Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy

Abstract

The plant kingdom produces hundreds of thousands of low molecular weight organic compounds. Based on the assumed functions of these compounds, 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 and metabolism. For decades, this functional trichotomy of plant metabolism has shaped theory and experimentation in plant biology. However, exact biochemical boundaries between these different metabolite classes were never fully established. A new wave of genetic and chemical studies now further blurs these boundaries by demonstrating that secondary metabolites are multifunctional; they can function as potent regulators of plant growth and defense as well as 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 multifunctionality 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 functional classification system for plant metabolites. Viewing secondary metabolites 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.

Figure 1.

Low molecular weight compounds in plants are functionally classified as primary metabolites, secondary metabolites, or hormones. Present work on plant secondary metabolites demonstrates that many of them also have regulatory roles, and some are demonstrated precursors of primary metabolites. Note that primary metabolites and hormones also show functional overlap with the other metabolite classes (not discussed here). These findings blur the functional trichotomy of plant metabolism and call for a reassessment of ecological and evolutionary frameworks that are based on this model.

Figure 2.

Glucosinolates and benzoxazinoids as examples of secondary metabolites that blurr the functional trichotomy of plant metabolism. Different functions of glucosinolates in Arabidopsis and benzoxazinoids in maize and wheat are depicted. Genes that are known to be involved in the different functions are indicated. Note that a direct role of benzoxazinoids and glucosinolates as plant primary metabolites (for instance, in the context of nitrogen/sulfur and/or energy storage) has not been clearly demonstrated so far. *MEDs and KFBs are likely regulated by aldoxime precursors of glucosinolates. For references, see the article.

Figure 3.

Functional integration of plant secondary metabolites shapes plant–herbivore and tritrophic interactions. Schematic representation of how different functions of secondary metabolites are used by plants, herbivores, and natural enemies of herbivores is shown. Plants use secondary metabolites for multiple purposes, including resistance, regulation, and primary metabolism (see Fig. 2). Recent work suggests that this multifunctionality is mirrored in adapted herbivores, which also use secondary metabolites for multiple purposes, including similar and new functions. Little is known about how adapted natural enemies use secondary metabolites, but multifunctional integration across three trophic levels is likely (Box 2). Circles represent hypothetical individual secondary metabolites (for color code, refer to Figs. 1 and 2). Solid lines indicate metabolic connections within an organism. Dashed lines indicate similar functions of the same compounds in different organisms.

Box 1.

Case study of secondary metabolite multifunctionality. Cited articles: Glauser et al., 2011; Robert et al., 2012, ; Maag et al., 2016.

Box 2.

Multifunctionality of plant secondary metabolites in tritrophic interactions. Cited articles: Fink and Brower, 1981; Hunter, 2003; Sarfraz et al., 2009; Sloggett and Davis, 2010; Aartsma et al., 2017; Rafter et al., 2017; Robert et al., 2017; Turlings and Erb, 2018; Sun et al., 2019a; Ugine et al., 2019; Zhang et al., 2019.