Advances in understanding the evolution of fungal genome architecture

Priest, Shelby; Yadav, Vikas; Heitman, Joseph

doi:10.12688/f1000research.25424.1

Cited by 43 publications

(42 citation statements)

References 167 publications

(179 reference statements)

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“…Polyploidy may be a response to stress, as it expands the genomic options for adaptation ( Fox et al 2020 ). Whole genome duplication has been an important contributor to the evolution of fungi, animals and plants ( Otto and Whitton 2000 ; Priest et al 2020 ). One of the most complex genomic resource management systems known has been described in Ciliates ( Prescott 2000 ).…”

Section: Evidence Of Extreme Polyploidy In Giant Bacterial Cellsmentioning

confidence: 99%

Challenges Faced by Highly Polyploid Bacteria with Limits on DNA Inheritance

Angert

2021

Genome Biology and Evolution

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Most studies of bacterial reproduction have centered on organisms that undergo binary fission. In these models, complete chromosome copies are segregated with great fidelity into two equivalent offspring cells. All genetic material is passed on to offspring, including new mutations and horizontally acquired sequences. However, some bacterial lineages employ diverse reproductive patterns that require management and segregation of more than two chromosome copies. Epulopiscium spp., and their close relatives within the Firmicutes phylum, are intestinal symbionts of surgeonfish (family Acanthuridae). Each of these giant (up to 0.6 mm long), cigar-shaped bacteria contains tens of thousands of chromosome copies. Epulopiscium spp. do not use binary fission but instead produce multiple intracellular offspring. Only ∼1% of the genetic material in an Epulopiscium sp. type B mother cell is directly inherited by its offspring cells. And yet, even in late stages of offspring development, mother-cell chromosome copies continue to replicate. Consequently, chromosomes take on a somatic or germline role. Epulopiscium sp. type B is a strict anaerobe and while it is an obligate symbiont, its host has a facultative association with this intestinal microorganism. Therefore, Epulopiscium sp. type B populations face several bottlenecks that could endanger their diversity and resilience. Multilocus sequence analyses revealed that recombination is important to diversification in populations of Epulopiscium sp. type B. By employing mechanisms common to others in the Firmicutes, the coordinated timing of mother-cell lysis, offspring development and congression may facilitate the substantial recombination observed in Epulopiscium sp. type B populations.

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Section: Evidence Of Extreme Polyploidy In Giant Bacterial Cellsmentioning

confidence: 99%

Challenges Faced by Highly Polyploid Bacteria with Limits on DNA Inheritance

Angert

2021

Genome Biology and Evolution

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“…Fungi comprise a diverse group of organisms evolving over the past 900 My ( Dornburg et al 2017 ; Kumar et al 2017 ), and this diversity is reflected in diverse histories of exon–intron structures. Some fungal clades have undergone massive loss of introns, in particular, the intracellular parasites microsporidia as well as saccharomycetous yeasts ( Byrne and Wolfe 2005 ; Neuvéglise et al 2011 ; Hooks et al 2014 ; Corradi 2015 ; Han and Weiss 2017 ; Whelan et al 2019 ; Priest et al 2020 ; Wang et al 2020 ). For instance, only 4% of S. cerevisiae genes have introns.…”

Section: Introductionmentioning

confidence: 99%

“…Previous results have suggested that frequent intron loss events, relatively few instances of intron gain, and the retention of ancestral introns characterize the evolution of introns throughout most fungal lineages ( Csűrös et al 2007 , 2011 ; Stajich et al 2007 ). With thousands of fungal genomes available to date ( Priest et al 2020 ), it is timely to revisit the ancestral states and scale of intron gain and loss in the fungal kingdom. Our analysis of 644 fungal genomes includes representatives from nearly all phylum-level clades, including the early-diverging Blastocladiomycota, Chytridiomycota, Mucoromycota, Zoopagomycota, Cryptomycota, and Microsporidia phyla.…”

Section: Introductionmentioning

confidence: 99%

“…Our analysis of 644 fungal genomes includes representatives from nearly all phylum-level clades, including the early-diverging Blastocladiomycota, Chytridiomycota, Mucoromycota, Zoopagomycota, Cryptomycota, and Microsporidia phyla. The diversity of exon–intron structures and the wealth of kingdom-wide genomic resources of fungi make them excellent models for studying the intron gain and loss dynamics and the functional roles of introns ( Priest et al 2020 ). Here, we show how intron gain and loss reshape the exon–intron gene structure and suggest why intron conservation may be important for function.…”

