Increasing the Genetic Recombination Frequency by Partial Loss of Function of the Synaptonemal Complex in Rice

Wang, Kejian; Liu, Qing; Liu, Wenzhen; Fu, Yaping

doi:10.1016/j.molp.2015.04.011

Cited by 31 publications

(23 citation statements)

References 9 publications

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“…From late pachytene to diplotene, HEI10 and HEIP1 foci almost completely colocalized in all wild-type nuclei observed. Furthermore, previous studies showed that in zep1 mutants, HEI10 foci (class I COs) increased ∼1.5-fold compared with that in wild type, which was further confirmed by genetic analysis (27). We found that HEI10 prominent foci always colocalized with HEIP1 in zep1 mutants.…”

Section: Discussionsupporting

confidence: 87%

HEIP1 regulates crossover formation during meiosis in rice

Qin

Shen

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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During meiosis, the number of double-strand breaks (DSBs) far exceeds the final number of crossovers (COs). Therefore, to identify proteins involved in determining which of these DSBs repaired into COs is critical in understanding the mechanism of CO control. Across species, HEI10-related proteins play important roles in CO formation. Here, through screening for HEI10-interacting proteins via a yeast two-hybrid system, we identify a CO protein HEI10 Interaction Protein 1 (HEIP1) in rice. HEIP1 colocalizes with HEI10 in a dynamic fashion along the meiotic chromosomes and specially localizes onto crossover sites from late pachytene to diplotene. Between these two proteins, HEI10 is required for the loading of HEIP1, but not vice versa. Moreover, mutations of the HEIP1 gene cause the severe reduction of chiasma frequency, whereas early homologous recombination processes are not disturbed and synapsis proceeds normally. HEIP1 interacts directly with ZIP4 and MSH5. In addition, the loading of HEIP1 depends on ZIP4, but not on MER3, MSH4, or MSH5. Together, our results suggest that HEIP1 may be a member of the ZMM group and acts as a key element regulating CO formation.

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Section: Discussionsupporting

confidence: 87%

HEIP1 regulates crossover formation during meiosis in rice

Qin

Shen

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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“…The data we present here hone in on the SC itself, independent of any procrossover activity, as the relevant molecular entity that is linked to limiting MutSg-mediated interhomolog crossing over. Taken together with recent studies that have observed excess crossing over caused by alterations in the abundance or structure of SC components in C. elegans and rice (Libuda et al 2013;Wang et al 2015), our data add weight to the idea that a conserved role of the SC structure is to limit interhomolog recombination. …”

supporting

confidence: 82%

“…In budding yeast it is thought that at least some SC proteins facilitate early steps in interhomolog recombination that may occur prior to the elaboration of full-length SC (Storlazzi et al 1996;Hunter and Kleckner 2001;Borner et al 2004) leaving open the question of whether the mature SC is required at all for crossover formation. Recent genetic data from Caenorhabditis elegans and rice, on the other hand, have raised the paradox that while SC components are essential for meiotic crossovers, strains partially depleted for SC protein activity exhibit an increase in crossovers (Libuda et al 2013;Wang et al 2015). These observations indicate that SC proteins are associated with both positive and negative roles in crossing over, but it remains unknown how the pro-and anticrossover functions attributed to SC components in these organisms are related to one another at the molecular level.…”

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confidence: 99%

Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSγ-Mediated Crossover Formation

