Ectomycorrhizal Fungi Modulate Biochemical Response against Powdery Mildew Disease in Quercus robur L.

Abstract

In light of climate change, pedunculate oak (Q. robur L.) was marked as the most threatened European tree species. Pedunculate oak is particularly jeopardized by powdery mildew disease caused by Erysiphe alphitoides. We hypothesized that priming of this tree species with ectomycorrhizal fungi could mitigate biotic stress and produce bioprotective properties against the disease. In this study, we have compared oaks’ foliar physiological and biochemical responses upon infection with E. alphitoides in the presence and absence of ectomycorrhizal fungi (ECM). The main aim of this study was to inspect how ECM modulate an oak’s biochemical response to infection with E. alphitoides, particularly at the level of the accumulation of the main polyamines (putrescine, spermidine, and spermine), soluble osmolytes (proline and glycine betaine), and phenolics (total phenolic content, flavonoids, and condensed tannins). A polyamine quantification was performed after derivatization by using high-performance liquid chromatography (HLPC) coupled with fluorescent detection. Oak seedlings inoculated with ECM fungi exhibited significantly higher levels of putrescine, spermine, and proline compared to non-inoculated seedlings, indicating the priming properties of the ECM. E. alphitoides caused an increase in individual and total polyamine content and lipid peroxidation in oak leaves regardless of the effect of ECM, while causing a decrease in physiological and antioxidative parameters and water use efficiency (WUE). Common biochemical parameters may contribute to understanding the underpinning plant defense mechanisms in three-way interactions among plants and pathogenic and ectomycorrhizal fungi and can be used as reliable adaptability descriptors in the context of climate change.

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

“…On the other hand, levels of GB did not change significantly under heat stress in non-mycorrhized oak seedlings, whereas levels of GB dropped dramatically in ectomycorrhizal-fungi-inoculated seedlings. This contrasts with previous findings in which pedunculate oak species subjected to a longer heat shock treatment (5 days) exhibited statistically higher levels of GB [ 23 ], especially since GB is known for its protective and stabilizing effects towards translational and photosynthetic machinery in plants during heat-stress-stimulated photoinhibition [ 78 ]. The ability of GB to up-regulate specific genes during heat stress (around 360 in Arabidopsis) that include various transcription factors, membrane trafficking components, ROS-scavenging enzymes such as lipoxygenase, monodehydroascorbate, or some signal transduction proteins (such as putative receptor kinase, calmodulin, protein kinase, and receptor protein kinase) may also explain why GB-enhanced plants are more heat-stress tolerant [ 79 , 80 ].…”

“…Although putrescine levels increased slightly in both mycorrhized and non-mycorrhized seedlings after heat treatment, mycorrhized oak seedlings had significantly lower levels of putrescine than non-mycorrhized oak seedlings. Similar findings were reported in oak seedlings exposed to mycorrhization and powdery mildew as co-occurring biotic stressors, with putrescine trends and patterns differing from spermine and spermine [ 23 ]. Similarly, the reduction of free putrescine has also been reported in two species of poplar seedlings ( Populus alba Villafranca and Populus nigra Jean Pourtet) as a result of inoculation with the two arbuscular mycorrhiza species Glomus mosseae or G. intraradices , whereas this inoculation in the presence of heavy metal (Zn) pollution as a co-occurring abiotic factor induces an opposite response, namely a significant increase in free putrescine [ 88 ].…”

“…Our findings are in accordance with those of Sarjala et al [ 105 ] who found increased spermidine levels in the roots and stems of Scots pine ( Pinus sylvestris L.) seedlings in the presence of two ectomycorrhizal fungi, Pisolithus tinctorius and Paxillus involutus , with different inoculation characteristics. Similarly, significant spermine and putrescine increments along with a non-significant change in total polyamines were recorded as a consequence of mycorrhization in pedunculate oak inoculated with the same ECTOVIT inoculum containing ectomycorrhizal spores when subjected to biotic stress with powdery mildew [ 23 ].…”

“…On the other hand, the presence of many soilborne beneficial microorganisms of microbial or fungal origin can alleviate abiotic stress factors in plants by boosting innate immunity and activating plant defense mechanisms by molecular and transcriptomic reprograming [ 20 , 21 , 22 ]. Amongst them, mycorrhizal fungi are known to help plants to mitigate different biotic [ 23 ] and abiotic stresses including high temperature [ 24 , 25 ]. Mycorrhizal fungi build reciprocally beneficial (symbiotic) associations with more than 80% of plant species, and these fungi can colonize the host plant’s root tissues either intracellularly as in arbuscular mycorrhiza, which is associated with Glomeromycota , or extracellularly as in ectomycorrhiza, which is associated with Basidiomycota and Ascomycota [ 25 ].…”

“…On the other hand, polyamines are another important group of biomolecules with high antioxidant properties and a high ROS-scavenging capacity [ 33 ] that have also been reported to be increased by the action of mycorrhizal fungi during both biotic [ 23 ] and abiotic stress [ 34 , 35 , 36 ]. Polyamines, as ubiquitous aliphatic polycations, have been shown to play multiple roles in plants, including plant growth regulators, transcription and post-translational process regulators, and signaling molecules [ 37 ] (polyamines are also important markers of abiotic and biotic stress) [ 33 , 36 , 38 ].…”