Metatranscriptomic comparison of endophytic and pathogenic Fusarium–Arabidopsis interactions reveals plant transcriptional plasticity

Authors: GUO, LI - Jiaotong University; YU, HOULIN - University Of Massachusetts, Amherst; WANG, BO - Jiaotong University; VESCIO, KATHERYN - University Of Massachusetts, Amherst; DEIULIO, GREGORY - University Of Massachusetts, Amherst; YANG, HE - University Of Massachusetts, Amherst; BERG, ANDREW - University Of Massachusetts, Amherst; ZHANG, LILI - University Of Massachusetts, Amherst; STEINBERG, CHRISTIAN - University Of Franche-Comte; EDEL-HERMANN, VERONIQUE - Institut National De La Recherche Agronomique (INRA); Kistler, Harold; MA, LI-JUN - University Of Massachusetts, Amherst

Submitted to: Biology of Plant Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2021
Publication Date: 4/15/2021
Citation: Guo, L., Yu, H., Wang, B., Vescio, K., Deiulio, G.A., Yang, H., Berg, A., Zhang, L., Steinberg, C., Edel-Hermann, V., Kistler, H.C., Ma, L. 2021. Metatranscriptomic comparison of endophytic and pathogenic Fusarium–Arabidopsis interactions reveals plant transcriptional plasticity. Biology of Plant Microbe Interactions. https://doi.org/10.1094/MPMI-03-21-0063-R.
DOI: https://doi.org/10.1094/MPMI-03-21-0063-R

Interpretive Summary: Some fungi are destructive to agriculture production because of their ability to cause disease on crop plants. However, other closely related fungi actually may be beneficial because they promote plant vigor or prevent the infection by harmful fungi. This study compares the genomes and plant interactions of two closely related strains of the fungus Fusarium oxysporum, one pathogenic and one non-pathogenic. Upon infection, the non-pathogenic strain of the fungus seemed to moderate the plant immune response and moreover, up regulated genes involved in reduction of nitrogen. This strain also appeared to promote plant growth perhaps by making nitrogen more readily available for the plant to use. Knowledge of the genetic mechanisms underlying increased plant vigor could be useful to design or select for beneficial fungi, perhaps reducing the need for fertilizers and attendant problems with pollution due to nitrogen runoff. We anticipate this information also will be a valuable resource for researchers studying the mechanisms involved in determining pathogenic versus beneficial microbial interactions.

Technical Abstract: Plants are continuously exposed to beneficial and pathogenic microbes. How plants recognize and respond to friends versus foes remains poorly understood. Here, we examined the molecular response of Arabidopsis thaliana plants challenged with an endophyte, Fusarium oxysporum strain Fo47, and a pathogen, F. oxysporum strain Fo5176. These two strains share a core genome of about 46 Mb, in addition to unique accessory genomes of 1,229 and 5,415 genes, respectively. Metatranscriptomic data reveal a shared pattern of expression for most plant genes (~80%) in responding to both fungal inoculums at all time points across the early infection course from 12 to 96 hours post inoculation (HPI). However, the distinct responding genes depict the transcriptional plasticity, as the pathogenic interaction activates plant stress responses and suppresses plant growth/development related functions; while the endophyte attenuates host immunity, but activates plant nitrogen assimilation. The differences in reprogramming of the plant transcriptome are most obvious at the earliest time point samples (12 HPI) and are linked to accessory genes encoded by the two closely related fungal genomes. Collectively, our results indicate that A. thaliana and F. oxysporum display 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.