Fungal symbiont Mycena complements impaired nitrogen utilization in Gastrodia elata and supplies indole-3-acetic acid to facilitate its seed germination

Nitrogen and auxin uptake plays pivotal roles in seed germination and development. Gastrodia elata, a fully mycoheterotrophic plant, depends entirely on its symbiotic association with Mycena for early growth and seed germination. The process by which Mycena enables the supply of nitrogen nutrients and auxin, which are deficient in G. elata, remains poorly understood. In this study, a genome-scale dataset for G. elata revealed the loss of genes associated with nitrogen utilization and indole-3-acetic acid (IAA) biosynthesis, genes which were present in Mycena. Further evaluation of the dynamic transcriptomic interactions between G. elata seeds and Mycena at different symbiotic stages demonstrated that genes involved in nitrogen- and tryptophan-dependent IAA biosynthesis were significantly upregulated in Mycena. Concurrently, G. elata seeds exhibited increased expression of genes involved in the "hormone signal transduction pathway" and "starch and sucrose metabolism pathway." As representative enzymes in nitrogen assimilation and IAA biosynthesis pathways, functional disruption of nitrite reductase (MyNir, EVM0012344) and amidase (MyAmid, EVM0010270) in Mycena significantly impeded the symbiotic germination of G. elata seeds. This disruption interfered with the energy supply and caused cellular restructuring and hormonal signaling crosstalk. In conclusion, our findings provide novel insights into the mutualistic symbiotic relationship between Mycena and G. elata. Specifically, the fungus Mycena compensated for the incomplete nitrogen metabolism of its plant partner, G. elata, promoting seed germination. These results shed light on plant-fungal symbiotic associations from the perspective of nitrogen utilization.