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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, which can colonize both plant hosts. We observed that all strains were able to advance from epidermis to endodermis within 3 days postinoculation (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 root 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) compared with 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. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license . 

The Fusarium oxysporum species complex (FOSC) includes both plant and human pathogens that cause devastating plant vascular wilt diseases and threaten public health. Each F. oxysporum genome comprises core chromosomes (CCs) for housekeeping functions and accessory chromosomes (ACs) that contribute to host-specific adaptation. This study inspects global transcription factor profiles (TFomes) and their potential roles in coordinating CC and AC functions to accomplish host-specific interactions. Remarkably, we found a clear positive correlation between the sizes of TFomes and the proteomes of an organism. With the acquisition of ACs, the FOSC TFomes were larger than the other fungal genomes included in this study. Among a total of 48 classified TF families, 14 families involved in transcription/translation regulations and cell cycle controls were highly conserved. Among the 30 FOSC expanded families, Zn2-C6 and Znf_C2H2 were most significantly expanded to 671 and 167 genes per family including well-characterized homologs of Ftf1 (Zn2-C6) and PacC (Znf_C2H2) that are involved in host-specific interactions. Manual curation of characterized TFs increased the TFome repertoires by 3% including a disordered protein Ren1. RNA-Seq revealed a steady pattern of expression for conserved TF families and specific activation for AC TFs. Functional characterization of these TFs could enhance our understanding of transcriptional regulation involved in FOSC cross-kingdom interactions, disentangle species-specific adaptation, and identify targets to combat diverse diseases caused by this group of fungal pathogens. 

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 F. 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 explores 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 F. oxysporum strains share a core genome of about 46 Mb, in addition to 1,229 and 5,415 unique accessory genes. Metatranscriptomic data reveal a shared pattern of expression for most plant genes (about 80%) in responding to both fungal inoculums at all timepoints from 12 to 96 h postinoculation (HPI). However, the distinct responding genes depict transcriptional plasticity, as the pathogenic interaction activates plant stress responses and suppresses functions related to plant growth and development, 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 timepoint 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. [Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license . 

The filamentous fungus Fusarium oxysporum is a soilborne pathogen of many cultivated species and an opportunistic pathogen of humans. F. oxysporum f. sp. matthiolae is one of three formae speciales that are pathogenic to crucifers, including Arabidopsis thaliana, a premier model for plant molecular biology and genetics. Here, we report a genome assembly of F. oxysporum f. sp. matthiolae strain PHW726, generated using a combination of PacBio and Illumina sequencing technologies. The genome assembly presented here should facilitate in-depth investigation of F. oxysporum–Arabidopsis interactions and shed light on the genetics of fungal pathogenesis and plant immunity. 

With growing populations and pressing environmental problems, future economies will be increasingly plant-based. Now is the time to reimagine plant science as a critical component of fundamental science, agriculture, environmental stewardship, energy, technology and healthcare. This effort requires a conceptual and technological framework to identify and map all cell types, and to comprehensively annotate the localization and organization of molecules at cellular and tissue levels. This framework, called the Plant Cell Atlas (PCA), will be critical for understanding and engineering plant development, physiology and environmental responses. A workshop was convened to discuss the purpose and utility of such an initiative, resulting in a roadmap that acknowledges the current knowledge gaps and technical challenges, and underscores how the PCA initiative can help to overcome them.