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 M...

Full description

Saved in:
Bibliographic Details
Main Authors: Soumya Moonjely, Frances Trail
Format: Article
Language:English
Published: American Society for Microbiology 2025-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00226-25
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849340158087790592
author Soumya Moonjely
Frances Trail
author_facet Soumya Moonjely
Frances Trail
author_sort Soumya Moonjely
collection DOAJ
description 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.
format Article
id doaj-art-4690d50f3d3843eeba475a9490ff8237
institution Kabale University
issn 2165-0497
language English
publishDate 2025-08-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj-art-4690d50f3d3843eeba475a9490ff82372025-08-20T03:43:58ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-08-0113810.1128/spectrum.00226-25Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonizationSoumya Moonjely0Frances Trail1Department of Plant Biology, Michigan State University, East Lansing, Michigan, USADepartment of Plant Biology, Michigan State University, East Lansing, Michigan, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/spectrum.00226-25Fusarium graminearumMetarhizium anisopliaeconidial germinationRNA sequencingplant host colonizationCAZymes
spellingShingle Soumya Moonjely
Frances Trail
Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
Microbiology Spectrum
Fusarium graminearum
Metarhizium anisopliae
conidial germination
RNA sequencing
plant host colonization
CAZymes
title Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
title_full Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
title_fullStr Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
title_full_unstemmed Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
title_short Comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
title_sort comparative transcriptomics reveal contrasting strategies between a fungal plant pathogen and an endophyte during initial host colonization
topic Fusarium graminearum
Metarhizium anisopliae
conidial germination
RNA sequencing
plant host colonization
CAZymes
url https://journals.asm.org/doi/10.1128/spectrum.00226-25
work_keys_str_mv AT soumyamoonjely comparativetranscriptomicsrevealcontrastingstrategiesbetweenafungalplantpathogenandanendophyteduringinitialhostcolonization
AT francestrail comparativetranscriptomicsrevealcontrastingstrategiesbetweenafungalplantpathogenandanendophyteduringinitialhostcolonization