Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster

<p>Abstract</p> <p>Background</p> <p>The biosynthesis of aflatoxin (AF) involves over 20 enzymatic reactions in a complex polyketide pathway that converts acetate and malonate to the intermediates sterigmatocystin (ST) and <it>O</it>-methylsterigmatocystin (OMST), the respective penultimate and ultimate precursors of AF. Although these precursors are chemically and structurally very similar, their accumulation differs at the species level for Aspergilli. Notable examples are <it>A</it>. <it>nidulans </it>that synthesizes only ST, <it>A</it>. <it>flavus </it>that makes predominantly AF, and <it>A</it>. <it>parasiticus </it>that generally produces either AF or OMST. Whether these differences are important in the evolutionary/ecological processes of species adaptation and diversification is unknown. Equally unknown are the specific genomic mechanisms responsible for ordering and clustering of genes in the AF pathway of <it>Aspergillus</it>.</p> <p>Results</p> <p>To elucidate the mechanisms that have driven formation of these clusters, we performed systematic searches of aflatoxin cluster homologs across five <it>Aspergillus </it>genomes. We found a high level of gene duplication and identified seven modules consisting of highly correlated gene pairs (<it>aflA/aflB, aflR/aflS, aflX/aflY</it>, <it>aflF/aflE, aflT/aflQ</it>, <it>aflC/aflW</it>, and <it>aflG/aflL</it>). With the exception of <it>A. nomius</it>, contrasts of mean <it>Ka/Ks </it>values across all cluster genes showed significant differences in selective pressure between section <it>Flavi </it>and non-section <it>Flavi </it>species. <it>A. nomius </it>mean <it>Ka/Ks </it>values were more similar to partial clusters in <it>A. fumigatus </it>and <it>A. terreus</it>. Overall, mean <it>Ka/Ks </it>values were significantly higher for section <it>Flavi </it>than for non-section <it>Flavi </it>species.</p> <p>Conclusion</p> <p>Our results implicate several genomic mechanisms in the evolution of ST, OMST and AF cluster genes. Gene modules may arise from duplications of a single gene, whereby the function of the pre-duplication gene is retained in the copy (<it>aflF</it>/<it>aflE</it>) or the copies may partition the ancestral function (<it>aflA/aflB</it>). In some gene modules, the duplicated copy may simply augment/supplement a specific pathway function (<it>aflR/aflS </it>and <it>aflX/aflY</it>) or the duplicated copy may evolve a completely new function (<it>aflT/aflQ </it>and <it>aflC/aflW</it>). Gene modules that are contiguous in one species and noncontiguous in others point to possible rearrangements of cluster genes in the evolution of these species. Significantly higher mean <it>Ka/Ks </it>values in section <it>Flavi </it>compared to non-section <it>Flavi </it>species indicate increased positive selection acting in the evolution of genes in OMST and AF gene clusters.</p

The evolutionary history of Cytochrome P450 genes in four filamentous Ascomycetes

BACKGROUND: The Cytochrome P450 system is important in fungal evolution for adapting to novel ecological niches. To elucidate the evolutionary process of cytochrome P450 genes in fungi with different life styles, we studied the patterns of gene gains and losses in the genomes of four filamentous Ascomycetes, including two saprotrophs (Aspergillus nidulans (AN) and Neurospora crassa (NC)) and two plant pathogens (Fusarium graminearum (FG) and Magnaporthe grisea (MG)). RESULTS: A total of 376 P450 genes were assigned to 168 families according to standard nomenclature. On average, only 1 to 2 genes per family were in each genome. To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans. Subsequently a novel approach based on parsimony was developed to build the evolutionary models. Based on these analyses, a core of 30 distinct clans of P450s was defined. The core clans experienced contraction in all four fungal lineages while new clans expanded in all with exception of NC. MG experienced more genes and clans gains compared to the other fungi. Parsimonious analyses unanimously supported one species topology for the four fungi. CONCLUSION: The four studied fungi exhibit unprecedented diversity in their P450omes in terms of coding sequence, intron-exon structures and genome locations, suggesting a complicated evolutionary history of P450s in filamentous Ascomycetes. Clan classification and a novel strategy were developed to study evolutionary history. Contraction of core clans and expansion of novel clans were identified. The exception was the NC lineage, which exhibited pure P450 gene loss

Cultural and Genetic Approaches to Manage Aflatoxin Contamination: Recent Insights Provide Opportunities for Improved Control.