et al. 2016

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During meiosis, crossover recombination creates attachments between homologous chromosomes that are essential for a precise reduction in chromosome ploidy. Many of the events that ultimately process DNA repair intermediates into crossovers during meiosis occur within the context of homologous chromosomes that are tightly aligned via a conserved structure called the synaptonemal complex (SC), but the functional relationship between SC and crossover recombination remains obscure. There exists a widespread correlation across organisms between the presence of SC proteins and successful crossing over, indicating that the SC or its building block components are procrossover factors . For example, budding yeast mutants missing the SC transverse filament component, Zip1, and mutant cells missing the Zip4 protein, which is required for the elaboration of SC, fail to form MutSg-mediated crossovers. Here we report the reciprocal phenotype-an increase in MutSg-mediated crossovers during meiosis-in budding yeast mutants devoid of the SC central element components Ecm11 or Gmc2, and in mutants expressing a version of Zip1 missing most of its N terminus. This novel phenotypic class of SC-deficient mutants demonstrates unequivocally that the tripartite SC structure is dispensable for MutSg-mediated crossover recombination in budding yeast. The excess crossovers observed in SC central element-deficient mutants are Msh4, Zip1, and Zip4 dependent, clearly indicating the existence of two classes of SC proteins-a class with procrossover function(s) that are also necessary for SC assembly and a class that is not required for crossover formation but essential for SC assembly. The latter class directly or indirectly limits MutSg-mediated crossovers along meiotic chromosomes. Our findings illustrate how reciprocal roles in crossover recombination can be simultaneously linked to the SC structure.KEYWORDS synapsis; crossover recombination; budding yeast T HE synaptonemal complex (SC) is correlated with successful interhomolog crossover formation during meiosis; mutants missing SC components nearly always exhibit a decrease in crossovers and (as a consequence) increased errors in chromosome segregation at meiosis I (Page and Hawley 2004). Transverse filaments establish a prominent component of the typically tripartite SC structure; transverse filaments are composed of coiled-coil proteins that form rod-like entities that orient perpendicular to the long axis of aligned chromosomes, bridging chromosome axes at a distance of 100 nm along the entire length of the chromosome pair (Page and Hawley 2004). The largely coiled-coil Zip1 protein is a major (and perhaps the only) transverse filament protein of the budding yeast SC (Sym et al. 1993;Dong and Roeder 2000) ( Figure 1A).Budding yeast mutants that are missing the SC transverse filament protein Zip1 lack MutSg-mediated crossovers (Novak et al. 2001;Borner et al. 2004;Voelkel-Meiman et al. 2015). Furthermore, crossover levels in double mutants missing Zip1 and any of the so-called s...

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“…3A), from 389 ± 18 cM in wild type to 3,037 ± 115 cM in figl1 recq4 (translating to 7.8 ± 0.4 and 60.7 ± 2.3 COs per meiosis, respectively). This is much higher than the greatest increase in meiotic recombination observed so far in any mutant (15)(16)(17). While Arabidopsis wild type had a very typical frequency of CO, with the genetic maps of each of the five chromosomes ranging from 70 to 110 cM (an average of 1.6 CO per chromosome), the figl1 recq4 was almost the highest recombining eukaryote (Fig.…”

Section: Significancementioning

confidence: 81%

Unleashing meiotic crossovers in hybrid plants

Fernandes

Séguéla-Arnaud

Larchevêque

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

159

161

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Meiotic crossovers shuffle parental genetic information, providing novel combinations of alleles on which natural or artificial selection can act. However, crossover events are relatively rare, typically one to three exchange points per chromosome pair. Recent work has identified three pathways limiting meiotic crossovers in that rely on the activity of FANCM [Crismani W, et al. (2012) 336:1588-1590], RECQ4 [Séguéla-Arnaud M, et al. (2015) 112:4713-4718], and FIGL1 [Girard C, et al. (2015) 11:e1005369]. Here we analyzed recombination in plants in which one, two, or all three of these pathways were disrupted in both pure line and hybrid contexts. The greatest effect was observed when combining and mutations, which increased the hybrid genetic map length from 389 to 3,037 cM. This corresponds to an unprecedented 7.8-fold increase in crossover frequency. Disrupting the three pathways did not further increase recombination, suggesting that some upper limit had been reached. The increase in crossovers is not uniform along chromosomes and rises from centromere to telomere. Finally, although in wild type recombination is much higher in male meiosis than in female meiosis (490 cM vs. 290 cM), female recombination is higher than male recombination in (3,200 cM vs. 2,720 cM), suggesting that the factors that make wild-type female meiosis less recombinogenic than male wild-type meiosis do not apply in the mutant context. The massive increase in recombination observed in hybrids opens the possibility of manipulating recombination to enhance plant breeding efficiency.

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Increasing the Genetic Recombination Frequency by Partial Loss of Function of the Synaptonemal Complex in Rice

Cited by 31 publications

References 9 publications

HEIP1 regulates crossover formation during meiosis in rice

HEIP1 regulates crossover formation during meiosis in rice

Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSγ-Mediated Crossover Formation

Unleashing meiotic crossovers in hybrid plants

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