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 processesand 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

Genetic variation, environment and demography intersect to shape Arabidopsis defense metabolite variation across Europe

“…This creates a complex system to which a plant must develop adaptation strategies to ensure survival and reproduction. Metabolites are frequent keys to these strategies, involving the production and accumulation of different metabolites from signaling hormones, primary metabolites and a wide array of multi-functional specialized metabolites (Erb & Kliebenstein, 2020;Hanower & Brzozowska, 1975;Hayat et al, 2012;Kim et al, 2012;D J Kliebenstein, 2004;Malcolm, 1994;Thakur & Rai, 1982;Wolters & Jürgens, 2009;Yang, Lin, & Kao, 2000).…”

“…A complication in the plants ability to create an optimal blend of metabolite-based strategies is the fact that individual specialized metabolites can have contrasting effects in a complex environment. For example, individual specialized metabolites can provide defense against some attackers while simultaneously causing sensitivity to other biotic attackers or abiotic stresses (Agrawal, 2000;Bialy, Oleszek, Lewis, & Fenwick, 1990;Erb & Kliebenstein, 2020;Futuyma & Agrawal, 2009;Hu et al, 2018;Lankau, 2007;Opitz & Müller, 2009;Uremıs, Arslan, Sangun, Uygur, & Isler, 2009;Züst & Agrawal, 2017). This creates offsetting ecological benefits and costs for individual metabolites that when summed across all the metabolites means that there are complex selective pressures driving the differentiation of metabolic profiles within a species and shaping genetic variation within and between populations depending on the diverse challenges faced (Fan, Leong, & Last, 2019;R.…”

Transcriptome Analysis Reveals a Potential Role of Benzoxazinoid in Regulating Stem Elongation in the Wheat Mutant qd

“…Benzoxazinoids are traditional crucial elements for crop disease resistance ( Ahmad et al, 2011 ; Tzin et al, 2017 ). Although benzoxazinoids are considered protective secondary metabolites, secondary metabolites are multifunctional and can function as potent regulators of plant growth ( Erb and Kliebenstein, 2020 ). Benzoxazinoids have been indicated to play a role in improving plant tolerance to soil salinity ( Makleit, 2005 ).…”

A Phytochemical Perspective on Plant Defense Against Nematodes

“…Also, "secondary" metabolites should not be seen as "non-essential": particularly under stressful conditions, impairments in secondary metabolism are often lethal (Seigler, 1998;Hartmann, 2007). Interested readers are referred to an excellent review article (Erb and Kliebenstein, 2020) for an in-depth discussion of plant secondary metabolites and their relation to primary metabolites.…”