Biology subjects

Sukno, S. A.

Publications and source records attributed to Sukno, S. A..

6 recordsLinked to original sources

bioRxiv2026

Genome-wide structural variants uncover strain-specific genes and evolutionary genomic determinants of a fungal maize pathogen

Genomic structural variants (SVs) are important sources of genetic diversity and contribute to the adaptation and evolution of plant-pathogenic fungi. Colletotrichum graminicola, the causal agent of maize (Zea mays L.) anthracnose, causes significant yield losses and serves as an important model for genetic studies. To investigate genomic plasticity in this pathogen, long-read genome assemblies were generated for four C. graminicola field strains collected in France, Croatia, Brazil, and Argentina and compared with the chromosome-level reference genome from the USA. Comparative analyses revealed extensive structural variation across core chromosomes, including large-scale translocations, inversions, duplications, and insertions and deletions, whereas minichromosomes showed markedly reduced collinearity among strains. Secreted proteins and predicted effectors were located significantly closer to regions affected by SVs. Approximately 174 kb of segmental duplications lacking genes were shared between core chromosome 04 and minichromosomes 11 and 13 in the reference genome but were absent from the other field strains, revealing a strain-specific structural link between core and minichromosomes. Protein clustering identified 733 candidate strain-specific genes across the reference genome. Approximately 72% of the genes annotated on the minichromosomes were strain-specific, indicating that most of their annotated genes lacked orthologous gene models in the other strains. Of the 733 candidate strain-specific genes, 492 retained homologous genomic sequences in at least one other strain and many also showed evidence of gene disruption. This pattern is consistent with lineage-specific pseudogenization and suggests that apparent gene presence-absence variation may arise through several evolutionary processes, including gene gain, gene loss and loss of gene function. Insertions and deletions in potentially regulatory flanking regions were associated with plant-pathogen interaction genes. In addition, interpretable machine learning analyses revealed a co-occurrence of duplications and LTR retrotransposons in genomic regions associated with secreted genes. This study shows that structural variation, transposable elements, and lineage-specific pseudogenization are important features of genome evolution in C. graminicola and identifies associations between genomic variation and genes involved in plant-pathogen interactions.

genomics↗

bioRxiv2026

Adaptive genomic compartments shaped by giant mobile elements underpin the ancient emergence of fungal pathogenicity

The emergence of new fungal pathogens often depends on the acquisition of complex adaptive traits, yet the mechanisms by which such traits arise remain poorly understood. Here we show that a biosynthetic gene cluster required for pathogenicity in the lupin pathogenic fungus Colletotrichum lupini was acquired within a genomic region derived from a giant Starship transposable element. Comparative and population genomic analyses reveal that the C. lupini genome contains multiple regions derived from ancestrally active Starship elements, enriched in lineage-specific genes and strongly induced during plant infection. One such region harbours a hybrid polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS) gene cluster that is conserved in pathogenic isolates but absent from closely related non-pathogenic species and from a non-pathogenic strain. Phylogenetic analyses of the PKS-NRPS backbone gene reveal incongruence with species relationships and a distribution across deeply divergent fungal lineages, consistent with horizontal acquisition. Disruption of the PKS-NRPS backbone gene abolishes pathogenicity, demonstrating that this cluster is required for host infection. Phylogenomic analyses further indicate that lupin pathogenicity emerged once within the C. lupini lineage prior to its diversification. Together, these findings identify a Starship-associated virulence determinant and support a model in which giant cargo-mobilizing mobile elements generate genomic novelty by facilitating the acquisition, assembly and integration of adaptive traits during the emergence of fungal pathogenicity.

genetics↗

bioRxiv2025

Gene duplication drove functional divergence of two effectors in the maize anthracnose pathogen

Colletotrichum species rank among the most important fungal pathogens, threatening food security by infecting nearly all major crops worldwide. Colletotrichum graminicola, the causal agent of maize anthracnose, secretes effector proteins to manipulate host defences and promote colonization. Building on previous work characterizing the nuclear effector CgEP1, we characterized its paralog CgEP4, which is highly conserved across strains of C. graminicola. Phylogenetic analysis of the two genes and their homologs in other species revealed that they originated from a gene duplication event approximately 28 to 18 million years ago, predating the diversification of the Graminicola species complex. This timing aligns with the ecological expansion of C4 grasses, suggesting that the functional divergence of these effectors was an adaptive response to facilitate the colonization of emerging monocot hosts. Functional characterization using gene deletion mutants demonstrated that CgEP4 has a critical role in pathogenicity, characterized by a significant reduction in virulence, delayed penetration, enhanced papilla formation, and decreased fungal biomass. This virulence defect is associated with compromised host colonization and a failure to suppress basal host defences. In the absence of CgEP4, the pathogen also showed defects in general fungal physiology and stress tolerance. Overall, our findings establish CgEP4 as a new, essential nuclear-localized effector that promotes fungal entry and colonization by manipulating host responses. Our findings demonstrate that evolutionary analysis is a valuable tool for discovering new genes important for host adaptation and pathogen evolution.

