Abstract
Land plants protect themselves from ultraviolet-B (UV-B) by accumulating UV-absorbing metabolites, which may also function as anti-insect toxins. Previous studies have shown that UV-B enhances the resistance of different plant species to pierce-sucking pests; however, whether and how UV-B influences plant defense against chewing caterpillars are not well understood. Here we show that UV-B treatment increased Spodoptera litura herbivory-induced jasmonic acid (JA) production in Arabidopsis and thereby Arabidopsis exhibited elevated resistance to S. litura. Using mutants impaired in the biosynthesis of JA and the defensive metabolites glucosinolates (GSs), we show that the UV-B-induced resistance to S. litura is dependent on the JA-regulated GSs and an unidentified anti-insect metabolite(s). Similarly, UV-B treatment also enhanced the levels of JA-isoleucine conjugate and defense-related secondary metabolites in tobacco, rice, and maize after these plants were treated with simulated herbivory of lepidopteran insects; consistently, these plants showed elevated resistance to insect larvae. Using transgenic plants impaired in JA biosynthesis or signaling, we further demonstrate that the UV-B-enhanced defense responses also require the JA pathway in tobacco and rice. Our findings reveal a likely conserved JA-dependent mechanism by which UV-B enhances plant defense against lepidopteran insects.
Highlights
Insect feeding is one of the major biotic factors threatening plant survival, and during coevolution, plant have developed complex defense systems to contend with insect herbivores[1]
Similar to the WT plants, uvr[] and gs[4] mutants exhibited elevated resistance to S. litura in the UV-B-treated group (Fig. 1A), indicating that UVR8 is not involved in UV-B-enhanced defense and that certain metabolites that were regulated by UV-B, but not GSs, conferred resistance to S. litura
Previous studies have shown that UV-B increases plant defense against pathogens and insects, and this is correlated with UV-B-induced accumulation of defense-related metabolites in the epidermal tissues[13,15,16,24]
Summary
Insect feeding is one of the major biotic factors threatening plant survival, and during coevolution, plant have developed complex defense systems to contend with insect herbivores[1]. Genetic and biochemical evidence revealed that JA-Ile (JA-isoleucine conjugate), instead of JA itself, induces many JA responses against herbivory[4,7], and plants impaired in JA-Ile accumulation are very susceptible to lepidopteran insect feeding[8,9]. Genetic evidence is still lacking to support the role of the JA pathway in UV-B-induced defense against chewing caterpillars[22] It is unclear whether UV-B positive affects insect resistance in monocots, and if so, by what mechanisms. By comparing UV-B-treated and untreated plants, we show that UV-B radiation on Arabidopsis, tobacco (Nicotiana tabacum), rice (Oryza sativa), and maize (Zea mays) plants elevated these plants’ JA/JA-Ile levels, defensive secondary metabolites, and resistance to lepidopteran chewing insects. Using genetically modified plants silenced in JA biosynthesis or signaling, we further demonstrate that the JA pathway plays a major role in enhancing UV-B-pretreated plants’ defense against chewing caterpillars, and this mechanism is likely to be conserved in both mono- and dicots
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