scholarly journals Variation of the meiotic recombination landscape and properties over a broad evolutionary distance in yeasts

2017 ◽  
Author(s):  
Christian Brion ◽  
Sylvain Legrand ◽  
Jackson Peter ◽  
Claudia Caradec ◽  
David Pflieger ◽  
...  

AbstractMeiotic recombination is a major factor of genome evolution, deeply characterized in only a few model species, notably the yeast Saccharomyces cerevisiae. Consequently, little is known about variations of its properties across species. In this respect, we explored the recombination landscape of Lachancea kluyveri, a protoploid yeast species that diverged from the Saccharomyces genus more than 100 million years ago and we found striking differences with S. cerevisiae. These variations include a lower recombination rate, a higher frequency of chromosomes segregating without any crossover and the absence of recombination on the chromosome arm containing the sex locus. In addition, although well conserved within the Saccharomyces clade, the S. cerevisiae recombination hotspots are not conserved over a broader evolutionary distance. Finally and strikingly, we found evidence of frequent reversion of meiotic commitment to mitotic growth allowing allele shuffling without meiosis completion. Identification of this major but underestimated evolutionary phenomenon illustrates the relevance of exploring non-model species.Author summaryMeiotic recombination promotes accurate chromosome segregation and genetic diversity. To date, the mechanisms and rules lying behind recombination were dissected using model organisms such as the budding yeast Saccharomyces cerevisiae. To assess the conservation and variation of this process over a broad evolutionary distance, we explored the meiotic recombination landscape in Lachancea kluyveri, a budding yeast species that diverged from S. cerevisiae more than 100 million years ago. The meiotic recombination map we generated revealed that the meiotic recombination landscape and properties significantly vary across distantly related yeast species, supporting that recombination hotspots conservation across yeast species is likely associated to the conservation of synteny. Finally, the frequent meiotic reversions we observed led us to re-evaluate their evolutionary importance.


Genetics ◽  
1997 ◽  
Vol 145 (3) ◽  
pp. 661-670 ◽  
Author(s):  
Qing-Qing Fan ◽  
Fei Xu ◽  
Michael A White ◽  
Thomas D Petes

In a wild-type strain of Saccharomyces cerevisiae, a hotspot for meiotic recombination is located upstream of the HIS4 gene. An insertion of a 49-bp telomeric sequence into the coding region of HIS4 strongly stimulates meiotic recombination and the local formation of meiosis-specific double-strand DNA breaks (DSBs). When strains are constructed in which both hotspots are heterozygous, hotspot activity is substantially less when the hotspots are on the same chromosome than when they are on opposite chromosomes.



1996 ◽  
Vol 16 (6) ◽  
pp. 2878-2887 ◽  
Author(s):  
X Liu ◽  
J Bowen ◽  
M A Gorovsky

H2A.F/Z histones are conserved variants that diverged from major H2A proteins early in evolution, suggesting they perform an important function distinct from major H2A proteins. Antisera specific for hv1, the H2A.F/Z variant of the ciliated protozoan Tetrahymena thermophila, cross-react with proteins from Saccharomyces cerevisiae. However, no H2A.F/Z variant has been reported in this budding yeast species. We sought to distinguish among three explanations for these observations: (i) that S. cerevisiae has an undiscovered H2A.F/Z variant, (ii) that the major S. cerevisiae H2A proteins are functionally equivalent to H2A.F/Z variants, or (iii) that the conserved epitope is found on a non-H2A molecule. Repeated attempts to clone an S. cerevisiae hv1 homolog only resulted in the cloning of the known H2A genes yHTA1 and yHTA2. To test for functional relatedness, we attempted to rescue strains lacking the yeast H2A genes with either the Tetrahymena major H2A genes (tHTA1 or tHTA2) or the gene (tHTA3) encoding hv1. Although they differ considerably in sequence from the yeast H2A genes, the major Tetrahymena H2A genes can provide the essential functions of H2A in yeast cells, the first such case of trans-species complementation of histone function. The Tetrahymena H2A genes confer a cold-sensitive phenotype. Although expressed at high levels and transported to the nucleus, hv1 cannot replace yeast H2A proteins. Proteins from S. cerevisiae strains lacking yeast H2A genes fail to cross-react with anti-hv1 antibodies. These studies make it likely that S. cerevisiae differs from most other eukaryotes in that it does not have an H2A.F/Z homolog. A hypothesis is presented relating the absence of H2A.F/Z in S. cerevisiae to its function in other organisms.



