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

Plants, as a whole, are well stocked with chemical defense compounds that serve to protect against herbivores and pathogens. However, within individual plants there is great variability in the amounts of chemical defenses between different organs, tissues, and stages of growth. For example, defense compounds are usually found in greater concentrations in young compared to old leaves and in reproduction than in plant organs. These patterns have been justified by various theories, among them the optimal defense theory, but this theory has proven difficult to test until a recent report by Hunziker et al. (1).

It was developed over many years by several authors (2-6), optimal defense theory posits that defenses incur costs as they redirect resources from growth and other plant operations. The defenses are then distributed within the tissues and organs of the plant in such a way as to increase the fitness of the plant. The optimal intra-implant distribution is assumed to depend on three factors: 1) value – the contribution of each tissue or organ to developmental fitness; 2) Danger – the chance of tissue being attacked by herbivores. and 3) cost – metabolic resources needed for biosynthesis and storage. The theory of optimal defense has mostly been tested by relating the distribution of defenses in different plant species to measures of value and risk (7-9), computational models (10) and information theory (11) were also applied. However, a direct manipulation of the distribution of defense within the implant will allow for a stronger test of the theory.

The discovery of carrier proteins with a high affinity for plant defense compounds provides a way to alter the distribution of chemical defenses in healthy plants. Hunziker et al. (1) Exploitation of membrane vectors to test the effect of glucosinolate distribution on caterpillar herb in a model plant Arabidopsis thaliana. Glucosinolates are mustard oil’s distinctive glucoside defences A. thaliana and other types of cabbage, such as cabbage, broccoli and rapeseed (12). When the plant is damaged, glucosinolates are activated by glucose cleavage, resulting in the production of toxic hydrolysis products. Distribution of glucosinolates in A. thaliana It was altered by eliminating the genes encoding three glucosinolate transporters (13). This is H+The symbionts move glucosinolates from older leaves to younger ones, resulting in higher concentrations in young adults (2 μg).−1 to 4 micrograms−1 fresh weight) vs. mature (1 mcg−1) and the elderly (<0.5 mcg−1) tree leaves. However, in the carrier mutants, there was a uniform concentration of glucosinolates in leaves of all age groups (averaging about 2 μg.−1) (Diagram 1).

Diagram 1.

Testing a classic environmental theory with a biochemical tool. The optimal defense theory posits that the distribution of chemical defenses within a plant depends on the relative fitness value of the plant parts. In the 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 transfer of glucosinolates from biosynthesis sites in old and mature leaves to young leaves, where they accumulate (a). To test whether this pattern confers fitness advantages, Hunziker et al. (1) Use of a glucosinolate double transporter mutant wherein the concentration of glucosinolates is the same in all leaf age groups (B). In wild plants, caterpillars feed only on old leaves, with little effect on the plant’s survival to reproduce. However, on the vector mutation, feeding occurs only on younger leaves, resulting in early death, and showing advantages of a wild-type distribution pattern for plant suitability. The relative glucosinolate concentration in leaves is shown by the number of yellow ovals, and the vector in blue. The chemical structure shown, 4-methylsulfinylbutyl glucosinolate, is the main glucosinolate in the leaves A. thaliana (column 0).

These dramatic differences in the distribution of glucosinolates provide an ideal opportunity to test predictions of the optimal defense hypothesis. When the Egyptian cotton leafworm newly hatched (Spodoptera littoralisThe larvae, a super universal feeder, are allowed to feed on the wild type A. thaliana, they feed exclusively on old leaves because their glucosinolate concentrations are significantly lower, up to one-tenth of the concentrations found in young leaves (1). However, on the double glucosinolate transporter mutant gtr1grtr2The caterpillars completely switch to feeding on young leaves. Since young leaves are less firm, more digestible and more nutritious than older leaves, they should be a much better food source in the absence of any difference in defences.

