The endonuclease homolog OsRAD1 promotes accurate meiotic double-strand break repair by suppressing non-homologous end joining

Hu, Qing; Tang, Ding; Wang, Hongjun; Shen, Yi; Chen, Xiaojun; Ji, Jianhui; Du, Guijie; Li, Yafei; Cheng, Zhihui

doi:10.1104/pp.16.00831

Cited by 16 publications

(18 citation statements)

References 52 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Chromosome fragmentation is a characteristic phenomenon observed in mutants defective in DSB repair machinery. Our results showed that the Zmrad51c mutant phenotype is similar to that of the Osrad51c and Atrad51c mutants, as well as other related mutants such as Osxrcc3 [44], Osrad1 [81], Osrad17 [82], Atrad50 [83], and Atmre11 [84]. However, the severity of the chromosome segregation seems to be much less in Zmrad51c compared to the Osrad51c and Atrad51c mutants.…”

Section: Discussionsupporting

confidence: 63%

ZmRAD51C Is Essential for Double-Strand Break Repair and Homologous Recombination in Maize Meiosis

Jing

Zhang

Wang

et al. 2019

IJMS

View full text Add to dashboard Cite

Radiation sensitive 51 (RAD51) recombinases play crucial roles in meiotic double-strand break (DSB) repair mediated by homologous recombination (HR) to ensure the correct segregation of homologous chromosomes. In this study, we identified the meiotic functions of ZmRAD51C, the maize homolog of Arabidopsis and rice RAD51C. The Zmrad51c mutants exhibited regular vegetative growth but complete sterility for both male and female inflorescence. However, the mutants showed hypersensitivity to DNA damage by mitomycin C. Cytological analysis indicated that homologous chromosome pairing and synapsis were rigorously inhibited, and meiotic chromosomes were often entangled from diplotene to metaphase I, leading to chromosome fragmentation at anaphase I. Immunofluorescence analysis showed that although the signals of the axial element absence of first division (AFD1) and asynaptic1 (ASY1) were normal, the assembly of the central element zipper1 (ZYP1) was severely disrupted. The DSB formation was normal in Zmrad51c meiocytes, symbolized by the regular occurrence of γH2AX signals. However, RAD51 and disrupted meiotic cDNA 1 (DMC1) signals were never detected at the early stage of prophase I in the mutant. Taken together, our results indicate that ZmRAD51C functions crucially for both meiotic DSB repair and homologous recombination in maize.

show abstract

Section: Discussionsupporting

confidence: 63%

ZmRAD51C Is Essential for Double-Strand Break Repair and Homologous Recombination in Maize Meiosis

Jing

Zhang

Wang

et al. 2019

IJMS

View full text Add to dashboard Cite

show abstract

“…There has been much speculation regarding the fact that while there are typically 300 DSBs in a meiotic cycle in Arabidopsis or rice (Chelysheva et al ., ; Hu et al ., ), this greatly exceeds the number of crossover events that occur (Wijnker et al ., ; Liu et al ., ). Our data provide strong support for the view that at least some of the other DSB positions during meiosis are involved in GC events (Sun et al ., ; Chelysheva et al ., ; Lu et al ., ), where there is non‐reciprocal information transfer of genetic material from a donor to a recipient allele.…”

Section: Discussionmentioning

confidence: 94%

“…Homologous alleles of the SD1 gene and other height‐related genes have been reported in previous studies, e.g. Rht gene (‘green revolution’ gene in wheat) (Peng et al ., ), Sdw1 gene (‘green revolution’ gene in barley) (Xu et al ., ), GA5 gene (in Arabidopsis) (Barboza et al ., ), BR2 gene (in maize) (Multani, ), DW3 (in sorghum) (Multani, ), and PpeGID1c (in peach) (Hu et al ., ; Wang et al ., ). All of these genes carry several natural alleles and affect correspondingly obvious phenotypes.…”

Section: Discussionmentioning

confidence: 99%

“…While there are known to be around 300 DSB events in a meiotic cycle in Arabidopsis or rice (Chelysheva et al ., ; Hu et al ., ), this greatly exceeds the number of crossover events that occur (Wijnker et al ., ; Si et al ., ; Liu et al ., ), inspiring much speculation as to what happens at the other DSB positions during meiosis (de Massy, ). One leading hypothesis is that these additional DSBs during meiosis are involved in GC events (Sun et al ., ; Chelysheva et al ., ; Lu et al ., ).…”

Section: Introductionmentioning

confidence: 94%

See 1 more Smart Citation

High‐resolution insight into recombination events at the SD1 locus in rice

Jia

Zhang

et al. 2018

The Plant Journal

View full text Add to dashboard Cite

These authors contributed equally to this work. SUMMARYRecombination during meiosis plays an important role in genome evolution by reshuffling existing genetic variations into fresh combinations with the possibility of recovery of lost ancestral genotypes. While crossover (CO) events have been well studied, gene conversion events (GCs), which represent non-reciprocal information transfer between chromosomes, are poorly documented and difficult to detect due to their relatively small converted tract size. Here, we document these GC events and their phenotypic effects at an important locus in rice containing the SD1 gene, where multiple defective alleles contributed to the semidwarf phenotype of rice in the 'Green Revolution' of the 1960s. Here, physical separation of two defects allows recombination to generate the wild-type SD1 gene, for which plant height can then be used as a reporter. By screening 18 000 F 2 progeny from a cross between two semi-dwarf cultivars that carry these different defective alleles, we detected 24 GC events, indicating a conversion rate of~3.3 3 10 À4 per marker per generation in a single meiotic cycle in rice. Furthermore, our data show that indels and single-nucleotide polymorphisms (SNPs) do not differ significantly in GC rates, at least at the SD1 locus. Our results provide strong evidence that GC by itself can regain an ancestral phenotype that was lost through mutation. This GC detection approach is likely to be broadly applicable to natural or artificial alleles of other phenotyperelated functional genes, which are abundant in other plant genomes.

