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Kema, G.

Publications and source records attributed to Kema, G..

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Frequent genetic exchange shapes the pan-mitogenome of the fungal plant pathogen Fusarium oxysporum

Mitochondria are present in almost all eukaryotic lineages. The mitochondrial genomes (mitogenomes) evolve separately from nuclear genomes, and they can therefore provide relevant insights into the evolution of their host species. Fusarium oxysporum is a major fungal plant pathogen that is assumed to reproduce clonally. However, horizontal chromosome transfer between strains can occur through heterokaryon formation, and recently signs of sexual recombination have been observed. Similarly, signs of recombination in F. oxysporum mitogenomes challenged the prevailing assumption of clonal reproduction in this species. Here, we construct, to our knowledge, the first fungal pan-mitogenome graph of nearly 500 F. oxysporum mitogenome assemblies to uncover the variation and evolution. In general, the gene order of fungal mitogenomes is not well conserved, yet the mitogenome of F. oxysporum and related species are highly co-linear. We observed two strikingly contrasting regions in the Fusarium oxysporum pan-mitogenome, comprising a highly conserved core mitogenome and a long variable region (6-16 kb in size), of which we identified three distinct types. The pan-mitogenome graph reveals that only five intron insertions occurred in the core mitogenome and that the long variable regions drive the difference between mitogenomes. Moreover, we observed that their evolution is neither concurrent with the core mitogenome nor with the nuclear genome. Our large-scale analysis of long variable regions uncovers frequent recombination between mitogenomes, even between strains that belong to different taxonomic clades. This challenges the common assumption of incompatibility between genetically diverse F. oxysporum strains and provides new insights into the evolution of this fungal species. Importance statementInsights into plant pathogen evolution is essential for the understanding and management of disease. Fusarium oxysporum is a major fungal pathogen that can infect many economically important crops. Pathogenicity can be transferred between strains by the horizontal transfer of pathogenicity chromosomes. The fungus has been thought to evolve clonally, yet recent evidence suggests active sexual recombination between related isolates, which could at least partially explain the horizontal transfer of pathogenicity chromosomes. By constructing a pan-genome graph of nearly 500 mitochondrial genomes, we describe the genetic variation of mitochondria in unprecedented detail and demonstrate frequent mitochondrial recombination. Importantly, recombination can occur between genetically diverse isolates from distinct taxonomic clades and thus can shed light on genetic exchange between fungal strains.

genomics↗

A chromosome-level genome assembly of Zasmidium syzygii isolated from banana leaves

Accurate taxonomic classification of samples from infected host material is essential for disease diagnostics and genome analyses. Despite the importance, diagnosis of fungal pathogens causing banana leaf diseases remains challenging. Foliar diseases of bananas are mainly caused by three Pseudocercospora species, of which the most predominant causal agent is P. fijiensis. Here, we sequenced and assembled four fungal isolates obtained from necrotic banana leaves in Bohol (Philippines) and obtained a high-quality genome assembly for one of these isolates. The samples were initially identified as P. fijiensis using PCR diagnostics, however, the assembly size was consistently 30 Mb smaller than expected. Based on the ITS sequences, we identified the samples as Zasmidium syzygii (98.7% identity). The high-quality Zasmidium syzygii assembly is 42.5 Mb in size, comprising 16 contigs, of which 11 are complete. The genome contains 98.6% of the expected single-copy BUSCO genes and contains 14,789 genes and 10.3% repeats. The three short-read assemblies are less continuous but have similar genome sizes (40.4 - 42.4 Mb) and contain between 96.5% and 98.4% BUSCO genes. All four isolates have identical ITS sequences and are distinct from Zasmidium isolates that were previously sampled from banana leaves. We thus report the first continuous genome assembly of a member of the Zasmidium genus, forming an essential resource for further analysis to enhance our understanding of the diversity of pathogenic fungal isolates as well as fungal diversity.

microbiology↗

Segmental Duplications Drive the Evolution of Accessory Regions in a Major Crop Pathogen

O_LIMany pathogens evolved compartmentalized genomes with conserved core and variable accessory regions which carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such accessory regions often spanning entire chromosomes. The presence of specific accessory regions influences the host range, and horizontal transfer of some accessory regions can modify the pathogenicity of the receiving strain. However, understanding how these accessory regions evolve in strains that infect the same host remains limited. C_LIO_LIHere, we define the pan-genome of 69 diverse Fusarium strains that cause Fusarium wilt of banana, a significant constraint to global banana production. In this diverse panel of Fusarium strains infecting banana, we analyzed the diversity and evolution of the accessory regions. C_LIO_LIAccessory regions in Fusarium strains infecting the same banana cultivar are highly diverse, and we could not identify any shared genomic regions and in planta induced effectors. We demonstrate that segmental duplications drive the evolution of accessory regions. Furthermore, we show that recent segmental duplications and aneuploidy occur specifically in accessory chromosomes and cause the expansion of accessory regions in F. oxysporum. C_LIO_LITaken together we conclude that extensive recent duplications drive the evolution of accessory regions in Fusarium, which contribute to the evolution of virulence. C_LI

genomics↗

Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus

Meiosis is a key cellular process of sexual reproduction involving the pairing of homologous sequences. In many species however, meiosis can also involve the segregation of supernumerary chromosomes, which can lack a homolog. How these unpaired chromosomes undergo meiosis is largely unknown. In this study we investigated chromosome segregation during meiosis in the haploid fungus Zymoseptoria tritici that possesses a large complement of supernumerary chromosomes. We used isogenic whole chromosome deletion strains to compare meiotic transmission of chromosomes when paired and unpaired. Unpaired chromosomes inherited from the male parent as well as paired supernumerary chromosomes showed Mendelian inheritance. In contrast, unpaired chromosomes inherited from the female parent showed non-Mendelian inheritance but were amplified and transmitted to all meiotic products. We concluded that the supernumerary chromosomes of Z. tritici show a meiotic drive and propose an additional feedback mechanism during meiosis which initiates amplification of unpaired female-inherited chromosomes.

molecular biology↗

Plasticity of the MFS1 promoter leads to multi drug resistance in the wheat pathogen Zymoseptoria tritici

The ascomycete Zymoseptoria tritici is the causal agent of septoria leaf blotch on wheat. Disease control relies mainly on resistant wheat cultivars and on fungicide applications. The fungus displays a high potential to circumvent both methods. Resistance against all unisite fungicides has been observed over decades. A different type of resistance has emerged among wild populations with multi-drug resistant (MDR) strains. Active fungicide efflux through overexpression of the major-facilitator gene, MFS1, explains this emerging resistance mechanism. In this study, we identified as responsible mutations three types of inserts in the MFS1 promoter, two of which harboring potential transcription factor binding sites. We show, that type I insertion leads to MFS1 overexpression and consequently to MDR. Interestingly, all three inserts correspond to repeated elements of the Z. tritici genome.\n\nThese results underline the plasticity of repeated elements leading to fungicide resistance in Z. tritici and which contribute to its adaptive potential.

microbiology↗