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 play 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 supplies nitrogen nutrients and auxin, which are deficient in G. elata, remains poorly understood. In this study, genome-scale analysis of G. elata revealed the loss of genes associated with nitrogen utilization and indole-3-acetic acid (IAA) biosynthesis, which are retained in Mycena. Further analysis of the dynamic transcriptomic interactions between G. elata seeds and Mycena across different symbiotic stages revealed that genes involved in nitrogen- and tryptophan-dependent IAA biosynthesis were significantly upregulated in Mycena during the symbiotic germination of G. elata seeds. Concurrently, G. elata seeds exhibited increased expression of genes involved in the hormone signal transduction pathway and the starch and sucrose metabolism pathway. Functional disruption of nitrite reductase (MyNir, EVM0012344) and amidase (MyAmid, EVM0010270), key enzymes in nitrogen assimilation and IAA biosynthesis in Mycena, significantly impaired the symbiotic germination of G. elata seeds. This disruption interfered with energy supply, caused cellular restructuring, and altered hormonal signaling crosstalk. In conclusion, our findings provide novel insights into the mutualistic symbiotic relationship between Mycena and G. elata. Specifically, the fungus Mycena compensates for the incomplete nitrogen metabolism of its plant partner, G. elata, and supplies IAA, thereby promoting seed germination. These results shed light on plant-fungal symbiotic associations from the perspective of nitrogen utilization.