A draft genome sequence of the rose black spot fungus Diplocarpon rosae reveals a high degree of genome duplication

Neu, Enzo; Featherston, Jonathan; Rees, D. J. G.; Debener, Thomas

doi:10.1371/journal.pone.0185310

Cited by 9 publications

(8 citation statements)

References 90 publications

(130 reference statements)

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“…7–8). Again, we identified only one intact copy of MSH4 in all species except the very recent polyploids ( Zygosaccharomyces rouxii ) and Diplocarpon rosae and Hortaea werneckii , two fungi that have retained 80 and 95% of gene duplicates post-WGDs, respectively 20,21 (Supplementary Fig. 8).…”

Section: Resultsmentioning

confidence: 95%

Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus

et al. 2019

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In allopolyploids, correct chromosome segregation requires suppression of non-homologous crossovers while levels of homologous crossovers are ensured. To date, no mechanism able to specifically inhibit non-homologous crossovers has been described in allopolyploids other than in bread wheat. Here, we show that reducing the number of functional copies of MSH4 , an essential gene for the main crossover pathway, prevents non-homologous crossovers in allotetraploid Brassica napus . We show that non-homologous crossovers originate almost exclusively from the MSH4 -dependent recombination pathway and that their numbers decrease when MSH4 returns to single copy in B. napus ; by contrast, homologous crossovers remain unaffected by MSH4 duplicate loss. We also demonstrate that MSH4 systematically returns to single copy following numerous independent polyploidy events, a pattern that is probably not by chance. These results suggest that stabilization of allopolyploid meiosis can be enhanced by loss of a key meiotic recombination gene.

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Section: Resultsmentioning

confidence: 95%

Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus

et al. 2019

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“…The DNA sequences of nuclear ribosomal ITS, elongation factor 1-α (EF1-α), glyceraldehyde-3-phosphate dehydrogenase (G3PDH), heat-shock protein 60 (HSP60) and DNAdependent RNA polymerase subunit II (RPB2) were obtained from the genome of M. coronaria NL1, 13 published genomes of Helotiales fungi and Blumeria graminis f. sp. hordei DH14 of Erysiphales [21,22,[31][32][33][34][35][36][37][38][39][40][41][42] and by homologous cloning from M. coronaria YL1 (S1 Table ). The concatenated DNA sequences of ITS, EF1-α, G3PDH, HSP60 and RPB2 were used to construct the phylogenetic tree.…”

Section: Plos Onementioning

confidence: 99%

“…The genomes of Marssonina brunnea f. sp. multigermtubi (hereafter M. brunnea) and Diplocarpon rosae (anamorph, Marssonina rosae) (hereafter M. rosae), the causal agents of poplar and rose black spot diseases, respectively, have been sequenced [21,22]. This study aimed to present the genome sequences and annotations of M. coronaria, identify species-specific carbohydrate-active enzyme (CAZymes), secondary metabolite biosynthetic gene clusters (SM-BGCs) and small-secreted proteins (SSPs) by comparing Marssonina spp.…”

Section: Introductionmentioning

confidence: 99%

Draft genome sequence of Marssonina coronaria, causal agent of apple blotch, and comparisons with the Marssonina brunnea and Marssonina rosae genomes

