scholarly journals Complex evolutionary origins of specialized metabolite gene cluster diversity among the plant pathogenic fungi of theFusarium graminearumspecies complex

2019 ◽  
Author(s):  
Sabina Moser Tralamazza ◽  
Liliana Oliveira Rocha ◽  
Ursula Oggenfuss ◽  
Benedito Corrêa ◽  
Daniel Croll
Keyword(s):  
Gene Cluster ◽  
Plant Pathogens ◽  
De Novo ◽  
Chromosomal Rearrangements ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Death Process ◽  
Head Blight ◽  
Fungal Genomes ◽  
Gain Loss

AbstractFungal genomes encode highly organized gene clusters that underlie the production of specialized (or secondary) metabolites. Gene clusters encode key functions to exploit plant hosts or environmental niches. Promiscuous exchange among species and frequent reconfigurations make gene clusters some of the most dynamic elements of fungal genomes. Despite evidence for high diversity in gene cluster content among closely related strains, the microevolutionary processes driving gene cluster gain, loss and neofunctionalization are largely unknown. We analyzed theFusarium graminearumspecies complex (FGSC) composed of plant pathogens producing potent mycotoxins and causing Fusarium head blight on cereals. Wede novoassembled genomes of previously uncharacterized FGSC members (two strains ofF. austroamericanum,F. cortaderiaeandF. meridionale). Our analyses of eight species of the FGSC in addition to 15 otherFusariumspecies identified a pangenome of 54 gene clusters within FGSC. We found that multiple independent losses were a key factor generating extant cluster diversity within the FGSC and theFusariumgenus. We identified a modular gene cluster conserved among distantly related fungi, which was likely reconfigured to encode different functions. We also found strong evidence that a rare cluster in FGSC was gained through an ancient horizontal transfer between bacteria and fungi. Chromosomal rearrangements underlying cluster loss were often complex and were likely facilitated by an enrichment in specific transposable elements. Our findings identify important transitory stages in the birth and death process of specialized metabolism gene clusters among very closely related species.

scholarly journals Complex Evolutionary Origins of Specialized Metabolite Gene Cluster Diversity among the Plant Pathogenic Fungi of the Fusarium graminearum Species Complex

2019 ◽  
Vol 11 (11) ◽  
pp. 3106-3122
Author(s):  
Sabina Moser Tralamazza ◽  
Liliana Oliveira Rocha ◽  
Ursula Oggenfuss ◽  
Benedito Corrêa ◽  
Daniel Croll
Keyword(s):  
Gene Cluster ◽  
Fusarium Graminearum ◽  
Species Complex ◽  
Plant Pathogens ◽  
De Novo ◽  
Fusarium Species ◽  
Gene Clusters ◽  
Death Process ◽  
Fusarium Graminearum Species Complex ◽  
Fungal Genomes

Abstract Fungal genomes encode highly organized gene clusters that underlie the production of specialized (or secondary) metabolites. Gene clusters encode key functions to exploit plant hosts or environmental niches. Promiscuous exchange among species and frequent reconfigurations make gene clusters some of the most dynamic elements of fungal genomes. Despite evidence for high diversity in gene cluster content among closely related strains, the microevolutionary processes driving gene cluster gain, loss, and neofunctionalization are largely unknown. We analyzed the Fusarium graminearum species complex (FGSC) composed of plant pathogens producing potent mycotoxins and causing Fusarium head blight on cereals. We de novo assembled genomes of previously uncharacterized FGSC members (two strains of F. austroamericanum, F. cortaderiae, and F. meridionale). Our analyses of 8 species of the FGSC in addition to 15 other Fusarium species identified a pangenome of 54 gene clusters within FGSC. We found that multiple independent losses were a key factor generating extant cluster diversity within the FGSC and the Fusarium genus. We identified a modular gene cluster conserved among distantly related fungi, which was likely reconfigured to encode different functions. We also found strong evidence that a rare cluster in FGSC was gained through an ancient horizontal transfer between bacteria and fungi. Chromosomal rearrangements underlying cluster loss were often complex and were likely facilitated by an enrichment in specific transposable elements. Our findings identify important transitory stages in the birth and death process of specialized metabolism gene clusters among very closely related species.