2021 ◽  
Author(s):  
Fabien Dutreux ◽  
Abhishek Dutta ◽  
Emilien Peltier ◽  
Sabrina Bibi-Triki ◽  
Anne Friedrich ◽  
...  

Meiotic recombination has been deeply characterized in a few model species only, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, most members of the ZMM pathway that implements meiotic crossover interference in S. cerevisiae have been lost in Lachancea yeast species after the divergence of Lachancea kluyveri from the rest of the clade. This suggests major differences in the control of crossover distribution. After investigating meiosis in L. kluyveri, we determined the meiotic recombination landscape of Lachancea waltii and identified several characteristics that should help understand better the underlying mechanisms. Such characteristics include systematic regions of loss of heterozygosity (LOH) in L. waltii hybrids, compatible with dysregulated Spo11-mediated DNA double strand breaks (DSB) independently of meiosis. They include a higher recombination rate in L. waltii than in L. kluyveri despite the lack of multiple ZMM pro-crossover factors. L. waltii exhibits an elevated frequency of zero-crossover bivalents as L. kluyveri but opposite to S. cerevisiae. L. waltii gene conversion tracts lengths are comparable to those observed in S. cerevisiae and shorter than in L. kluyveri despite the lack of Mlh2, a factor limiting conversion tracts size in S. cerevisiae. L. waltii recombination hotspots are not shared with either S. cerevisiae or L. kluyveri, showing that meiotic recombination hotspots can evolve at a rather limited evolutionary scale within budding yeasts. Finally, in line with the loss of several ZMM genes, we found only residual crossover interference in L. waltii likely coming from the modest interference existing between recombination precursors.



Genetics ◽  
2003 ◽  
Vol 165 (1) ◽  
pp. 101-114 ◽  
Author(s):  
Stuart J Haring ◽  
George R Halley ◽  
Alex J Jones ◽  
Robert E Malone

Abstract This study addresses three questions about the properties of recombination hotspots in Saccharomyces cerevisiae: How much DNA is required for double-strand-break (DSB) site recognition? Do naturally occurring DSB sites compete with each other in meiotic recombination? What role does the sequence located at the sites of DSBs play? In S. cerevisiae, the HIS2 meiotic recombination hotspot displays a high level of gene conversion, a 3′-to-5′ conversion gradient, and two DSB sites located ∼550 bp apart. Previous studies of hotspots, including HIS2, suggest that global chromosome structure plays a significant role in recombination activity, raising the question of how much DNA is sufficient for hotspot activity. We find that 11.5 kbp of the HIS2 region is sufficient to partially restore gene conversion and both DSBs when moved to another yeast chromosome. Using a variety of different constructs, studies of hotspots have indicated that DSB sites compete with one another for DSB formation. The two naturally occurring DSBs at HIS2 afforded us the opportunity to examine whether or not competition occurs between these native DSB sites. Small deletions of DNA at each DSB site affect only that site; analyses of these deletions show no competition occurring in cis or in trans, indicating that DSB formation at each site at HIS2 is independent. These small deletions significantly affect the frequency of DSB formation at the sites, indicating that the DNA sequence located at a DSB site can play an important role in recombination initiation.



2000 ◽  
Vol 97 (21) ◽  
pp. 11383-11390 ◽  
Author(s):  
J. L. Gerton ◽  
J. DeRisi ◽  
R. Shroff ◽  
M. Lichten ◽  
P. O. Brown ◽  
...  


