Unveiling Transcriptional Dynamics Across Five Developmental Stages of the Edible Mushroom Oudemansiella raphanipes

TL;DR

This study maps the genetic activity of the edible mushroom Oudemansiella raphanipes across five developmental stages, linking its unique nutritional profile to specific molecular processes.

Contribution

The first comprehensive transcriptomic atlas of O. raphanipes development and its connection to nutritional traits.

Findings

Transcriptional reprogramming is most dramatic during the spore-to-mycelium transition with 19,827 differentially expressed genes.

Stage-specific pathways like glycerophospholipid metabolism and starch/sucrose metabolism are linked to developmental processes.

Sustained transcriptional programs in mature fruiting bodies correlate with high protein and low fat nutritional traits.

Abstract

Oudemansiella raphanipes is a prized edible mushroom renowned for its “three-high, one-low” nutritional profile (high protein, fiber, vitamins; low fat). However, the stage-specific molecular dynamics governing its development and their potential link to its superior nutrition remain unknown, hindering targeted genetic improvement. This study aimed to decipher the first comprehensive transcriptomic atlas across its five key developmental stages and to explore potential molecular signatures linked to its distinctive nutrition. We first confirmed the superior nutritional profile of O. raphanipes via comparative analysis with nine commercial mushrooms. RNA sequencing (RNA-seq) was performed on samples from five defined developmental stages (spores, mycelia, primordia, closed-cap and open-cap fruiting bodies), followed by de novo transcriptome assembly, functional annotation, and differential expression analysis. Results revealed extensive transcriptional reprogramming, with the most dramatic changes occurring at the spore-to-mycelium transition (19,827 differentially expressed genes). Stage-specific pathway enrichment highlighted regulators of germination (e.g., ribosome, transmembrane transport), primordium formation (e.g., glycerophospholipid metabolism, GTPase signaling), fruiting body development (e.g., starch/sucrose metabolism, terpenoid synthesis), and maturation (e.g., glycolysis, fatty acid biosynthesis, transcription factors MADS-box/bZIP). We identified 588 stage-exclusive genes in spores and 515 constitutively upregulated genes linked to energy metabolism and proteostasis. Crucially, integrating nutritional phenotypes with stage-resolved transcriptomics revealed that sustained transcriptional programs in mature fruiting bodies are associated with its nutritional excellence; e.g., upregulation of ribosomal/amino acid metabolic pathways aligns with high protein content, while active fatty acid degradation correlates with low fat levels. Our study provides the first multi-stage transcriptomic blueprint for O. raphanipes development, revealing stage-specific regulators and proposing molecular associations for its nutritional traits. This resource offers a foundational basis and candidate genetic targets for future breeding strategies aimed at enhancing agronomic and nutritional traits in this prized fungus.

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