Metatranscriptomic Comparison of Endophytic and Pathogenic Fusarium–Arabidopsis Interactions Reveals Plant Transcriptional Plasticity

Abstract

Plants are continuously exposed to beneficial and pathogenic microbes, but how plants recognize and respond to friends versus foes remains poorly understood. Here, we compared the molecular response of Arabidopsis thaliana independently challenged with a Fusarium oxysporum endophyte Fo47 versus a pathogen Fo5176. These two Fusarium oxysporum strains share a core genome of about 46 Mb, in addition to unique 1,229 and 5,415 accessory genes. Metatranscriptomic data reveal a shared pattern of expression for most plant genes (~80%) in responding to both fungal inoculums at all time points from 12 to 96 h post inoculation (HPI). However, the distinct responding genes depict transcriptional plasticity, as the pathogenic interaction activates plant stress responses and suppresses plant growth/development related functions, while the endophytic interaction attenuates host immunity but activates plant nitrogen assimilation. The differences in reprogramming of the plant transcriptome are most obvious in 12 HPI, the earliest time point sampled and are linked to accessory genes in both fungal genomes. Collectively, our results indicate that the A. thaliana and F. oxysporum interaction displays both transcriptome conservation and plasticity in the early stages of infection, providing insights into the fine-tuning of gene regulation underlying plant differential responses to fungal endophytes and pathogens.

Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

“…Regulation of certain genes located on accessory chromosomes has also been seen to direct plant infection phenotypes in an endophytic versus pathogenic FOSC strain ( Guo et al 2021 ). Accessory chromosomes—chromosomes that are not essential for survival, but potentially confer functional advantages ( Bertazzoni et al 2018 )—are likely another important factor impacting lifestyle in Fusarium .…”

Metabolomic Insights Into Endophyte-Derived Bioactive Compounds

“…With the advent of omics technologies (mainly metagenomics, metatranscriptomics, metaproteomics, and microbial metabolomics) in plant microbiome research, there has been a leap in our understanding of the composition and abundance of plant-associated microbial diversity, and the role of the plant microbiome in affecting host’s responses ( Kaul et al, 2016 ). While metagenomic analyses of plant samples provide a snapshot of the abundance and functional potential of the plant-associated microbiota ( Sessitsch et al, 2012 ; Mishra et al, 2021b ), the metatranscriptomic and metaproteomic approaches reveal the “expressed” (RNA and protein components, respectively) fraction of the microbial genome ( Liao et al, 2019 ; Guo et al, 2021 ). However, since metabolites constitute the last step of gene expression, the high throughput quantitative analysis of metabolites would provide the ultimate and most authentic representation of the physiological state of an organism.…”

Conserved secreted effectors determine endophytic growth and multi-host plant compatibility in a vascular wilt fungus

“…A hallmark of hemibiotrophic pathogens is a switch from biotrophy to necrotrophy coinciding with a major shift in the gene expression pattern (37). In contrast to air-borne plant pathogens, the transcriptional dynamics of hemibiotrophic fungal root infection has not been explored in detail (38). Here we performed RNA sequencing (RNAseq) of tomato roots inoculated with Fol4287 during early stages of biotrophic growth in the root cortex (1, 2 and 3 dpi) as well as during colonization of the root vascular tissue (7 dpi), which marks the transition from biotrophy to necrotrophy.…”