Background Pinus massoniana Lamb. is an important afforestation tree species with high economic, ecological and medicinal values. Aluminum (Al) toxicity driven by soil acidification causes dieback of P. massoniana plantations. Previous studies showed that ectomycorrhizal fungi alleviate Al stress damages in Pinus, but the underlying molecular mechanisms and key genes induced by ectomycorrhizal fungi inoculation under Al stress in Pinus have not been explored. Herein, we applied Al stress for 60 days to P. massoniana seedlings inoculated with Suillus luteus (SL) and those non-inoculated. Then, we compared their growth parameters and transcriptome in order to detect candidate genes induced by SL conferring Al tolerance in P. massoniana. Result Our results showed that SL inoculation confers Al stress tolerance in P. massoniana through improved growth performance, strong antioxidant enzyme activities and reduced malondialdehyde accumulation as compared to non-inoculated seedlings. Transcriptome sequencing further supported these findings as very few genes (51 genes) were transcriptionally altered by Al in SL inoculated plants as compared to non-inoculated plants (2140 genes). We identified three core genes (cox1, cox3 and Nd1) that were strongly up-regulated by Al in the SL inoculated plants but were down-regulated in the non-inoculated plants. We also identified 42 genes specifically regulated by SL inoculated plants under Al stress, which are involved in a wide range of biological processes such as antioxidative response, transporters, hormone signaling and plant pathogen infection responses. Conclusions Altogether, our data suggest that SL inoculation induces priming of key stress response pathways and triggers specific genes that efficiently alleviate Al stress effects in P. massoniana. The candidate genes resources generated in this study are of utmost importance for functional characterization and molecular studies aiming at improving Al tolerance in plants.

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Global warming significantly impacts forest range areas by increasing soil acidification or aluminum toxicity. Aluminum (Al) toxicity retards plant growth by inhibiting the root development process, hindering water uptake, and limiting the bioavailability of other essential micronutrients. Pinus massoniana (masson pine), globally recognized as a reforestation plant, is resistant to stress conditions including biotic and abiotic stresses. This resistance is linked to the symbiotic relationship with diverse ectomycorrhizal fungal species. In the present study, we investigated the genetic regulators as expressed proteins, conferring a symbiotic relationship between Al-stress resistance and Suillus luteus in masson pine. Multi-treatment trials resulted in the identification of 12 core Al-stress responsive proteins conserved between Al stress conditions with or without S. luteus inoculation. These proteins are involved in chaperonin CPN60-2, protein refolding and ATP-binding, Cu-Zn-superoxide dismutase precursor, oxidation-reduction process, and metal ion binding, phosphoglycerate kinase 1, glycolytic process, and metabolic process. Furthermore, 198 Al responsive proteins were identified specifically under S. luteus-inoculation and are involved in gene regulation, metabolic process, oxidation-reduction process, hydrolase activity, and peptide activity. Chlorophyll a-b binding protein, endoglucanase, putative spermidine synthase, NADH dehydrogenase, and glutathione-S-transferase were found with a significant positive expression under a combined Al and S. luteus treatment, further supported by the up-regulation of their corresponding genes. This study provides a theoretical foundation for exploiting the regulatory role of ectomycorrhizal inoculation and associated genetic changes in resistance against Al stress in masson pine.