2006 ◽  
Vol 172 (6) ◽  
pp. 861-874 ◽  
Author(s):  
Jessica D. Tytell ◽  
Peter K. Sorger

Accurate chromosome segregation during mitosis requires biorientation of sister chromatids on the microtubules (MT) of the mitotic spindle. Chromosome–MT binding is mediated by kinetochores, which are multiprotein structures that assemble on centromeric (CEN) DNA. The simple CENs of budding yeast are among the best understood, but the roles of kinesin motor proteins at yeast kinetochores have yet to be determined, despite evidence of their importance in higher eukaryotes. We show that all four nuclear kinesins in Saccharomyces cerevisiae localize to kinetochores and function in three distinct processes. Kip1p and Cin8p, which are kinesin-5/BimC family members, cluster kinetochores into their characteristic bilobed metaphase configuration. Kip3p, a kinesin-8,-13/KinI kinesin, synchronizes poleward kinetochore movement during anaphase A. The kinesin-14 motor Kar3p appears to function at the subset of kinetochores that become detached from spindle MTs. These data demonstrate roles for structurally diverse motors in the complex processes of chromosome segregation and reveal important similarities and intriguing differences between higher and lower eukaryotes.



1997 ◽  
Vol 17 (12) ◽  
pp. 7029-7039 ◽  
Author(s):  
D K Nag ◽  
M P Koonce ◽  
J Axelrod

During meiosis, a diploid cell undergoes two rounds of nuclear division following one round of DNA replication to produce four haploid gametes. In yeast, haploid meiotic products are packaged into spores. To gain new insights into meiotic development and spore formation, we followed differential expression of genes in meiotic versus vegetatively growing cells in the yeast Saccharomyces cerevisiae. Our results indicate that there are at least five different classes of transcripts representing genes expressed at different stages of the sporulation program. Here we describe one of these differentially expressed genes, SSP1, which plays an essential role in meiosis and spore formation. SSP1 is expressed midway through meiosis, and homozygous ssp1 diploid cells fail to sporulate. In the ssp1 mutant, meiotic recombination is normal but viability declines rapidly. Both meiotic divisions occur at the normal time; however, the fraction of cells completing meiosis is significantly reduced, and nuclei become fragmented soon after meiosis II. The ssp1 defect does not appear to be related to a microtubule-cytoskeletal-dependent event and is independent of two rounds of chromosome segregation. The data suggest that Ssp1 is likely to function in a pathway that controls meiotic nuclear divisions and coordinates meiosis and spore formation.



2014 ◽  
Vol 25 (19) ◽  
pp. 2934-2947 ◽  
Author(s):  
Ping Li ◽  
Hui Jin ◽  
Hong-Guo Yu

During meiosis, homologues are linked by crossover, which is required for bipolar chromosome orientation before chromosome segregation at anaphase I. The repetitive ribosomal DNA (rDNA) array, however, undergoes little or no meiotic recombination. Hyperrecombination can cause chromosome missegregation and rDNA copy number instability. We report here that condensin, a conserved protein complex required for chromosome organization, regulates double-strand break (DSB) formation and repair at the rDNA gene cluster during meiosis in budding yeast. Condensin is highly enriched at the rDNA region during prophase I, released at the prophase I/metaphase I transition, and reassociates with rDNA before anaphase I onset. We show that condensin plays a dual role in maintaining rDNA stability: it suppresses the formation of Spo11-mediated rDNA breaks, and it promotes DSB processing to ensure proper chromosome segregation. Condensin is unnecessary for the export of rDNA breaks outside the nucleolus but required for timely repair of meiotic DSBs. Our work reveals that condensin coordinates meiotic recombination with chromosome segregation at the repetitive rDNA sequence, thereby maintaining genome integrity.



2019 ◽  
Author(s):  
Paula Alonso-Ramos ◽  
David Álvarez-Melo ◽  
Katerina Strouhalova ◽  
Carolina Pascual-Silva ◽  
George B. Garside ◽  
...  