scholarly journals Conservation of a gene cluster reveals novel cercosporin biosynthetic mechanisms and extends production to the genus Colletotrichum

2017 ◽  
Author(s):  
Ronnie de Jonge ◽  
Malaika K. Ebert ◽  
Callie R. Huitt-Roehl ◽  
Paramita Pal ◽  
Jeffrey C. Suttle ◽  
...  
Keyword(s):  
Sugar Beet ◽  
Gene Cluster ◽  
Fungal Pathogens ◽  
Plant Pathogens ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Phylogenomic Analysis ◽  
First Case ◽  
Horizontal Transfers ◽  
Fungal Genus

AbstractSpecies 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.Significance 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.

scholarly journals Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum

2018 ◽  
Vol 115 (24) ◽  
pp. E5459-E5466 ◽  
Author(s):  
Ronnie de Jonge ◽  
Malaika K. Ebert ◽  
Callie R. Huitt-Roehl ◽  
Paramita Pal ◽  
Jeffrey C. Suttle ◽  
...  
Keyword(s):  
Sugar Beet ◽  
Gene Cluster ◽  
Plant Pathogens ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Cercospora Beticola ◽  
Phylogenomic Analysis ◽  
Food Crops ◽  
Horizontal Transfers ◽  
Insight Into

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 Cercospora 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 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, previously shown to be involved with cercosporin autoresistance, and four additional genes required for cercosporin biosynthesis, including the final pathway enzymes that install the unusual cercosporin methylenedioxy bridge. Lastly, we demonstrate production of cercosporin by Colletotrichum fioriniae, the first known cercosporin producer within this agriculturally important genus. Thus, our results provide 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.

scholarly journals Gene cluster conservation identifies melanin and perylenequinone biosynthesis pathways in multiple plant pathogenic fungi

2018 ◽  
Author(s):  
Malaika K. Ebert ◽  
Rebecca E. Spanner ◽  
Ronnie de Jonge ◽  
David J. Smith ◽  
Jason Holthusen ◽  
...  
Keyword(s):  
Gene Cluster ◽  
Plant Pathogens ◽  
Phylogenetic Analyses ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Host Cells ◽  
Plant Pathogenic Fungi ◽  
Biosynthetic Pathways ◽  
Biosynthetic Gene ◽  
Melanin Production

SummaryPerylenequinones are a family of structurally related polyketide fungal toxins with nearly universal toxicity. These photosensitizing compounds absorb light energy which enables them to generate reactive oxygen species that damage host cells. This potent mechanism serves as an effective weapon for plant pathogens in disease establishment. The sugar beet pathogenCercospora beticolasecretes the perylenequinone cercosporin during infection. We have shown recently that the cercosporin toxin biosynthesis(CTB)gene cluster is present in several other phytopathogenic fungi, prompting the search for biosynthetic gene clusters (BGCs) of structurally similar perylenequinones in other fungi. Here, we report the identification of the elsinochrome and phleichrome BGCs ofElsinoё fawcettiiandCladosporium phlei,respectively, based on gene cluster conservation with theCTBand hypocrellin BGCs. Furthermore, we show that previously reported BGCs for elsinochrome and phleichrome are involved in melanin production. Phylogenetic analysis of the corresponding melanin polyketide synthases (PKSs) and alignment of melanin BGCs revealed high conservation between the established and newly identifiedC. beticola, E. fawcettii,andC. phleimelanin BGCs. Mutagenesis of the identified perylenequinone and melanin PKSs inC. beticolaandE. fawcettiicoupled with mass spectrometric metabolite analyses confirmed their roles in toxin and melanin production.Originality and significance statementGenes involved in secondary metabolite (SM) production are often clustered together to form biosynthetic pathways. These pathways frequently have highly conserved keystone enzymes which can complicate allocation of a biosynthetic gene cluster (BGC) to the cognate SM. In our study, we utilized a combination of comparative genomics, phylogenetic analyses and biochemical approaches to reliably identify BGCs for perylenequinone toxins and DHN-melanin in multiple plant pathogenic fungi. Furthermore, we show that earlier studies that aimed to identify these perylenequinone pathways were misdirected and actually reported DHN-melanin biosynthetic pathways. Our study outlines a reliable approach to successfully identify fungal SM pathways.