Aspergillus flavus is a morphologically complex species that can produce the group of polyketide derived carcinogenic and mutagenic secondary metabolites, aflatoxins, as well as other secondary metabolites such as cyclopiazonic acid and aflatrem. Aflatoxin causes aflatoxicosis when aflatoxins are ingested through contaminated food and feed. In addition, aflatoxin contamination is a major problem, from both an economic and health aspect, in developing countries, especially Asia and Africa, where cereals and peanuts are important food crops. Earlier measures for control of A. flavus infection and consequent aflatoxin contamination centered on creating unfavorable environments for the pathogen and destroying contaminated products. While development of atoxigenic (nonaflatoxin producing) strains of A. flavus as viable commercial biocontrol agents has marked a unique advance for control of aflatoxin contamination, particularly in Africa, new insights into the biology and sexuality of A. flavus are now providing opportunities to design improved atoxigenic strains for sustainable biological control of aflatoxin. Further, progress in the use of molecular technologies such as incorporation of antifungal genes in the host and host-induced gene silencing, is providing knowledge that could be harnessed to develop germplasm that is resistant to infection by A. flavus and aflatoxin contamination. This review summarizes the substantial progress that has been made to understand the biology of A. flavus and mitigate aflatoxin contamination with emphasis on maize. Concepts developed to date can provide a basis for future research efforts on the sustainable management of aflatoxin contamination

The evolutionary history of Cytochrome P450 genes in four filamentous Ascomycetes

Abstract Background The Cytochrome P450 system is important in fungal evolution for adapting to novel ecological niches. To elucidate the evolutionary process of cytochrome P450 genes in fungi with different life styles, we studied the patterns of gene gains and losses in the genomes of four filamentous Ascomycetes, including two saprotrophs (Aspergillus nidulans (AN) and Neurospora crassa (NC)) and two plant pathogens (Fusarium graminearum (FG) and Magnaporthe grisea (MG)). Results A total of 376 P450 genes were assigned to 168 families according to standard nomenclature. On average, only 1 to 2 genes per family were in each genome. To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans. Subsequently a novel approach based on parsimony was developed to build the evolutionary models. Based on these analyses, a core of 30 distinct clans of P450s was defined. The core clans experienced contraction in all four fungal lineages while new clans expanded in all with exception of NC. MG experienced more genes and clans gains compared to the other fungi. Parsimonious analyses unanimously supported one species topology for the four fungi. Conclusion The four studied fungi exhibit unprecedented diversity in their P450omes in terms of coding sequence, intron-exon structures and genome locations, suggesting a complicated evolutionary history of P450s in filamentous Ascomycetes. Clan classification and a novel strategy were developed to study evolutionary history. Contraction of core clans and expansion of novel clans were identified. The exception was the NC lineage, which exhibited pure P450 gene loss

Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens

<p>Abstract</p> <p>Background</p> <p>Duplication, followed by fixation or random loss of novel genes, contributes to genome evolution. Particular outcomes of duplication events are possibly associated with pathogenic life histories in fungi. To date, differential gene gain and loss have not been studied at genomic scales in fungal pathogens, despite this phenomenon's known importance in virulence in bacteria and viruses.</p> <p>Results</p> <p>To determine if patterns of gene duplication differed between pathogens and non-pathogens, we identified gene families across nine euascomycete and two basidiomycete species. Gene family size distributions were fit to power laws to compare gene duplication trends in pathogens <it>versus </it>non-pathogens. Fungal phytopathogens showed globally altered patterns of gene duplication, as indicated by differences in gene family size distribution. We also identified sixteen examples of gene family expansion and five instances of gene family contraction in pathogenic lineages. Expanded gene families included those predicted to be important in melanin biosynthesis, host cell wall degradation and transport functions. Contracted families included those encoding genes involved in toxin production, genes with oxidoreductase activity, as well as subunits of the vacuolar ATPase complex. Surveys of the functional distribution of gene duplicates indicated that pathogens show enrichment for gene duplicates associated with receptor and hydrolase activities, while euascomycete pathogens appeared to have not only these differences, but also significantly more duplicates associated with regulatory and carbohydrate binding functions.</p> <p>Conclusion</p> <p>Differences in the overall levels of gene duplication in phytopathogenic species <it>versus </it>non-pathogenic relatives implicate gene inventory flux as an important virulence-associated process in fungi. We hypothesize that the observed patterns of gene duplicate enrichment, gene family expansion and contraction reflect adaptation within pathogenic life histories. These adaptations were likely shaped by ancient, as well as contemporary, intimate associations with monocot hosts.</p

Analysis of mycobiomes to uncover biodiversity: a case study between soil fungi and orchid species in Sweden

Abstracts from the April 12-14, 2019 MASC Conferenc

Population structure and diversity of an invasive pine needle pathogen reflects anthropogenic activity

Dothistroma septosporum is a haploid fungal pathogen that causes a serious needle blight disease of pines, particularly as an invasive alien species on Pinus radiata in the Southern Hemisphere. During the course of the last two decades, the pathogen has also incited unexpected epidemics on native and non-native pine hosts in the Northern Hemisphere. Although the biology and ecology of the pathogen has been well documented, there is a distinct lack of knowledge regarding its movement or genetic diversity in many of the countries where it is found. In this study we determined the global population diversity and structure of 458 isolates of D. septosporum from 14 countries on six continents using microsatellite markers. Populations of the pathogen in the Northern Hemisphere, where pines are native, displayed high genetic diversities and included both mating types. Most of the populations from Europe showed evidence for random mating, little population differentiation and gene flow between countries. Populations in North America (USA) and Asia (Bhutan) were genetically distinct but migration between these continents and Europe was evident. In the Southern Hemisphere, the population structure and diversity of D. septosporum reflected the anthropogenic history of the introduction and establishment of plantation forestry, particularly with Pinus radiata. Three introductory lineages in the Southern Hemisphere were observed. Countries in Africa, that have had the longest history of pine introductions, displayed the greatest diversity in the pathogen population, indicating multiple introductions. More recent introductions have occurred separately in South America and Australasia where the pathogen population is currently reproducing clonally due to the presence of only one mating type.The Department of Science and Technology (DST)/National Research Foundation (NRF), the Tree Protection Co-operative Programme (TPCP), the Claude Leon Foundation and the THRIP initiative of the Department of Trade and Industry, South Africa.http://onlinelibrary.wiley.comjournal/10.1002/(ISSN)2045-7758am201

Climate and seasonality drive the richness and composition of tropical fungal endophytes at a landscape scale

Understanding how species-rich communities persist is a foundational question in ecology. In tropical forests, tree diversity is structured by edaphic factors, climate, and biotic interactions, with seasonality playing an essential role at landscape scales: wetter and less seasonal forests typically harbor higher tree diversity than more seasonal forests. We posited that the abiotic factors shaping tree diversity extend to hyperdiverse symbionts in leaves—fungal endophytes—that influence plant health, function, and resilience to stress. Through surveys in forests across Panama that considered climate, seasonality, and covarying biotic factors, we demonstrate that endophyte richness varies negatively with temperature seasonality. Endophyte community structure and taxonomic composition reflect both temperature seasonality and climate (mean annual temperature and precipitation). Overall our findings highlight the vital role of climate-related factors in shaping the hyperdiversity of these important and little-known symbionts of the trees that, in turn, form the foundations of tropical forest biodiversity