Leaf UV-B Irradiation and Mycorrhizal Symbionts Affect Lettuce VOC Emissions and Defence Mechanisms, but Not Aphid Feeding Preferences

Abstract

Arbuscular mycorrhizal fungi (AMF) and ultraviolet-B radiation (UV-B) play important roles in plant–insect interactions by altering plant physiology and histology. We hypothesized that UV-B-induced oxidative stress was mitigated by AMF symbiosis. In this study, we conducted a multifactorial experiment to explore lettuce plant response to AMF inoculation and UV-B exposure (0.4 W m−2; 16 h d−1; 2 weeks), either together or individually, as well as the interaction with the polyphagous insect pest Myzus persicae (Sulzer). Lettuce plants subjected to UV-B radiation showed an increase in callose and oxidative stress indicators, as well as a decrease in stomatal density. Mycorrhizal colonization cancelled out the effect of UV-B on stomatal density, while the symbiosis was not affected by UV-B treatment. The plant volatile emission was significantly altered by UV-B treatment. Specifically, the non-terpene 1-undecene abundance (+M/+UVB: 48.0 ± 7.78%; −M/+UVB: 56.6 ± 14.90%) was increased, whereas the content of the non-terpene aldehydes decanal (+M/+UVB: 8.50 ± 3.90%; −M/+UVB: 8.0 ± 4.87%) and undecanal (+M/+UVB: 2.1 ± 0.65%; −M/+UVB: 1.20 ± 1.18%) and the sesquiterpene hydrocarbons (+M/+UVB: 18.0 ± 9.62 %; −M/+UVB: 19.2 ± 5.90%) was decreased. Mycorrhization, on the other hand, had no significant effect on the plant volatilome, regardless of UV-B treatment. Aphid population was unaffected by any of the treatments, implying a neutral plant response. Overall, this study provides new insights about the interactions among plants, UV-B, and AMF, outlining their limited impact on a polyphagous insect pest.

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?

“…Other studies reported the marginal effect of UV-B treatment on different Spodoptera species (Lindroth et al 2000 ; Wargent and Jordan 2013 ). Our findings support the hypothesis that generalist herbivores, such as lepidopteran caterpillars or polyphagous aphids [e.g., Myzus persicae (Sulzer)] (Zeni et al 2023 ), have evolved the ability to withstand the chemical defense mechanisms of a wide range of plant species. However, it is important to consider that higher UV-B doses than the one used in this work could further enhance the biochemical defenses in terms of phenolic accumulation, without impairing plant growth and development.…”

“…Overall, UV-B irradiation priming over AMF inoculation of the most suitable plant genotype may represent a promising approach to increase the nutraceutical and commercial quality of lettuce plants. The enhanced chemical defenses of plants did not impact the feeding behavior of S. littoralis larvae, probably due to (i) the generalist feeding traits of such herbivores, (ii) the mild UV-B treatments, and (iii) the limited time for the induction of mycorrhizal effects on plant secondary metabolism (see also Zeni et al 2023 ). Therefore, further investigations are needed to assess whether different doses of UV-B/AMF and exposure durations (smaller or greater) that increase plant antioxidant defenses within a hormetic framework may alter the feeding behavior of oligophagous insect pests.…”

“…These indicate the hormetic-biphasic property of radiation and numerous chemical agents, with this dose-dependency explaining the contradictory findings between studies (Christou et al 2022 ; Volkova et al 2022 ). Recently, UV-B-induced oxidative stress was studied through histochemical detection of hydrogen peroxide and lipid peroxidation, as well as defense-related callose deposition in lettuce plants (Zeni et al 2023 ); the authors also showed that the UV-B-induced stress was partially mitigated by the presence of AMF. Herein, the UV-B-triggered increase in the content of total phenolics, flavonoids, anthocyanins, as well as the higher antioxidant capacity, is in accordance with the results reported by Aksakal et al ( 2017 ) and Esringu et al ( 2016 ), who found that a 12- and 18-h UV-B irradiation (3.3 W m −2 ) effectively enhanced the contents of total phenolics and the antioxidant activity in lettuce seedlings, respectively.…”

“…Insect-plant interactions result in a wide range of outcomes depending on a variety of both abiotic and biotic factors. For instance, both UV-B treatment and AMF inoculation have been observed to stimulate plant defense mechanisms by impacting plant physiology and biochemistry (Qi et al 2018 ; Zeni et al 2023 ). All these changes can affect the following trophic levels, such as the interaction between treated plants and herbivore insects (Gange 2007 ; Qi et al 2018 ).…”

“…Previous research has shown that both plant UV-B light exposure and mycorrhizal symbiosis can influence the arthropod feeding activity (Barber et al 2013 ; Qi et al 2018 ). However, little has been done to shed light on the potential effects of the interaction between UV-B radiation and AMF colonization of horticultural crops and their key arthropod pests (Zeni et al 2023 ). In this framework, one may question whether UV radiation exposure and mycorrhizal symbionts can boost plant tolerance to polyphagous insect pests attacking horticultural crops.…”