scholarly journals A Rare Thioquinolobactin Siderophore Present in a Bioactive Pseudomonas sp. DTU12.1

2019 ◽  
Vol 11 (12) ◽  
pp. 3529-3533
Author(s):  
Pavelas Sazinas ◽  
Morten Lindqvist Hansen ◽  
May Iren Aune ◽  
Marie Højmark Fischer ◽  
Lars Jelsbak
Keyword(s):  
Gene Cluster ◽  
Secondary Metabolite ◽  
Genome Sequence ◽  
Complete Genome Sequence ◽  
Complete Genome ◽  
Plant Pathogens ◽  
Gene Clusters ◽  
Fungal Species ◽  
Antagonistic Activity ◽  
Evolutionary Origins

Abstract Many of the soil-dwelling Pseudomonas species are known to produce secondary metabolite compounds, which can have antagonistic activity against other microorganisms, including important plant pathogens. It is thus of importance to isolate new strains of Pseudomonas and discover novel or rare gene clusters encoding bioactive products. In an effort to accomplish this, we have isolated a bioactive Pseudomonas strain DTU12.1 from leaf-covered soil in Denmark. Following genome sequencing with Illumina and Oxford Nanopore technologies, we generated a complete genome sequence with the length of 5,943,629 base pairs. The DTU12.1 strain contained a complete gene cluster for a rare thioquinolobactin siderophore, which was previously described as possessing bioactivity against oomycetes and several fungal species. We placed the DTU12.1 strain within Pseudomonas gessardii subgroup of fluorescent pseudomonads, where it formed a distinct clade with other Pseudomonas strains, most of which also contained a complete thioquinolobactin gene cluster. Only two other Pseudomonas strains were found to contain the gene cluster, though they were present in a different phylogenetic clade and were missing a transcriptional regulator of the whole cluster. We show that having the complete genome sequence and establishing phylogenetic relationships with other strains can enable us to start evaluating the distribution and evolutionary origins of secondary metabolite clusters.

scholarly journals Genome, Transcriptome, and Functional Analyses of Penicillium expansum Provide New Insights Into Secondary Metabolism and Pathogenicity

2015 ◽  
Vol 28 (3) ◽  
pp. 232-248 ◽  
Author(s):  
Ana-Rosa Ballester ◽  
Marina Marcet-Houben ◽  
Elena Levin ◽  
Noa Sela ◽  
Cristina Selma-Lázaro ◽  
...  
Keyword(s):  
Secondary Metabolites ◽  
Secondary Metabolism ◽  
Plant Pathogens ◽  
Citrus Fruit ◽  
Genomic Analysis ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Penicillium Expansum ◽  
Pome Fruit ◽  
Penicillium Species

The relationship between secondary metabolism and infection in pathogenic fungi has remained largely elusive. The genus Penicillium comprises a group of plant pathogens with varying host specificities and with the ability to produce a wide array of secondary metabolites. The genomes of three Penicillium expansum strains, the main postharvest pathogen of pome fruit, and one Pencillium italicum strain, a postharvest pathogen of citrus fruit, were sequenced and compared with 24 other fungal species. A genomic analysis of gene clusters responsible for the production of secondary metabolites was performed. Putative virulence factors in P. expansum were identified by means of a transcriptomic analysis of apple fruits during the course of infection. Despite a major genome contraction, P. expansum is the Penicillium species with the largest potential for the production of secondary metabolites. Results using knockout mutants clearly demonstrated that neither patulin nor citrinin are required by P. expansum to successfully infect apples. Li et al. ( MPMI-12-14-0398-FI ) reported similar results and conclusions in MPMI's June 2015 issue.

