Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization

ABSTRACT Conidial germination marks the beginning of the fungal life cycle on the host plant, leading to disease or mutually beneficial relationships. Using comparative transcriptomics, we aim to unravel the transcriptional similarities and differences of Fusarium graminearum (plant pathogen), and Metarhizium anisopliae (endophyte), during conidial germination and initial colony establishment, to identify the key traits that support their distinct lifestyles. F. graminearum and M. anisopliae belong in the order, Hypocreales. However, their contrasting roles as pathogen and endophyte provide an excellent model for exploring initial colony establishment on the hosts. Our comparison crosses four stages including fresh conidia, polar growth, hyphal extension, and first hyphal branching (on medium) or appressorium formation (on barley). F. graminearum exhibited a higher number of upregulated genes associated with host interactions, including genes for CAZymes, specialized metabolites, and effectors, particularly during the appressorium stage, reflecting its pathogenic nature. By comparison, analysis of the M. anisopliae transcriptome revealed reduced transcript levels of CAZyme and specialized metabolite genes, reflecting a less aggressive host penetration approach. The candidate genes associated with indole-3-acetic acid synthesis were upregulated during the appressorium stage in M. anisopliae, supporting its endophytic lifestyle, and suggesting that the fungus uses a phytohormone-based strategy to interact with plant hosts. Collectively, our findings provide valuable insights into the gene networks directing conidial germination and initiation of infection in pathogenic versus endophytic fungi, as well as documenting appressorium formation of M. anisopliae for the first time in barley.IMPORTANCEConidial germination is the initial step for fungal colonization in diverse environments. Here, we examine the transcriptional similarities and differences in conidial germination and colony establishment of Fusarium graminearum and Metarhizium anisopliae, two fungal species with distinct lifestyles belonging to the Order Hypocreales. F. graminearum is a plant pathogen and the causal agent of Fusarium head blight on cereal crops, whereas M. anisopliae is an insect pathogen and root endophyte which forms beneficial associations with plants. We compared the transcriptome profiles of these species under two nutrient conditions across four developmental stages of conidial germination. Our study shows that the expression profile of genes encoding carbohydrate-active enzymes, specialized metabolites, and putative effectors varies between F. graminearum and M. anisopliae. The results of this study provide insights into gene networks associated with spore germination stages on the host in a pathogenic vs an endophytic fungus.