Plants protect themselves from herbivores by optimizing the distribution of chemical defenses

Plants, as a whole, are well stocked with chemical defense compounds that function in protection against herbivores and pathogens. Within individual plants, however, there is extensive variation in the amounts of chemical defenses among different organs, tissues, and developmental stages. For example, defense compounds are typically present in greater concentrations in young compared to old leaves and in reproductive compared to vegetative organs. These patterns have been rationalized by various theories, chief among them the optimal defense theory, but this theory has proved very difficult to test until a recent report from Hunziker et al. 

Developed over many years by several authors, the optimal defense theory assumes that defenses incur costs because they redirect resources from growth and other plant processes. Hence defenses are distributed within plant tissues and organs in a way that maximizes plant fitness. The optimal intraplant distribution is hypothesized to be based on three factors: 1) value—the contribution of each tissue or organ toward evolutionary fitness; 2) risk—the chance of a tissue being attacked by herbivores; and 3) cost—the metabolic resources needed for biosynthesis and storage. The optimal defense theory has been mostly tested by correlating the distribution of defenses in various plant species with measurements of value and risk, and computational models and information theory have also been applied. However, the direct manipulation of intraplant defense distribution would allow a more powerful test of the theory.

The discovery of transporter proteins with high affinities for plant defense compounds provides a way to alter the distribution of chemical defenses in intact plants. Hunziker et al. exploit membrane transporters to test the influence of glucosinolate distribution on caterpillar herbivory in the model plant Arabidopsis thaliana. Glucosinolates are the characteristic mustard oil glucoside defenses of A. thaliana and other Brassicaceae species, such as cabbages, broccoli, and rapeseed. Upon plant damage, glucosinolates are activated by glucose cleavage, leading to the production of toxic hydrolysis products. The distribution of glucosinolates in A. thaliana was altered by knocking out the genes encoding three glucosinolate transporters. These H+/symporters mobilize glucosinolates from older to younger leaves, leading to higher concentrations in young (2 µmol⋅g−1 to 4 µmol⋅g−1 fresh weight) compared to mature (1 µmol⋅g−1) and older (<0.5 µmol⋅g−1) leaves. However, in transporter mutants, there was a uniform concentration of glucosinolates in leaves of all age classes (averaging about 2 µmol⋅g−1)

Read the complete research at www.pnas.org

Plants protect themselves from herbivores by optimizing the distribution of chemical defenses, Jonathan Gershenzon, Chhana Ullah
Proceedings of the National Academy of Sciences Jan 2022, 119 (4) e2120277119; DOI: 10.1073/pnas.2120277119 


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