Ectomycorrhizal Fungi Modulate Pedunculate Oak’s Heat Stress Responses through the Alternation of Polyamines, Phenolics, and Osmotica Content

Abstract

The physiological and biochemical responses of pedunculate oaks (Quercus robur L.) to heat stress (HS) and mycorrhization (individually as well in combination) were estimated. One-year-old Q. robur seedlings were grown under controlled conditions in a pot experiment, inoculated with a commercial inoculum of ectomycorrhizal (ECM) fungi, and subjected to 72 h of heat stress (40 °C/30 °C day/night temperature, relative humidity 80%, photoperiod 16/8 h) in a climate chamber, and they were compared with seedlings that were grown at room temperature (RT). An in-depth analysis of certain well-known stress-related metrics such as proline, total phenolics, FRAP, ABTS, non-protein thiols, and lipid peroxidation revealed that mycorrhized oak seedlings were more resistant to heat stress (HS) than non-mycorrhized oaks. Additionally, levels of specific polyamines, total phenolics, flavonoids, and condensed tannins as well as osmotica (proline and glycine betaine) content were measured and compared between four treatments: plants inoculated with ectomycorrhizal fungi exposed to heat stress (ECM-HS) and those grown only at RT (ECM-RT) versus non-mycorrhized controls exposed to heat stress (NM-HS) and those grown only at room temperature (NM-RT). In ectomycorrhiza inoculated oak seedlings, heat stress led to not only a rise in proline, total phenols, FRAP, ABTS, non-protein thiols, and lipid peroxidation but a notable decrease in glycine betaine and flavonoids. Amounts of three main polyamines (putrescine, spermine, and spermidine) were quantified by using high-performance liquid chromatography coupled with fluorescent detection (HPLC/FLD) after derivatization with dansyl-chloride. Heat stress significantly increased putrescine levels in non-mycorrhized oak seedlings but had no effect on spermidine or spermine levels, whereas heat stress significantly increased all inspected polyamine levels in oak seedlings inoculated with ectomycorrhizal inoculum. Spermidine (SPD) and spermine (SPM) contents were significantly higher in ECM-inoculated plants during heat stress (approximately 940 and 630 nmol g−1 DW, respectively), whereas these compounds were present in smaller amounts in non-mycorrhized oak seedlings (between 510 and 550 nmol g−1 DW for Spd and between 350 and 450 nmol g−1 DW for Spm). These findings supported the priming and biofertilizer roles of ectomycorrhizal fungi in the mitigation of heat stress in pedunculate oaks by modification of polyamines, phenolics, and osmotica content.

A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak

“…Polyamines, as ubiquitous low molecular weight polycations with numerous regulative roles in plant cells, play a pivotal role as mediators of abiotic and biotic stress tolerance in plants, as well as conductors of signaling in plant-fungi communication [ 27 , 74 , 75 , 76 ]. The roles and mechanism of polyamines alleviation of drought [ 77 , 78 , 79 ] and heat stress [ 17 ], or a combination of drought and heat stress [ 31 ] has been previously reported. To the best of the author’s knowledge, this is the first study examining the effects of mycorrhization and drought on pedunculate oaks.…”

“…Ectomycorrhizal fungi (ECM) are among the most abundant and important microbes that colonize pedunculate oak, with 23 taxa of ECM detected and molecularly identified on fine roots of the pedunculate oak [ 16 ]. Recently, ectomycorrhizal fungi have been proven to mitigate heat stress in pedunculate oaks [ 17 ], as well as alleviate infection with powdery mildew, a foliar fungal disease caused by Erysiphe alphitoides [(Griffon and Maubl.) U. Braun and S.…”

“…On the other hand, while polyamines are well established as a marker of abiotic and biotic stress in vegetables and crops [ 26 ], data on woody plant species are very scarce [ 17 , 27 ]. Polyamines, as ubiquitous aliphatic polycations that regulate growth, transcription, and post-translational processes in plants, are also important antioxidants with a high ROS-scavenging capacity in both free and conjugated forms [ 28 ].…”

Ecophysiological response of Populus alba L. to multiple stress factors during the revitalisation of coal fly ash lagoons at different stages of weathering

“…By regulating the transfer between soil and roots and between roots and leaves, concentrations of these elements are kept within a normal range in their tissue ( Pandey et al., 2012 ; Mukhopadhyay et al., 2017 ; Kostić et al., 2022b ). Tolerant plant species also respond to abiotic stress by increasing their antioxidant capacity, which helps them to maintain a normal cellular balance between production and binding, degradation, and neutralisation of ROS by enzymatic or non-enzymatic antioxidants (carotenoids and anthocyanins) and secondary metabolites (phenols) ( Cervilla et al., 2012 ; Gajić et al., 2020 ; Kebert et al., 2022 ; Vuksanović et al., 2022 ). Intolerant species exibit decreased antioxidant capacity and fewer mechanisms for detoxification in relation to ROS production, resulting in chain reactions in which free radicals damage important biomolecules, such as chloroplast pigments, lipids, and nucleic acids, oxidatively.…”

Variations in Proline Content, Polyamine Profiles, and Antioxidant Capacities among Different Provenances of European Beech (Fagus sylvatica L.)

“…Due to its antioxidant potential and chaperone and osmoprotective activities, proline is undoubtedly one of the most studied osmolytes related to abiotic stress in plants [22,23]. Increased resistance to various abiotic stressors, including heat [24], drought [25], or a combination of heat and drought [26], or drought and rising CO 2 [27], as well as the presence of heavy metals [28,29] or xenobiotics [30] in various woody plant species, has been linked to increased endogenous proline levels. As a multifunctional amino acid, proline not only helps plants adapt to a variety of biotic and abiotic stressors, but it also functions as a signaling molecule that controls gene expression and plant development, modifies redox balance, and modulates defense against pathogens [23].…”