show abstract

“…Hus1 mutant female flies and worms are sterile [72,73], and Drosophila Hus1 is required for proper SC disassembly, and efficient DSB processing by HR [74]. In plants, both RAD1 and HUS1 promote accurate DSB repair during meiosis, in particular suppressing nonhomologous end-joining [75], and ZMM-independent CO formation between heterologues [76].…”

Section: Discussionmentioning

confidence: 99%

Separable roles of the DNA damage response kinase Mec1(ATR) and its activator Rad24(RAD17) within the regulation of meiotic recombination

Crawford

Cooper

Marsolier‐Kergoat

et al. 2018

Preprint

View full text Add to dashboard Cite

13 During meiosis, programmed DNA double-strand breaks (DSBs) are formed by the 14 topoisomerase-like enzyme, Spo11, activating the DNA damage response (DDR) kinase 15 Mec1 ATR via the checkpoint clamp loader, Rad24 RAD17 . At single loci, loss of Mec1 and Rad24 16 activity alters Spo11-dependent DSB formation and recombination outcome, but their genome-17 42 the generalised pathway, DNA damage leads to the activation of Tel1 ATM (Ataxia Telengiectasia-43 Mutated) and Mec1 ATR (Rad3-related) checkpoint kinases (Human orthologues are indicated 44with superscript text), via the Mre11-Rad50-Xrs2 NBS1 -complex and Rad24 RAD17 (reviewed in [2]). 45Rad24 RAD17 is the loader of the Ddc1 RAD9 -Rad17 RAD1 -Mec3 HUS1 ("9-1-1") checkpoint clamp, that 46 binds to the ssDNA/dsDNA junctions that arise following resection of DNA ends [3]. Tel1 ATM and 47 Mec1 ATR modulate downstream targets via Rad53 CHK2 [4], causing cell cycle arrest and the 48 modulation of transcription [5]. Notably, in mammalian cells, RAD17 and ATR have both 49 overlapping and distinct functions in the DDR. RAD17 is required for the recruitment of RAD9 50 after DNA damage, a function that it performs even in the absence of ATR [6]. Conversely, ATR 51 can localize to sites of DNA damage independently of RAD17, and can also be activated by 52 other factors such as RPA-coated ssDNA [7], suggesting separable and complementary roles 53 for ATR and RAD17.54 55 In meiosis, Spo11-DSBs initiate homologous recombination and are therefore essential for the 56 generation of crossovers (COs) between homologous chromosomes. In most organisms, 57 including mammals and S. cerevisiae, the organism utilised in the work presented here, such 58 recombination-dependent interactions facilitate homologue pairing during leptotene-zygotene, 59 full alignment and connection via the synaptonemal complex at pachytene, and subsequent 60 reductional chromosome segregation at the meiosis I nuclear division [8]. In S. cerevisiae 61 meiosis, similar to the vegetative DDR pathway, the 9-1-1 clamp complex, its loader Rad24, and 62 the Mre11-Rad50-Xrs2 complex act as damage sensors [9], with ssDNA, produced by the 63 resection of Spo11-DSBs, activating Mec1 [10]. By sensing ongoing recombination activity and 64 unrepaired DSBs, Mec1 acts as a molecular rheostat to modulate the progression of meiotic 65 prophase via the Ndt80 transcription factor, and the Mek1 kinase, a paralogue of Rad53 (CHK2 66 in mammals; [10-13]). Due to this transient checkpoint activation, Mec1 is able to prolong the 67 stage during which Spo11-DSB formation can occur [14], and both Mec1 and Rad24 promote 68 CO formation and suppress ectopic (non-allelic) recombination [15,16]. The interaction between 69 Mec1 and the 9-1-1 complex also contributes to other Mec1 functions such as phosphorylation 70 of the meiosis-specific chromosome axis protein, Hop1 (HORMAD1/2 in mammals [17]), which 71is important for the maintenance of homologue bias and chiasma formation [18,19]. In mammals, 72 Crawford et al. 2018 3 ATR local...

show abstract

The endonuclease homolog OsRAD1 promotes accurate meiotic double-strand break repair by suppressing non-homologous end joining

Cited by 16 publications

References 52 publications

ZmRAD51C Is Essential for Double-Strand Break Repair and Homologous Recombination in Maize Meiosis

ZmRAD51C Is Essential for Double-Strand Break Repair and Homologous Recombination in Maize Meiosis

High‐resolution insight into recombination events at the SD1 locus in rice

Separable roles of the DNA damage response kinase Mec1(ATR) and its activator Rad24(RAD17) within the regulation of meiotic recombination

Contact Info

Product

Resources

About