RNAi is a critical determinant of centromere evolution in closely related fungi

Yadav, Vikas; Sun, Sheng; Billmyre, R. Blake; Thimmappa, Bhagya C.; Shea, Terrance; Lintner, Robert E.; Bakkeren, Guus; Cuomo, Christina A.; Heitman, Joseph; Sanyal, Kaustuv

doi:10.1073/pnas.1713725115

Cited by 125 publications

(277 citation statements)

References 55 publications

Supporting

Mentioning

260

Contrasting

Order By: Relevance

“…Genomic DNA samples were extracted using a modified CTAB protocol as previously reported [31,106]. Specifically, to enrich samples with high molecular weight, after precipitation, the genomic DNA was picked out from the solution instead of spun down, and the samples were checked by CHEF for their sizes and integrity, following manufacturer's protocol (BioRad, Hercules, CA, USA).…”

Section: Oleaginosum Atcc20508mentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

Sun

Coelho

Heitman

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

Author summarySexual development in fungi is governed by mating-type (MAT) genes, and the corresponding MAT loci show similarities to sex chromosomes in animals and plants. One common feature is an evolutionary trend towards combining sex-associated genes on the same chromosome, which can evolve by selection because it facilitates linkage of favorable allele combinations.Here, we show that this occurred in the Trichosporonales, a sister group to the Tremellales, similar to the expanded, fused MAT loci discovered previously in the human pathogen Cryptococcus neoformans. Our data suggest that fusion of MAT loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions in fungi. amylolentus, Kwoniella heveanensis, Kwoniella mangrovensis, Cryptococcus wingfieldii, andCryptococcus floricola are all tetrapolar [29][30][31][32][33]. The fused C. neoformans MAT locus encompasses more than 20 genes over a region spanning more than 100 kb and has two alleles designated a and . In the majority of basidiomycetes, each MAT allele at the HD locus carries both the HD1 and the HD2 transcription factor genes, whereas in C. neoformans, the MAT locus contains only the HD1 gene SXI1, and MATa contains only the HD2 gene SXI2a. Except for a gene conversion hotspot, the C. neoformans MAT locus displays suppressed meiotic recombination [23,34,35].Among the Tremellomycetes, pathogenic Cryptococci are so far the only species for which fused MAT loci have been described [17,23]. In a previous study, we analyzed the genome sequence of Cutaneotrichosporon oleaginosum strain IBC0246 (formerly Trichosporon oleaginosus), which belongs to the Trichosporonales, a sister order to the Tremellales within the Tremellomycetes class. Trichosporonales species are widely distributed in the environment and have been isolated from a variety of substrates including soil, decaying plant material, and water. Many species are saprobes, but some have also been found to be associated with animals including humans either as commensals or pathogens [36][37][38].Despite their common occurrence in the environment, Trichosporonales are an understudied fungal group, and sexual reproduction has not yet been observed for any of the known species [39,40]. Recently, several Trichosporonales were studied with respect to their biotechnological properties, including the oil-accumulating C. oleaginosum, which was first isolated from a dairy plant, and has the ability to metabolize chitin-rich and other nonconventional substrates [41][42][43][44]. The sequenced C. oleaginosum strain is haploid, and similar in genome size and gene content to genomes from the sister order Tremellales, and this was also the case for several other Trichosporonales genomes that have since been sequenced [43,[45][46][47][48][49][50]. Interestingly, C. oleaginosum showed some similarities to C. neoformans in the organization of MAT loci. This included recruitment of genes with diverse functions during mati...

show abstract

Section: Oleaginosum Atcc20508mentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

Sun

Coelho

Heitman

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The centromeres of C. deuterogattii consist of truncated transposable elements, and active transposable elements are missing throughout the genome [24]. This is in stark contrast to C. neoformans, which has active transposable elements in centromeric regions [24,25,29].…”

Section: Introductionmentioning

confidence: 97%

“…The dramatic reduction in centromere size in C. deuterogattii may be attributable to loss of the RNAi pathway and the DNMT5 gene, which encodes a DNA methyl transferase [24,28]. The centromeres of C. deuterogattii consist of truncated transposable elements, and active transposable elements are missing throughout the genome [24]. This is in stark contrast to C. neoformans, which has active transposable elements in centromeric regions [24,25,29].…”

Section: Introductionmentioning

confidence: 99%

“…Cryptococcus neoformans, revealing dramatically smaller centromeres in C. deuterogattii [24,25]. C. deuterogattii is responsible for an ongoing outbreak in the Pacific Northwest regions of Canada and the United States [26].…”

Section: Introductionmentioning

confidence: 99%

“…deuterogattii is a haploid basidiomycetous fungus with 14 chromosomes [24,27,28]. The dramatic reduction in centromere size in C. deuterogattii may be attributable to loss of the RNAi pathway and the DNMT5 gene, which encodes a DNA methyl transferase [24,28]. The centromeres of C. deuterogattii consist of truncated transposable elements, and active transposable elements are missing throughout the genome [24].…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Centromere deletion in Cryptococcus deuterogattii leads to neocentromere formation and chromosome fusions

Schotanus

Heitman

2019

Preprint

Self Cite

View full text Add to dashboard Cite

AbstractThe human fungal pathogen Cryptococcus deuterogattii is RNAi-deficient and lacks active transposons in its genome. C. deuterogattii has regional centromeres that contain only transposon relics. To investigate impact of centromere loss on the C. deuterogattii genome, either centromere 9 or 10 was deleted. Deletion of either centromere resulted in neocentromere formation and interestingly, the genes covered by these neocentromeres maintained wild-type expression levels. In contrast to cen9Δ mutants, cen10Δ mutant strains exhibited growth defects and were aneuploid for chromosome 10. At an elevated growth temperature (37°C), the cen10Δ chromosome was found to have undergone fusion with another native chromosome in some isolates and this fusion restored wild-type growth. Following chromosomal fusion, the neocentromere was inactivated, and the native centromere of the fused chromosome served as the active centromere. The neocentromere formation and chromosomal fusion events observed in this study in C. deuterogattii may be similar to events that triggered genomic changes within the Cryptococcus/Kwoniella species complex and may contribute to speciation throughout the eukaryotic domain.