Most genomes within the species complex of Fusarium oxysporum are organized into two compartments: the core chromosomes (CCs) and accessory chromosomes (ACs). As opposed to CCs, which are conserved and vertically transmitted to carry out essential housekeeping functions, lineage- or strain-specific ACs are believed to be initially horizontally acquired through unclear mechanisms. These two genomic compartments are different in terms of gene density, the distribution of transposable elements, and epigenetic markers. Although common in eukaryotes, the functional importance of ACs is uniquely emphasized among fungal species, specifically in relationship to fungal pathogenicity and their adaptation to diverse hosts. With a focus on the cross-kingdom fungal pathogen Fusarium oxysporum, this review provides a summary of the differences between CCs and ACs based on current knowledge of gene functions, genome structures and epigenetic signatures, and explore the transcriptional crosstalk between the core and accessory genomes.
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.
Here, we report a chromosome-level genome assembly of Fusarium oxysporum strain Fo47 (12 pseudomolecules; contig N50: 4.52Mb), generated using a combination of PacBio long-read, Illumina paired end and Hi-C sequencing data. Although F. oxysporum causes vascular wilt to over 100 plant species, the strain Fo47 is classified as an endophyte and widely used as a biocontrol agent for plant disease control. The Fo47 genome carries a single accessory chromosome of 4.23 Mb, compared to the reference genome of F. oxysporum f.sp. lycopersici strain Fol4287. The high-quality assembly and annotation of the Fo47 genome will be a valuable resource for studying the mechanisms underlying the endophytic interactions between F. oxysporum and plants, as well as deciphering the genome evolution of the F. oxysporum species complex.
Plant xylem colonization is the hallmark of vascular wilt diseases caused by phytopathogens within the Fusarium oxysporum species complex. Recently, xylem colonization has also been reported among endophytic F. oxysporum strains, resulting in some uncertainty. This study compares xylem colonization processes by pathogenic versus endophytic strains in Arabidopsis thaliana and Solanum lycopersicum using Arabidopsis pathogen Fo5176, tomato pathogen Fol4287, and the endophyte Fo47 that can colonize both plant hosts. We observed that all strains were able to advance from epidermis to endodermis within 3 days post-inoculation (dpi) and reached the root xylem at 4 dpi. However, this shared progression was restricted to lateral roots and the elongation zone of the primary root. Only pathogens reached the xylem above the primary-root maturation zone (PMZ). Related to the distinct colonization patterns, we also observed stronger induction of callose at the PMZ and lignin deposition at primary-lateral roots junctions by the endophyte in both plants. This observation was further supported by stronger induction of Arabidopsis genes involved in callose and lignin biosynthesis during the endophytic colonization (Fo47) comparing to the pathogenic interaction (Fo5176). Moreover, both pathogens encode more plant cell wall degrading enzymes than the endophyte Fo47. Therefore, observed differences in callose and lignin deposition could be the combination of host production and the subsequent fungal degradation. In summary, this study demonstrates spatial differences between endophytic and pathogenic colonization, strongly suggesting that further investigations of molecular arm-races are needed to understand how plants differentiate friend from foe.
DUF828-containing proteins are unique to plants but, aside from FORKED1, their function is unknown. We find that DUF828 proteins act with FORKED1 to establish the reticulate leaf vein pattern.
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