2021

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Marssonina coronaria Ellis & Davis is a filamentous fungus in the class Leotiomycetes that causes apple blotch, an economically important disease of apples worldwide. Here, we sequenced the whole genome of M. coronaria strain NL1. The genome contained 50.3 Mb with 589 scaffolds and 9,622 protein-coding genes. A phylogenetic analysis using multiple loci and a whole-genome alignment revealed that M. coronaria is closely related to Marssonina rosae and Marssonina brunnea. A comparison of the three genomes revealed 90 species-specific carbohydrate-active enzymes, 19 of which showed atypical distributions, and 12 species-specific secondary metabolite biosynthetic gene clusters, two of which have the potential to synthesize products analogous to PR toxin and swainsonine, respectively. We identified 796 genes encoding for small secreted proteins in Marssonina spp., many encoding for unknown hypothetical proteins. In addition, we revealed the genetic architecture of the MAT1-1 and MAT1-2 mating-type loci of M. coronaria, as well as 16 tested isolates carrying either MAT1-1 idiomorph (3) or MAT1-2 idiomorph (13). Our results showed a series of species-specific carbohydrate-active enzyme, secondary metabolite biosynthetic gene clusters and small-secreted proteins that may be involved in the adaptation of Marssonina spp. to their distinct hosts. We also confirmed that M. coronaria possesses a heterothallic mating system and has outcrossing potential in nature.

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“…Diplocarpon rosae and Hortaea werneckii (in orange on Figure 1A), two fungi that have retained 80% and 95% of gene duplicates post-WGDs, respectively 24,25 . Remnants of a second copy of MSH4 carrying inactivating changes were also detected in Linum usitatissimum, Glycine max and Populus trichocarpa (in orange or blue on Figure 1A) as well as in Salmo salar and Oncorhynchus mykiss (in blue on Figure 1B).…”

Section: Msh4 Illustrates Convergent Loss Of Duplicated Meiotic Recommentioning

confidence: 99%

“…The trees were customized and annotated using iTOL (https://itol.embl.de/). The occurrence and age for the past WGDs were taken from 24,25,30,[68][69][70][71][72][73] .…”

Section: Phylogeny Constructionmentioning

confidence: 99%

Meiotic effects ofMSH4copy number variation support an adaptive role for post-polyploidy gene loss

Gonzalo

Lucas

et al. 2018

Preprint

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Many eukaryotes descend from polyploid ancestors that experienced massive duplicate gene loss. This genomic erosion is particularly strong for duplicated (meiotic) recombination genes that return to a single copy more rapidly than genome average following polyploidy. To better understand the evolutionary forces underlying duplicate loss, we analysed how varying copy numbers of MSH4, an essential meiotic recombination gene, influences crossover formation in allotetraploid Brassica napus. We show that faithful chromosome segregation and crossover frequencies between homologous chromosomes are unchanged with MSH4 duplicate loss; by contrast, crossovers between homoeologous chromosomes (which result in genomic rearrangements) decrease with reductions in MSH4 copy number. We also found that inter-homoeologue crossovers originate almost exclusively from the MSH4-dependent crossover pathway. Limiting the efficiency of this pathway by decreasing the copy number of key meiotic recombination genes could therefore contribute to adaptation to polyploidy, by promoting regular chromosome segregation and genomic stability. TextGene duplication and gene loss are two driving forces in evolution 1-3 . These two mechanisms are well illustrated by the evolution of the meiotic recombination machinery. At the outset, the emergence of meiosis required key evolutionary breakthroughs 4-6 that were all made possible through iterative gene duplications followed by acquisition of new functions. These include, among others, the formation of programmed DNA double-strand breaks by SPO11 proteins 7 , the promotion of double-strand break repair using homologous templates by DMC1, RAD51 and some other related proteins 8 or the resolution of recombination intermediates as crossovers by MSH and MLH proteins 9 . After this initial phase, genes involved in meiotic recombination (and DNA repair in general) have tended to return preferentially to single copy following subsequent duplications 10,11 , with some

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A draft genome sequence of the rose black spot fungus Diplocarpon rosae reveals a high degree of genome duplication

Cited by 9 publications

References 90 publications

Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus

Reducing MSH4 copy number prevents meiotic crossovers between non-homologous chromosomes in Brassica napus

Draft genome sequence of Marssonina coronaria, causal agent of apple blotch, and comparisons with the Marssonina brunnea and Marssonina rosae genomes

Meiotic effects ofMSH4copy number variation support an adaptive role for post-polyploidy gene loss

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