Section: Introductionmentioning

confidence: 99%

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Analysis of Fungal Genomes Reveals Commonalities of Intron Gain or Loss and Functions in Intron-Poor Species

Lim

Weinstein

Roy

et al. 2021

Molecular Biology and Evolution

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Previous evolutionary reconstructions have concluded that early eukaryotic ancestors including both the last common ancestor of eukaryotes and of all fungi had intron-rich genomes. By contrast, some extant eukaryotes have few introns, underscoring the complex histories of intron-exon structures, and raising the question as to why these few introns are retained. Here we have used recently available fungal genomes to address a variety of questions related to intron evolution. Evolutionary reconstruction of intron presence and absence using 263 diverse fungal species supports the idea that massive intron reduction through intron loss has occurred in multiple clades. The intron densities estimated in various fungal ancestors differ from zero to 7.6 introns per one kbp of protein-coding sequence. Massive intron loss has occurred not only in microsporidian parasites and saccharomycetous yeasts, but also in diverse smuts and allies. To investigate the roles of the remaining introns in highly-reduced species, we have searched for their special characteristics in eight intron-poor fungi. Notably, the introns of ribosome associated genes RPL7 and NOG2 have conserved positions; both intron-containing genes encoding snoRNAs. Furthermore, both the proteins and snoRNAs are involved in ribosome biogenesis, suggesting that the expression of the protein-coding genes and non-coding snoRNAs may be functionally coordinated. Indeed, these introns are also conserved in three-quarters of fungi species. Our study shows that fungal introns have a complex evolutionary history and underappreciated roles in gene expression.

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“…The completeness of the assembly was evaluated with plant-specific (viridiplantae_odb10.2019- [11][12][13][14][15][16][17][18][19][20] and eudicot-specific (eudicots_odb10.2019- [11][12][13][14][15][16][17][18][19][20] Benchmarking Universal Single-Copy Orthologs (BUSCO v4.1.4) [40].…”

mentioning

confidence: 99%

A chromosome-level genome assembly of the European Beech (Fagus sylvatica) reveals anomalies for organelle DNA integration, repeat content and distribution of SNPs

Mishra

Ulaszewski

Meger

et al. 2021

Preprint

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Background: The European Beech is the dominant climax tree in most regions of Central Europe and valued for its ecological versatility and hardwood timber. Even though a draft genome has been published recently, higher resolution is required for studying aspects of genome architecture and recombination. Results: Here we present a chromosome-level assembly of the more than 300 year-old reference individual, Bhaga, from the Kellerwald-Edersee National Park (Germany). Its nuclear genome of 541 Mb was resolved into 12 chromosomes varying in length between 28 Mb and 73 Mb. Multiple nuclear insertions of parts of the chloroplast genome were observed, with one region on chromosome 11 spanning more than 2 Mb of the genome in which fragments up to 54,784 bp long and covering the whole chloroplast genome were inserted randomly. Unlike in Arabidopsis thaliana, ribosomal cistrons are present in Fagus sylvatica only in four major regions, in line with FISH studies. On most assembled chromosomes, telomeric repeats were found at both ends, while centromeric repeats were found to be scattered throughout the genome apart from their main occurrence per chromosome. The genome-wide distribution of SNPs was evaluated using a second individual from Jamy Nature Reserve (Poland). SNPs, repeat elements and duplicated genes were unevenly distributed in the genomes, with one major anomaly on chromosome 4. Conclusions: The genome presented here adds to the available highly resolved plant genomes and we hope it will serve as a valuable basis for future research on genome architecture and for understanding the past and future of European Beech populations in a changing climate.

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Advances in understanding the evolution of fungal genome architecture

Cited by 43 publications

References 167 publications

Challenges Faced by Highly Polyploid Bacteria with Limits on DNA Inheritance

Challenges Faced by Highly Polyploid Bacteria with Limits on DNA Inheritance

Analysis of Fungal Genomes Reveals Commonalities of Intron Gain or Loss and Functions in Intron-Poor Species

A chromosome-level genome assembly of the European Beech (Fagus sylvatica) reveals anomalies for organelle DNA integration, repeat content and distribution of SNPs

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