Plant secondary metabolites as defenses, regulators and primary metabolites- The blurred functional trichotomy

Abstract

The plant kingdom produces hundreds of thousands of small molecular weight organic compounds. Based on their assumed functions, the research community has classified them into three overarching groups: primary metabolites which are directly required for plant growth, secondary (or specialized) metabolites which mediate plant-environment interactions and hormones which regulate organismal processes, including metabolism. For decades, this functional trichotomy has shaped theory and experimentation in plant biology. However, evidence is accumulating that the boundaries between the different types of metabolites are blurred. An increasing number of mechanistic studies demonstrate that secondary metabolites are multifunctional and can act as potent regulators of plant growth and defense. Secondary metabolites are also re-integrated into primary metabolism, thus behaving like primary metabolites sensu lato. Several adaptive scenarios may have favored this functional diversity for secondary metabolites, including signaling robustness and cost-effective storage and recycling. Secondary metabolite multi-functionality can provide new explanations for ontogenetic patterns of defense production and can refine our understanding of plant-herbivore interactions, in particular by accounting for the discovery that adapted herbivores misuse plant secondary metabolites for multiple purposes, some of which mirror their functions in plants. In conclusion, recent work unveils the limits of our current classification system for plant metabolites and suggests that viewing them as integrated components of metabolic networks that are dynamically shaped by environmental selection pressures and transcend multiple trophic levels can improve our understanding of plant metabolism and plant-environment interactions.

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