Do changes in Lactuca sativa metabolic performance, induced by mycorrhizal symbionts and leaf UV-B irradiation, play a role towards tolerance to a polyphagous insect pest?

Abstract

The increased ultraviolet radiation (UV) due to the altered stratospheric ozone leads to multiple plant physiological and biochemical adaptations, likely affecting their interaction with other organisms, such as pests and pathogens. Arbuscular mycorrhizal fungi (AMF) and UV-B treatment can be used as eco-friendly techniques to protect crops from pests by activating plant mechanisms of resistance. In this study, we investigated plant (Lactuca sativa) response to UV-B exposure and Funneliformis mosseae (IMA1) inoculation as well as the role of a major insect pest, Spodoptera littoralis. Lettuce plants exposed to UV-B were heavier and taller than non-irradiated ones. A considerable enrichment in phenolic, flavonoid, anthocyanin, and carotenoid contents and antioxidant capacity, along with redder and more homogenous leaf color, were also observed in UV-B-treated but not in AMF-inoculated plants. Biometric and biochemical data did not differ between AMF and non-AMF plants. AMF-inoculated plants showed hyphae, arbuscules, vesicles, and spores in their roots. AMF colonization levels were not affected by UV-B irradiation. No changes in S. littoralis-feeding behavior towards treated and untreated plants were observed, suggesting the ability of this generalist herbivore to overcome the plant chemical defenses boosted by UV-B exposure. The results of this multi-factorial study shed light on how polyphagous insect pests can cope with multiple plant physiological and biochemical adaptations following biotic and abiotic preconditioning.

Keywords: Anthropogenic change; Chemical ecology; Feeding behavior; Noctuidae; Plant nutraceutical; Plant–insect tolerance; Priming; Spodoptera littoralis.

Fig. 1

Light photomicrographs of fungal structures formed by Funneliformis mosseae IMA1 on the roots of Lactuca sativa L. (+ M) exposed or not to UV-B light (+ UV-B or − UV-B). a, b. Fungal extraradical and intraradical hyphae and appressoria formed on the root surface (scale bars: a, 30 µm; b, 20 µm); c, d. Arbuscules produced within cortical root cells (scale bar 15 µm)

Fig. 2

Determination of (a) total phenolics; (b) flavonoids; antioxidant capacity measured through (c) ABTS, and (d) FRAP assays; (e) total anthocyanins of mycorrhizal (+ M) or non-mycorrhizal (− M) lettuce plants, UV-B-treated (+ UV-B) or untreated (− UV-B). The two-way ANOVA results are shown in the box below each histogram. n.s., not significant. According to two-way ANOVA, there were no significant interaction effects (n = 3, p > 0.05)

Fig. 3

3D scatter chart setting L*, a*, and b* as coordinates, according to the CIE L*a*b* system. Different symbols refer to individual lettuce plants from the different groups referred to the mycorrhizal (+ M) or non-mycorrhizal (− M) lettuce plants, treated with UV-B radiation (+ UV-B) or not (− UV-B). Lightness (L*), redness (a*), and yellowness (b*) values for each plant are the mean of three independent measurements on three fully expanded leaves

Fig. 4

Boxplot showing the percentage of leaf area (cm²) consumed by larvae of Spodoptera littoralis in differently treated lettuce plants. + M/ + UV-B = lettuce plants exposed to UV-B radiation and inoculated with the arbuscular mycorrhizal symbiont Funneliformis mossae; − M/ + UV-B = UV-B-exposed plants not inoculated with F. mossae; + M/ − UV-B = plants inoculated with F. mosseae and not exposed to UV-B; − M/ − UV-B = untreated lettuce plants, unexposed and not mycorrhizal inoculated (control). Each box plot indicates the median (lower, upper quartile and extreme values, outliers); n.s., not significant (Kruskal–Wallis test, p > 0.05)