Symbiotic Fungi of an Ambrosia Beetle Alter the Volatile Bouquet of Cork Oak Seedlings

Abstract

In Portugal, fungal symbionts of the ambrosia beetle Platypus cylindrus affect tree vigor of cork oak (Quercus suber) and are linked with the cork oak decline process. Fungal symbionts play crucial roles in bark and ambrosia beetles life history and recent work indicates complex interactions on the fungal and plant metabolic level. Colonized trees may respond with an array of currently unknown volatile metabolites being indicative of such interactions, acting as infochemicals with their environment. In this study, we examined volatile organic compounds (VOCs) of cork oak seedlings wound-inoculated with strains of three fungal associates of P. cylindrus (Raffaelea montetyi, R. quercina and Ceratocystiopsis sp. nov.) over a 45-day period by means of thermodesorption GC/MS techniques. Fungal strains induced largely quantitative but species-specific changes among the 58 VOCs characterized. Overall, monoterpenes – the major volatiles of cork oak foliage, were significantly reduced, possibly a result of fungal biotransformation. Acetophenone, sulcatone, nonanal – volatiles known for mediating ambrosia beetle behavior, increased in response to fungal inoculation. Qualitative VOC profiles of excised tissue of wood lesions (21 VOCs) and pure fungal cultures (60 VOC) showed little overlap with seedling VOCs, indicating their plant derived but fungal induced origin. This chemoecological study expands on the limited knowledge of VOCs as infochemicals emitted from oak trees threatened by oak decline in relation to beetle-vectored ophiostomatoid fungi. It opens new avenues of research to clarify mutualistic or pathogenic aspects of these complex symbiotic interactions and develop new control strategies for P. cylindrus including its mycobiota.

Bark Beetles Utilize Ophiostomatoid Fungi to Circumvent Host Tree Defenses

“…Therefore, the conversion of monoterpenes to their less toxic oxygenated derivatives by fungal symbionts could reduce the extent of monoterpene toxicity to MPB. Earlier studies reported a similar detoxification mechanism by fungal symbionts of several bark beetle species [ 10 , 44 ]. Auto-oxidation of monoterpenes can also occur as the resin encounter air; however, in this study, we found the concentrations of several oxygenated monoterpenes such as borneol and terpinene-4-ol were multiple folds higher in the fungal treated tissues compared to the control, suggesting the possible role of fungi in the detoxification process.…”

“…Our research objectives are (1) to investigate the host terpene detoxification by MPBs’ fungal symbionts [ 38 , 44 , 45 ]; (2) to determine the benefits of maintaining multiple species of fungal symbionts to MPBs; (3) to test whether MPB elicits behavioral responses to FVOCs produced its fungal symbionts. Here, we inoculated the mature lodgepole pine trees in a forest stand with three fungal species ( G. clavigera, L. longiclavatum, and O. montium ) of MPB.…”

Traveling across Life Sciences with Acetophenone—A Simple Ketone That Has Special Multipurpose Missions

“…It was found recently that strains of fungal associates of P. cylindrus , which is a major cork oak pest in Portugal, induced an increase in volatiles known for mediating ambrosia beetle behavior (mainly acetophenone, sulcatone, and nonanal) in response to fungal inoculation. This may help to elucidate the mutualistic or pathogenic aspects of these complex symbiotic interactions and develop new control strategies for P. cylindrus [ 48 ].…”

Sesquiterpenes of the ectomycorrhizal fungus Pisolithus microcarpus alter root growth and promote host colonization

“…Inoculation of cork oak with Raffaelea montetyi , R. quercina , and Ceratocystiopsis sp. nov., four fungi farmed by ambrosia beetles during their establishment within the host plant, leads to a reduction in the host biosynthesis of monoterpenes, possibly as a means of controlling plant immunity (Nones et al 2022 ). Fungal colonization can also systemically affect terpene synthesis (Sarkar and Sadhukhan 2023 ).…”