Ultraviolet-B enhances the resistance of multiple plant species to lepidopteran insect herbivory through the jasmonic acid pathway

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.

Figure 1

JA pathway is required for UV-B-enhanced Arabidopsis resistance to S. litura. (A) Mean masses (±SE) of S. litura, after 12 days of feeding on control and UV-B-pretreated wild-type (WT), uvr8-2, gs4, and dde2-2 Arabidopsis. Control and UV-B-pre-exposed WT and mutant Arabidopsis were treated with simulated herbivory (SH+) or left untreated (SH−), and the levels of JA (B), JA-Ile (C), and total GSs (D) were determined in samples collected at 2 h (for B and C) or 48 h (for D). For A, n = 30-50; for B–D, n = 6–8. Asterisks (*P < 0.05, **P < 0.01, Student’s t-test) and different letters (P < 0.05, Duncan’s multiple range test) indicate significant differences between treatments within the same genotype.

Figure 2

JA pathway is essential for UV-B-induced N. tabacum defense against S. litura. (A) Mean masses (±SE) of S. litura, eight days after feeding on control and UV-B-pretreated wild type (WT) and irAOC tobacco plants. Control and UV-B-pre-exposed WT and irAOC tobacco plants were treated with simulated herbivory (SH+) or left untreated (SH−), and the levels of JA and JA-Ile (B), TPI activity (C), and total DTGs (D) were quantified in samples harvested at 2 h (for B) or 48 h (for C and D). For A, n = 30–50; for B–D, n = 6–8. Asterisks (**P < 0.01, Student’s t-test) and different letters (P < 0.05, Duncan’s multiple range test) indicate significant differences between treatments within the same genotype (for A, C, D) or group of compounds (for B).

Figure 3

UV-B elevates rice resistance to M. separata. (A) Mean (±SE) M. separata masses, 8 days after feeding on control and UV-B-pretreated wild type (WT) and irCOI rice plants. Control and UV-B-pre-exposed WT and irCOI1 rice plants were treated with simulated herbivory (SH+) or left untreated (SH−), and the levels of JA and JA-Ile (B), and TPI activity were analyzed in samples collected at 2 h (for B) or 48 h (for C). For A, n = 30–50; for B–C, n = 6–8. Asterisks (**P < 0.01, Student’s t-test) and different letters (P < 0.05, Duncan’s multiple range test) indicate significant differences between treatments within the same genotype (for A, C) or group of compounds (for B).

Figure 4

UV-B elevates maize resistance to S. litura. (A) Mean masses (±SE) of S. litura insects, 8 days after feeding on control and UV-B-pretreated maize plants. Control and UV-B-pre-exposed maize plants were treated with simulated herbivory (SH+) or left untreated (SH−), and the levels of JA and JA-Ile (B) and accumulation of BXs were analyzed in samples harvested at 2 h (for B) or 48 h (for C). For A, n = 30–50, for B–C, n = 6–8. Asterisks (**P < 0.01, Student’s t-test) represent significant differences between treatments, and different letters (P < 0.05, Duncan’s multiple range test) indicate significant differences between treatments within the same group of compounds.