scholarly journals Comparative genome analyses of four rice-infecting Rhizoctonia solani isolates reveal extensive enrichment of homogalacturonan modification genes

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Da-Young Lee ◽  
Jongbum Jeon ◽  
Ki-Tae Kim ◽  
Kyeongchae Cheong ◽  
Hyeunjeong Song ◽  
...  
Keyword(s):  
Rhizoctonia Solani ◽  
Single Molecule ◽  
De Novo ◽  
Average Length ◽  
Gene Clusters ◽  
Anastomosis Group ◽  
Secreted Proteins ◽  
Geographical Regions ◽  
Wide Range ◽  
Fungal Genomes

Abstract Background Plant pathogenic isolates of Rhizoctonia solani anastomosis group 1-intraspecific group IA (AG1-IA) infect a wide range of crops causing diseases such as rice sheath blight (ShB). ShB has become a serious disease in rice production worldwide. Additional genome sequences of the rice-infecting R. solani isolates from different geographical regions will facilitate the identification of important pathogenicity-related genes in the fungus. Results Rice-infecting R. solani isolates B2 (USA), ADB (India), WGL (India), and YN-7 (China) were selected for whole-genome sequencing. Single-Molecule Real-Time (SMRT) and Illumina sequencing were used for de novo sequencing of the B2 genome. The genomes of the other three isolates were then sequenced with Illumina technology and assembled using the B2 genome as a reference. The four genomes ranged from 38.9 to 45.0 Mbp in size, contained 9715 to 11,505 protein-coding genes, and shared 5812 conserved orthogroups. The proportion of transposable elements (TEs) and average length of TE sequences in the B2 genome was nearly 3 times and 2 times greater, respectively, than those of ADB, WGL and YN-7. Although 818 to 888 putative secreted proteins were identified in the four isolates, only 30% of them were predicted to be small secreted proteins, which is a smaller proportion than what is usually found in the genomes of cereal necrotrophic fungi. Despite a lack of putative secondary metabolite biosynthesis gene clusters, the rice-infecting R. solani genomes were predicted to contain the most carbohydrate-active enzyme (CAZyme) genes among all 27 fungal genomes used in the comparative analysis. Specifically, extensive enrichment of pectin/homogalacturonan modification genes were found in all four rice-infecting R. solani genomes. Conclusion Four R. solani genomes were sequenced, annotated, and compared to other fungal genomes to identify distinctive genomic features that may contribute to the pathogenicity of rice-infecting R. solani. Our analyses provided evidence that genomic conservation of R. solani genomes among neighboring AGs was more diversified than among AG1-IA isolates and the presence of numerous predicted pectin modification genes in the rice-infecting R. solani genomes that may contribute to the wide host range and virulence of this necrotrophic fungal pathogen.

scholarly journals MoCpa1-mediated arginine biosynthesis is crucial for fungal growth, conidiation, and plant infection of Magnaporthe oryzae

2020 ◽  
Author(s):  
Osakina Aron ◽  
Min Wang ◽  
Anjago Wilfred Mabeche ◽  
Batool Wajjiha ◽  
Shuai Yang ◽  
...  
Keyword(s):  
Amino Acid ◽  
Magnaporthe Oryzae ◽  
Plant Pathogens ◽  
De Novo ◽  
Pathogenic Fungi ◽  
Host Cells ◽  
Arginine Biosynthesis ◽  
Carbamoyl Phosphate ◽  
Genome Database ◽  
Fungal Plant Pathogens