An important control was the use of a quaternary mutation in the glucosinolate biosynthesis genes that does not produce residual glucosinolates (1, 14). with this A. thaliana Larvae also mostly feed on young leaves, indicating that the distribution of glucosinolates was the main mediating factor for leaf preference in carrier mutants, and not the differential distributions of other metabolites. Caterpillar feed selection in these experiments was closely related to plant fitness. When only the young leaves were damaged, due to their low glucosinolate content, none of the plants survived to reproduce. In contrast, when only the old leaves were damaged, all the plants survived to reproduce.

Hunziker et al. (1) Another prediction test of the theory of optimal defense: that defenses are directly assigned to the risk of herbivore attack. The risks to plant tissues are higher when other tissues of the same plant are also attacked, and in fact, after herbivores, the accumulation of several types of glucosinolates has been shown to increase in the remaining unconsumed leaves. It has been shown that glucosinolates and other defense metabolites are increased after herbivorous insects in several plant species (15).

Hunziker et al. It is an outstanding example of how discoveries of plant biochemistry provide tools for testing a classic hypothesis in plant ecology.

Regarding the distribution of defenses within the plant, the results of this investigation (1) can be generalized to other types and other classes of chemical defenses. Defense compounds are often found in greater concentrations in young than in older leaves (16), and it can now be assumed that this pattern has significant fitness benefits for plants in general. in a A. thaliana, this pattern is generated by transfer of glucosinolates from old leaves to young leaves. Similar translocations can be inferred in other species, although the site of biosynthesis may differ. In this study, it was concluded that the biosynthesis of glucosinolates mainly occurs in old and mature leaves A. thaliana, based on greater expression of biosynthetic genes than in young leaves. However, in other species, a skewed distribution of defenses in different leaf age groups can arise from synthesis elsewhere, for example, in young leaves or in another organ such as roots (17), followed by selective transfer to leaves of different ages. Unfortunately, the sites of synthesis for most plant defenses and the basis for selective transport are unknown.

The transfer of plant defenses between organs and tissues is not a general feature of all classes of defense compounds, but is likely to be limited to water-soluble substances such as alkalis, non-proteinogenic amino acids, glucosinolates, cyanogenic glycosides, iridoid glycosides and other glycosides. Lipophilic defenses, which include many terpenes, phenolic compounds, and other components of resins and essential oils, are usually synthesized in glandular trichome cells, resin ducts, or other secretory structures, and then stored there without further movement (18). However, the distribution of lipophilic defenses in plants may adopt the same patterns predicted by the optimal defense theory, although the resulting gradient of defense concentration may then arise from selective biosynthesis, not selective transport.

Optimal defense theory has generally been applied to plant defenses against herbivores rather than pathogens, but the distribution of both constitutive and inducible defenses against pathogens can also be governed by the same basic principles, resulting in different levels of protection in different organs, although there are many . Further investigation is needed. Defenses against pathogens are also mobile in plants, with primary infection in an organ sometimes resulting in systemic resistance throughout the plant (19). Although this acquired systemic resistance is usually attributed to mobile signaling molecules, actual anti-disease agents can also be mobile, as shown in the current study of glucosinolates (1).

Hunziker et al. (1) is an outstanding example of how discoveries of plant biochemistry can provide tools for testing a classic hypothesis in plant ecology. Our knowledge of plant defense vectors has increased rapidly in recent years (20, 21), and these proteins can be used in a range of biochemical, physiological and environmental studies. In plant protection, carriers give plants the ability to quickly mobilize chemical defenses to where they are needed and recover them from the organ when they are not needed. Thus, these proteins may be major innovations in allowing plants to survive the attack of herbivores and pathogens without breaking their metabolic budgets.


  • Author contributions: JG and CU wrote the paper.

  • The book declares no competing interest.

  • See the accompanying article, “Feeding preference for herbivores supports optimal defense theory of specialized metabolites within plants,” 10.1073/pnas.2111977118.

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