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Thomma, B. P.

Publications and source records attributed to Thomma, B. P..

5 recordsLinked to original sources

AMAPEC: accurate antimicrobial activity prediction for fungal effector proteins

Evolutionary histories of effector proteins secreted by fungal pathogens to mediate plant colonization remain largely elusive. While most functionally characterized effectors modulate plant immunity, recent discoveries have revealed novel functions in targeting host-associated microbiota. We now developed an Antimicrobial Activity Predictor for Effector Candidates (AMAPEC), and identified a wealth of antimicrobial effectors, including many highly conserved ones -- suggesting ancient evolutionary origins. Surprisingly, several plant immune-modulating effectors display antimicrobial activity. We propose that these evolved from ancestral antimicrobials while retaining their original functions. In addition to roles in suppressing host immunity, they may manipulate plant microbiota to promote colonization. We argue that microbial antagonism is a fundamental fungal effector function and suggest that fungi repurposed ancient antimicrobials to serve multiple roles during host-pathogen co-evolution.

microbiology↗

High quality genome assembly and annotation (v1) of the eukaryotic terrestrial microalga Coccomyxa viridis SAG 216-4

Unicellular green algae of the genus Coccomyxa are recognized for their worldwide distribution and ecological versatility. Most species described to date live in close association with various host species, such as in lichen associations. However, little is known about the molecular mechanisms that drive such symbiotic lifestyles. We generated a high-quality genome assembly for the lichen photobiont Coccomyxa viridis SAG 216-4 (formerly C. mucigena). Using long-read PacBio HiFi and Oxford Nanopore Technologies in combination with chromatin conformation capture (Hi-C) sequencing, we assembled the genome into 21 scaffolds with a total length of 50.9 Mb, an N50 of 2.7 Mb and a BUSCO score of 98.6%. While 19 scaffolds represent full-length nuclear chromosomes, two additional scaffolds represent the mitochondrial and plastid genomes. Transcriptome-guided gene annotation resulted in the identification of 13,557 protein-coding genes, of which 68% have annotated PFAM domains and 962 are predicted to be secreted.

genomics↗

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogen Verticillium dahliae

Transposable elements (TEs) are a major source of genetic and regulatory variation in their host genome and are consequently thought to play important roles in evolution. Many fungal and oomycete plant pathogens have evolved dynamic and TE-rich genomic regions containing genes that are implicated in host colonization. TEs embedded in these regions have typically been thought to accelerate the evolution of these genomic compartments, but little is known about their dynamics in strains that harbor them. Here, we used whole-genome sequencing data of 42 strains of the fungal plant pathogen Verticillium dahliae to systematically identify polymorphic TEs that may be implicated in genomic as well as in gene expression variation. We identified 2,523 TE polymorphisms and characterize a subset of 8% of the TEs as dynamic elements that are evolutionary younger, less methylated, and more highly expressed when compared with the remaining 92% of the TE complement. As expected, the dynamic TEs are enriched in the dynamic genomic regions. Besides, we observed an association of dynamic TEs with pathogenicity-related genes that localize nearby and that display high expression levels. Collectively, our analyses demonstrate that TE dynamics in V. dahliae contributes to genomic variation, correlates with expression of pathogenicity-related genes, and potentially impacts the evolution of dynamic genomic regions. Significance statementTransposable elements (TEs) are ubiquitous components of genomes and are major sources of genetic and regulatory variation. Many plant pathogens have evolved TE-rich genomic regions containing genes with roles in host colonization, and TEs are thought to contribute to accelerated evolution of these dynamic regions. We analyzed the fungal plant pathogen Verticillium dahliae to identify TE variation between strains and to demonstrate that polymorphic TEs have specific characteristic that separates them from the majority of TEs. Polymorphic TEs are enriched in dynamic genomic regions and are associated with structural variants and highly expressed pathogenicity-related genes. Collectively, our results provide evidence for the hypothesis that dynamic TEs contribute to increased genomic diversity, functional variation, and the evolution of dynamic genomic regions.

genomics↗

Chromatin features define adaptive genomic regions in a fungal plant pathogen

Understanding the complex information stored in a genome remains challenging since multiple connected regulatory mechanisms act at various scales to determine function. Increased comprehension of genome function at scales beyond contiguous nucleotides will help understand genetic diseases, the emergence of pathogenesis, and more broadly the genomics of adaptation. Here we report the analysis of DNA methylation, histone modification, and DNA accessibility in the plant pathogenic vascular wilt fungus Verticillium dahliae. Functional analysis details that DNA methylation is restricted to repetitive elements, such as transposable element DNA, but interestingly only some repetitive DNA is methylated. This incomplete DNA methylation is associated with repetitive DNA residing in specific compartments of the genome that were previously defined as Lineage-Specific (LS) regions. These regions are hypervariable between V. dahliae isolates and contain genes that support host colonization and adaptive traits. LS regions are associated with H3 Lys-27 methylated histones (H3K27me3), and repetitive DNA within LS regions are more transcriptionally active and have increased DNA accessibility, representing a hybrid chromatin state when compared to repetitive regions within the core genome. We used machine learning algorithms trained on epigenetic and DNA accessibility data to predict LS regions with high recall, identifying approximately twice as much LS DNA in the V. dahliae genome as previously recognized. Collectively, these results characterize LS regions in an intermediate chromatin state and provide evidence that links chromatin features and genome architecture to adaptive regions within the genome.

genomics↗

Ancient duplication and horizontal transfer of a toxin gene cluster reveals novel mechanisms in the cercosporin biosynthesis pathway

Species in the genus Cercospora cause economically devastating diseases in sugar beet, maize, rice, soy bean and other major food crops. Here we sequenced the genome of the sugar beet pathogen C. beticola and found it encodes 63 putative secondary metabolite gene clusters, including the cercosporin toxin biosynthesis (CTB) cluster. We show that the CTB gene cluster has experienced multiple duplications and horizontal transfers across a spectrum of plant pathogenic fungi, including the wide host range Colletotrichum genus as well as the rice pathogen Magnaporthe oryzae. Although cercosporin biosynthesis has been thought to-date to rely on an eight gene CTB cluster, our phylogenomic analysis revealed gene collinearity adjacent to the established cluster in all CTB cluster-harboring species. We demonstrate that the CTB cluster is larger than previously recognized and includes cercosporin facilitator protein (CFP) previously shown to be involved with cercosporin auto-resistance, and four additional genes required for cercosporin biosynthesis including the final pathway enzymes that install the unusual cercosporin methylenedioxy bridge. Finally, we demonstrate production of cercosporin by Colletotrichum fioriniae, the first known cercosporin producer within this agriculturally important genus. Thus, our results provide new insight into the intricate evolution and biology of a toxin critical to agriculture and broaden the production of cercosporin to another fungal genus containing many plant pathogens of important crops worldwide.\n\nSignificance StatementSpecies in the fungal genus Cercospora cause diseases in many important crops worldwide. Their success as pathogens is largely due to the secretion of cercosporin during infection. We report that the cercosporin toxin biosynthesis (CTB) cluster is ancient and was horizontally transferred to diverse fungal pathogens on an unprecedented scale. Since these analyses revealed genes adjacent to the established CTB cluster, we evaluated their role in C. beticola to show that four are necessary for cercosporin biosynthesis. Finally, we confirmed that the apple pathogen Colletotrichum fioriniae produces cercosporin, the first case outside the family Mycosphaerellaceae. Other Colletotrichum plant pathogens also harbor the CTB cluster, which points to a wider concern that this toxin may play in virulence and human health.

evolutionary biology↗