AbstractArginine is an important amino acid involved in processes such as cell signal transduction, protein synthesis, and sexual reproduction. To understand the biological roles of arginine biosynthesis in pathogenic fungi, we used Cpa1, the carbamoyl phosphate synthase arginine-specific small chain subunit in Saccharomyces cerevisiae as a query to identify its ortholog in Magnaporthe oryzae genome database and named it MoCpa1. MoCpa1 is a 471-amino acid protein containing the CPSase_sm_chain domain and the GATase domain. MoCpa1 transcripts were highly expressed at the conidiation, early-infection, and late-infection stages of the fungus. Targeted deletion of MoCPA1 gene resulted in the ΔMocpa1 mutant exhibiting arginine auxotrophy on MM, confirming its role in de novo arginine biosynthesis. The ΔMocpa1 mutant presented significantly decreased sporulation with some of its conidia being defective in morphology. Furthermore, the ΔMocpa1 mutant was nonpathogenic on rice and barley leaves, which was a result of defects in appressorium-mediated penetration and restricted invasive hyphal growth within host cells. Addition of exogenous arginine partially rescued conidiation and pathogenicity defects on the barley and rice leaves, while introduction of MoCPA1 gene in ΔMocpa1 mutant fully complemented the lost phenotype. Further confocal microscopy examination revealed that MoCpa1 is localized in the mitochondria. In summary, our results demonstrate that MoCpa1-mediated arginine biosynthesis is crucial for fungal development, conidiation, appressorium formation and infection-related morphogenesis in M. oryzae, thus serving as an attractive target for mitigating obstinate fungal plant pathogens.

scholarly journals The Genomic Sequence of Pseudomonas fluorescens Pf-5: Insights Into Biological Control

2007 ◽  
Vol 97 (2) ◽  
pp. 233-238 ◽  
Author(s):  
Joyce E. Loper ◽  
Donald Y. Kobayashi ◽  
Ian T. Paulsen
Keyword(s):  
Biological Control ◽  
Pseudomonas Fluorescens ◽  
Secondary Metabolite ◽  
Plant Pathogens ◽  
Genomic Sequence ◽  
Biological Control Agent ◽  
Seedling Emergence ◽  
Pathogenic Fungi ◽  
Gene Clusters ◽  
Membrane Receptors

The complete sequence of the 7.07 Mb genome of the biological control agent Pseudomonas fluorescens Pf-5 is now available, providing a new opportunity to advance knowledge of biological control through genomics. P. fluorescens Pf-5 is a rhizosphere bacterium that suppresses seedling emergence diseases and produces a spectrum of antibiotics toxic to plant-pathogenic fungi and oomycetes. In addition to six known secondary metabolites produced by Pf-5, three novel secondary metabolite biosynthesis gene clusters identified in the genome could also contribute to biological control. The genomic sequence provides numerous clues as to mechanisms used by the bacterium to survive in the spermosphere and rhizosphere. These features include broad catabolic and transport capabilities for utilizing seed and root exudates, an expanded collection of efflux systems for defense against environmental stress and microbial competition, and the presence of 45 outer membrane receptors that should allow for the uptake of iron from a wide array of siderophores produced by soil microorganisms. As expected for a bacterium with a large genome that lives in a rapidly changing environment, Pf-5 has an extensive collection of regulatory genes, only some of which have been characterized for their roles in regulation of secondary metabolite production or biological control. Consistent with its commensal lifestyle, Pf-5 appears to lack a number of virulence and pathogenicity factors found in plant pathogens.

scholarly journals Biosynthetic gene clusters and the evolution of fungal chemodiversity

2020 ◽  
Vol 37 (7) ◽  
pp. 868-878 ◽  
Author(s):  
Antonis Rokas ◽  
Matthew E. Mead ◽  
Jacob L. Steenwyk ◽  
Huzefa A. Raja ◽  
Nicholas H. Oberlies
Keyword(s):  
Gene Cluster ◽  
Horizontal Transfer ◽  
De Novo ◽  
Functional Divergence ◽  
Gene Clusters ◽  
Biosynthetic Gene Cluster ◽  
Biosynthetic Gene ◽  
Biosynthetic Gene Clusters ◽  
Evolutionary Processes

This highlight synthesizes knowledge of the molecular evolutionary processes – functional divergence, horizontal transfer, and de novo assembly – that govern biosynthetic gene cluster diversification and the generation of chemodiversity in fungi.

Sign in / Sign up

Export Citation Format

Share Document