plant biology↗

bioRxiv2024

Long-distance gene flow and recombination shape the evolutionary history of a maize pathogen

The evolutionary history of crop pathogens is shaped by a complex interaction of natural and anthropogenic factors. The ascomycete fungus Colletotrichum graminicola causes maize anthracnose. The disease can result in significant yield losses and is also an important model for genetic studies. We conducted a comprehensive investigation into the evolutionary genomics of C. graminicola using a collection of 212 isolates from 17 countries. Genomic analyses supported the existence of three geographically isolated genetic lineages, with a significant pattern of isolation by distance. We identified two distinct gene flow patterns, driven by short and long-distance dispersion, likely resulting from the natural spread of the pathogen and the exchange of contaminated seeds. We present evidence of genetic introgression between lineages, suggesting a long history of recombination. We identified significant recombination events coalescing at distinct points in time, with the North American lineage displaying evidence of most ancient recombination. Demographic modeling indicated that North America is an intermediate between Brazil, Europe and an ancestral, unsampled source population, hypothesized to be Mesoamerican. Our analyses revealed that the global genomic structure of C. graminicola is shaped by geographic differentiation driven by long-distance migration and a long history of recombination and introgression. We show historical relationships among these lineages, identifying a potential route for fungal spread, with the North American population emerging ancestrally, followed sequentially by the Brazilian and European populations. Our research indicates that the European lineage is more virulent, which has implications for the potential emergence of new outbreaks of maize anthracnose in Europe.

genomics↗

bioRxiv2022

Genome evolution and transcriptome plasticity associated with adaptation to monocot and eudicot plants in Colletotrichum fungi

Colletotrichum fungi infect a wide diversity of monocot and eudicot hosts, causing plant diseases on almost all economically important crops worldwide. In addition to its economic impact, Colletotrichum is a suitable model for the study of gene family evolution on a fine scale to uncover events in the genome that are associated with the evolution of biological characters important for host interactions. Here we present the genome sequences of 30 Colletotrichum species, 18 of them newly sequenced, covering the taxonomic diversity within the genus. A time-calibrated tree revealed that the Colletotrichum ancestor diverged in the late Cretaceous around 70 million years ago (mya) in parallel with the diversification of flowering plants. We provide evidence of independent host jumps from eudicots to monocots during the evolution of this pathogen, coinciding with a progressive shrinking of the degradative arsenal and expansions in lineage specific genes. Comparative transcriptomics of four reference species with different evolutionary histories and adapted to different hosts revealed similarity in gene content but differences in the modulation of their transcription profiles. Only a few orthologs show similar expression profiles on different plant cell walls. Combining genome sequences and expression profiles we identified a set of core genes, such as specific transcription factors, involved in plant cell wall degradation in Colletotrichum.Together, these results indicate that the ancestral Colletotrichum were associated with eudicot plants and certain branches progressively adapted to different monocot hosts, reshaping part of the degradative and transcriptional arsenal.

microbiology↗

bioRxiv2022

Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose

BackgroundColletotrichum graminicola, the causal agent of maize anthracnose, is an important crop disease worldwide. Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. The genus Colletotrichum is largely recognized as asexual, but several species have been reported to have a sexual cycle. Here, we employed a population genomics approach to investigate the genetic diversity and reproductive biology of C. graminicola isolates infecting maize. We sequenced 108 isolates of C. graminicola collected in 14 countries using restriction site-associated DNA sequencing (RAD-Seq) and whole-genome sequencing (WGS). ResultsClustering analyses based on single-nucleotide polymorphisms showed populational differentiation at a global scale, with three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen, and geographic subdivision. Distinct levels of genetic diversity were observed between these clades, suggesting different evolutionary histories. Intra and inter-continental migration was predicted between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality and evidence of genetic recombination were detected from the analysis of linkage disequilibrium and the pairwise homoplasy index (PHI) test for clonality. We show evidence that even if rare (possibly due to losses of sex and meiosis-associated genes) C. graminicola can undergo sexual recombination based on lab assays and genomic analyses. ConclusionsOur results support hypotheses of intra and intercontinental pathogen migration and genetic recombination with great impact on C. graminicola population structure.

genomics↗