Jonathan Gershenzon and Chhana Ullah

PNAS January 25, 2022 119 (4) e2120277119

Fig. 1. Testing a classical ecological theory with a biochemical tool. The optimal defense theory posits that the distribution of chemical defenses within a plant is based on the relative fitness value of plant parts. In wild-type A. thaliana, glucosinolates are present in much higher concentration in young leaves (y) than in mature (m) or old (o) leaves, due to the transport of glucosinolates out of their sites of biosynthesis in the old and mature leaves to young leaves, where they accumulate (A). To test whether this pattern confers fitness benefits, Hunziker et al. (1) employ a double glucosinolate transporter mutant in which the concentration of glucosinolates is the same in all leaf age classes (B). On wild-type plants, caterpillars fed only on older leaves, with little effect on plant survival to reproduction. However, on the transporter mutant, feeding occurred only on younger leaves, leading to premature death, and showing the advantages of the wild-type distribution pattern for plant fitness. Relative glucosinolate concentration in leaves is depicted by the number of yellow ovals, and the transporter is given in blue. The chemical structure shown, 4-methylsulfinylbutyl glucosinolate, is the major glucosinolate in the leaves of A. thaliana (Col-0).

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. (1).

Developed over many years by several authors (2⇓⇓⇓–6), 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 (7⇓–9), and computational models (10) and information theory (11) have also been applied. However, the direct manipulation of intraplant defense distribution would allow a more powerful test of the theory.

See more: https://www.pnas.org/content/119/4/e2120277119