AbstractMeiotic defects derived from incorrect DNA repair during gametogenesis can lead to mutations, aneuploidies and infertility. Effective and coordinated resolution of meiotic recombination intermediates is necessary to accomplish both rounds of successful chromosome segregation. Cdc14 is an evolutionarily conserved dual-specificity phosphatase required for mitotic exit and meiotic progression. Mutations that inactivate the phosphatase lead to meiotic failure. Here, we have identified previously undescribed roles of Cdc14 in ensuring correct meiotic recombination. We found that recombination intermediates accumulate during prophase I when Cdc14 is depleted. Furthermore, Cdc14 plays a role in correct homolog disjunction at the end of anaphase I, both by modulating the timely removal of arm-cohesion between sister chromatids and by promoting elimination of SPO11-dependent entanglements. We also demonstrate that Cdc14 is required for correct sister chromatid segregation during the second meiotic division, independent of centromeric cohesion but dependent on the correct reduplication of SPBs during meiosis II, and on the activity of the Holliday Junction resolvase Yen1/GEN1. Timely activation of Yen1/GEN1 in anaphase I and II is impaired in the meiosis defective allele, cdc143HA. Based on these new findings, we propose previously undescribed functions of Cdc14 in the regulation of meiotic recombination; roles that are independent of sister chromatid cohesion, spindle dynamics and the metabolism of gamete morphogenesis.Author SummaryMeiotic recombination is fundamental for sexual reproduction, with efficient and orchestrated resolution of recombination intermediates critical for correct chromosome segregation. Homologous recombination is initiated by the introduction of programmed DNA Double-Strand Breakds (DSBs) followed by the formation of complex branched DNA intermediates, including double Holliday Junctions (dHJs). These recombination intermediates are eventually repaired into crossover or non-crossover products. In some cases, unresolved recombination intermediates, or toxic repair products, might persist until the metaphase to anaphase transition, requiring a set of late-acting repair enzymes to process them. Unrestrained activity of these enzymes, however, is equally detrimental for genome integrity, thus several layers of regulation tightly control them. For example, in budding yeast meiosis, Yen1/GEN1 is mainly activated during the second meiotic division, although how it is activated is unknown. Here, we have identified that the phosphatase Cdc14 is required during meiotic divisions for timely nuclear localization and activation of Yen1 in budding yeast meiosis. Additionally, we have been able to identify previously undescribed roles of Cdc14 in controlling meiotic recombination. Strikingly, we found that levels of recombination intermediates increase during prophase I in cdc14 meiotic deficient cells, indicating that Cdc14 plays a direct role in monitoring meiotic DSB repair, possibly in Yen1-independent manner. Resolution of recombination intermediates in the absence of Cdc14 is dependent on SGS1 and MUS81/MMS4, otherwise accumulating different types of aberrant recombination intermediates and a highly reduced efficiency in CO formation. Deficient resolution of JMs in cdc14 meiotic cells, together with difficulties in SPB reduplication, likely contribute to the missegregation problems observed during the second meiotic division.



Genetics ◽  
1990 ◽  
Vol 126 (4) ◽  
pp. 1127-1138 ◽  
Author(s):  
J S King ◽  
R K Mortimer

Abstract A model of chiasma interference is proposed and simulated on a computer. The model uses random events and a polymerization reaction to regulate meiotic recombination between and along chromosomes. A computer simulation of the model generates distributions of crossovers per chromosome arm, position of events along the chromosome arm, distance between crossovers in two-event tetrads, and coincidence as a function of distance. Outputs from the simulation are compared to data from Saccharomyces cerevisiae and the X chromosome of Drosophila melanogaster. The simulation demonstrates that the proposed model can produce the regulation of recombination observed in both genetic and cytological experiments. While the model was quantitatively compared to data from only Drosophila and Saccharomyces, the regulation observed in these species is qualitatively similar to the regulation of recombination observed in other organisms.



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