively produced PSMs represent the first line of defense through functioning as toxins, cues associated with toxicity and as detractants that interfere with antagonist host-search patterns. Information made available and utilizable by inducibility of secondary metabolite production allows plants to include the associated biological communities to cope with antagonists and to more efficiently target a specific attacker.

Introduction

The immense diversity of plant secondary metabolites (PSMs; >100 000 already identified) has long fascinated researchers. Initially thought to be mere byproducts of primary metabolism, PSMs have been found to serve a multitude of ecological functions [1] and have been a main focus of ecological and evolutionary studies into plant defense theory [2]. Plant metabolism in general and secondary metabolism in particular under unchallenged, low-stress situations (constitutive) is frequently found to be characteristic to species or higher taxonomic units, although chemical phylogeny hypotheses do not always match phylogenies based on molecular and genetic data [3]. However, a large diversity of abiotic and biotic environmental factors are found to significantly affect evolution and phenotypic plasticity of plant secondary metabolism, which led to a number of hypotheses on the adaptive value of PSMs to cope with environmental stresses [4]. Most notably, constitutive and herbivory-induced PSM production are central to the hypotheses on plant defenses against herbivory. Plant chemicals mediate toxicity, digestibility-reducing, repellent or indirect defensive effects [e.g. attraction of natural enemies of herbivores by herbivore-induced volatile organic compound (VOC) emission]. Thus in the plant defense framework PSMs function as resistance-mediating traits and herbivores are hypothesized as major agents of natural selection on both the constitutive and inducible expression of chemical traits [5]. Accordingly, herbivores choose a plant host and the specific tissues based on its nutritional composition and PSM production [6].

Two basic hypothetical concepts dominated the discussion about the evolutionary relationship between constitutive and inducible PSM production. On one hand through inducing PSMs only when needed (when herbivores attack), plants can optimize their investment into costly defenses (Box 1) [7^•]. As an alternative to cost-saving it was suggested that the change of the plant phenotype in response to herbivory itself is functional, because it provides a ‘moving target’ for the attacking herbivore [8]. Both hypotheses in principle assume a defensive function of PSM but differ in their predictions about the costs associated with maintaining the metabolic ability to change phenotype in response to stress (Box 1).

Recent application of new molecular approaches allow us to more precisely compare costs of constitutive resistance expression with the costs associated with the maintenance of endogenous signaling pathways that underlie inducibility of resistance [11]. These new assessments suggest significant fitness costs of maintaining early wound signaling cascades. In addition ecological costs associated with inducibility are thought to be largely underestimated [11, 12]. Thus, it is rather the costs and benefits that result from the way PSMs mediate interactions with a diverse community of organisms (ecological costs and benefits) that maintain natural variation in plant defense strategies. Hence, defense strategies should vary with the biological community the plant is interacting with as well as the biotic and abiotic environmental conditions in which these interactions occur.

With increasing importance of complex community-wide interactions, PSM production loses its relative importance as a defense per se, and is increasingly and more generally important as information that connects the parts of the interaction network. When conceptualizing secondary metabolite production as information, the constitutively produced arsenal of secondary metabolites becomes the first line of a plant's defense, limiting the number of potential herbivores, but also mutualists interacting with plant metabolites [13] (Figure 1a). Organisms entering a plant community that includes potential hosts are challenged to find the appropriate host species (community level) and pheno-/chemotype (population level) in a sea of non-hosts that provide a potentially conflicting environmental context, the information landscape, from which host information has to be filtered. A plant's susceptibility to herbivores thus is predicted to depend on the population genetic structure (chemotype diversity and distribution) and the community neighborhood. Plant induced responses, in contrast, can alter the spatio-temporal distribution and diversity of plant phenotypes within a population on an ecological time scale and so change the information available to a host-searching herbivore and other organisms interacting with the plant, including natural enemies of herbivores, plant mutualists, or neighboring plants. Thus, induced PSM production becomes a second line of defense that presumably allows a more targeted response (quantitative and qualitative) to attacking herbivores but also the alteration of information provision to other interacting organisms (Figure 1b).

This paper outlines predictions and reviews recent studies associated with the concept of chemical information transfer within communities of organisms interacting with plants. The strength of natural selection acting on the content of this information is dependent on the major interacting organisms as well as the environment (the ecological context) in which interactions are played out.