Transcriptome characterization of the ectomycorrhizal fungus Laccaria bicolor to understand metabolic reprogramming during symbiotic interaction with Populus tremuloides

Ectomycorrhizal (ECM) symbiosis is a mutualistic association between soil fungi and the lateral roots of tree species dominating forest ecosystems. This mutualistic association plays a fundamental role in shaping healthy plant communities by enhancing soil nutrient mobilization and uptake, particularly nitrogen. ECM fungi are the most efficient exploiters in nitrogen (N)-limiting environments and play a critical role in N acquisition by plants. However, very little is known about the regulatory mechanisms employed by ECM fungus to exploit diverse N resources. Our main goal was to understand the regulation of molecular processes in a specific ECM fungus that drive efficient nutrient mobilization and development of symbiosis. A comparative transcriptomics approach was used to understand the development of symbiosis and metabolic reprogramming in the ECM fungus, Laccaria bicolor, an efficient growth-promoting fungus during its interaction with host Populus tremuloides. The global gene expression analysis during different stages of symbiosis development revealed potential genetic determinants and molecular processes that modulate early signaling events along with reorientation of metabolism and morphology in ECM fungi that are required for symbiotic establishment. The transcriptome characterization of Laccaria during functional symbiosis revealed that N was assimilated via a glutamate dehydrogenase (GDH-NADPH) pathway during ECM symbiosis and that glutamate was the primary amino acid transported from the fungal partner to the host. The results also suggested that urea and allantoate may serve as N-rich metabolites that are exchanged during symbiosis. It was demonstrated that general amino acid permeases (GAPs) play an important role in mediating amino acid transport during symbiosis. To understand how an ECM fungus exploits diverse N resources and improves plant nutrition, a Laccaria transcriptome was analyzed on variable N regimens. The glutamine synthetase/glutamate synthase (GS/GOGAT) pathway was the main route of N assimilation under N-limiting conditions. Results demonstrated that Laccaria has regulated the uptake system for oligopeptide transport and endogenous metabolism to utilize peptides as a sole N source. Overall, the results of this study provided a better understanding of molecular mechanisms that drive efficient nutrient assimilation during ectomycorrhizal symbiosis and, hence, give us a better understanding of an essential biological process that controls the health and vigor of forest ecosystems.