Ectomycorrhizal (ECM) fungi, symbiotically associated with woody plants, markedly improve the uptake of mineral nutrients such as potassium (K) and phosphorus (P) by their host trees. Although it is well known that ECM fungi can obtain K and P from soil minerals through biological weathering, the mechanisms regulating this process are still poorly understood at the molecular level. Here, we investigated the transcriptional regulation of the ECM fungus Amanita pantherina in weathering K-containing feldspar and apatite using transcriptome sequencing (RNA-seq) and validated these results for differentially expressed genes using real-time quantitative PCR. The results showed that A. pantherina was able to improve relevant metabolic processes, such as promoting the biosynthesis of unsaturated fatty acids and steroids in the weathering of K-containing feldspar and apatite. The expression of genes encoding ion transporters was markedly enhanced during exposure to solid K-containing feldspar and apatite, and transcripts of the high-affinity K transporter ApHAK1, belonging to the HAK family, were significantly upregulated. The results also demonstrated that there was no upregulation of organic acid biosynthesis, reflecting the weak weathering capacity of the A. pantherina isolate used in this study, especially its inability to utilize P in apatite. Our findings suggest that under natural conditions in forests, some ECM fungi with low weathering potential of their own may instead enhance the uptake of mineral nutrients using their high-affinity ion transporter systems. IMPORTANCE In this study, we revealed the molecular mechanism and possible strategies of A. pantherina with weak weathering potential in the uptake of insoluble mineral nutrients by using transcriptome sequencing (RNA-seq) technology and found that ApHAK1, a K transporter gene of this fungus, plays a very important role in the acquisition of K and P. Ectomycorrhizal (ECM) fungi play critical roles in the uptake of woody plant nutrients in forests that are usually characterized by nutrient limitation and in maintaining the stability of forest ecosystems. However, the regulatory mechanisms of ECM fungi in acquiring nutrients from minerals/rocks are poorly understood. This study investigated the transcriptional regulation of A. pantherina weathering K-containing feldspar and apatite and improves the understanding of fungal-plant interactions in promoting plant nutrition enabling increased productivity in sustainable forestry.

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