A Multiprotein Complex Regulates Interference-Sensitive Crossover Formation in Rice

Zhang, Jie; Wang, Chong; Higgins, James D.; Kim, Yujin; Moon, Sunok; Jung, Ki‐Hong; Qu, Shuying; Liang, Wanqi

doi:10.1104/pp.19.00082

Cited by 19 publications

(20 citation statements)

References 67 publications

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“…Fluorescent in situ hybridization (FISH) assay was performed as described ( Cheng, 2013 ). The sequences of the centromere and 5 S rDNA FISH probes were designed and labeled as described ( Mizuno et al, 2006 ; Zhang et al, 2019 ). Images were captured with an Eclipse Ni-E microscope and NIS elements software (Nikon).…”

Section: Methodsmentioning

confidence: 99%

Rice OsBRCA2 Is Required for DNA Double-Strand Break Repair in Meiotic Cells

Wang

Shen

et al. 2020

Front. Plant Sci.

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The mammalian BREAST CANCER 2 ( BRCA2 ) gene is a tumor suppressor that plays a crucial role in DNA repair and homologous recombination (HR). Here, we report the identification and characterization of OsBRCA2 , the rice orthologue of human BRCA2 . Osbrca2 mutant plants exhibit normal vegetative growth but experience complete male and female sterility as a consequence of severe meiotic defects. Pairing, synapsis and recombination are impaired in osbrca2 male meiocytes, leading to chromosome entanglements and fragmentation. In the absence of OsBRCA2, localization to the meiotic chromosome axes of the strand-invasion proteins OsRAD51 and OsDMC1 is severely reduced and in vitro OsBRCA2 directly interacts with OsRAD51 and OsDMC1. These results indicate that OsBRCA2 is essential for facilitating the loading of OsRAD51 and OsDMC1 onto resected ends of programmed double-strand breaks (DSB) during meiosis to promote single-end invasions of homologous chromosomes and accurate recombination. In addition, treatment of osbrca2-1 seedlings with mitomycin C (MMC) led to hypersensitivity. As MMC is a genotoxic agent that creates DNA lesions in the somatic cells that can only be repaired by HR, these results suggest that OsBRCA2 has a conserved role in DSB repair and HR in rice.

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Section: Methodsmentioning

confidence: 99%

Rice OsBRCA2 Is Required for DNA Double-Strand Break Repair in Meiotic Cells

Wang

Shen

et al. 2020

Front. Plant Sci.

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“…In rice (Oryza sativa), MutSg promotes formation of the obligate CO and is required for 78% to 90% of chiasmata (Luo et al, 2013;Zhang et al, 2014;Wang et al, 2016). In addition, a direct physical association between OsMSH4 and OsMSH5 as well as between OsMSH5 and HEI10 was demonstrated using yeast two-hybrid and pull-down assays (Zhang et al, 2014), as were interactions between OsMSH5 and replication protein A family members (OsRPA1a, OsRPA2b, OsRPA1c, and OsRPA2c; Wang et al, 2016) and OsSHOC1 (Zhang et al, 2019). In Arabidopsis and rice mutSg mutants, immunolocalization of the synaptonemal complex transverse filament proteins appeared normal, indicating a minimal effect on synapsis during prophase I (Higgins et al, 2004;Luo et al, 2013;Zhang et al, 2014).…”

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confidence: 98%

MutS homologue 4 and MutS homologue 5 Maintain the Obligate Crossover in Wheat Despite Stepwise Gene Loss following Polyploidization

et al. 2020

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Crossovers (COs) ensure accurate chromosome segregation during meiosis while creating novel allelic combinations. Here, we show that allotetraploid (AABB) durum wheat (Triticum turgidum ssp. durum) utilizes two pathways of meiotic recombination. The class I pathway requires MSH4 and MSH5 (MutSg) to maintain the obligate CO/chiasma and accounts for ;85% of meiotic COs, whereas the residual ;15% are consistent with the class II CO pathway. Class I and class II chiasmata are skewed toward the chromosome ends, but class II chiasmata are significantly more distal than class I chiasmata. Chiasma distribution does not reflect the abundance of double-strand breaks, detected by proxy as RAD51 foci at leptotene, but only ;2.3% of these sites mature into chiasmata. MutSg maintains the obligate chiasma despite a 5.4-kb deletion in MSH5B rendering it nonfunctional, which occurred early in the evolution of tetraploid wheat and was then domesticated into hexaploid (AABBDD) common wheat (Triticum aestivum), as well as an 8-kb deletion in MSH4D in hexaploid wheat, predicted to create a nonfunctional pseudogene. Stepwise loss of MSH5B and MSH4D following hybridization and whole-genome duplication may have occurred due to gene redundancy (as functional copies of MSH5A, MSH4A, and MSH4B are still present in the tetraploid and MSH5A, MSH5D, MSH4A, and MSH4B are present in the hexaploid) or as an adaptation to modulate recombination in allopolyploid wheat.

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“…23 In Arabidopsis and rice, knock-out of SHOC1 can lead to a striking reduction in the number of meiotic crossovers. [24][25][26] In mice, it is demonstrated that Mzip2 knock-out male and female mice are sterile. Spermatogenesis in Mzip2 −/− mice arrests at zygotene stage, and there is no SC assembly and expression of MLH1 loci in the Mzip2 deficiency spermatocytes.…”

Section: Discussionmentioning

confidence: 99%

Bi-allelic SHOC1 loss-of-function mutations cause meiotic arrest and non-obstructive azoospermia

et al. 2020

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BackgroundThe genetic causes of human idiopathic non-obstructive azoospermia (NOA) with meiotic arrest remain unclear.MethodsTwo Chinese families with infertility participated in the study. In family 1, two brothers were affected by idiopathic NOA. In family 2, the proband was diagnosed with idiopathic NOA, and his elder sister suffered from infertility. Whole-exome sequencing (WES) was conducted in the two patients in family 1, the proband in family 2 and 362 additional sporadic patients with idiopathic NOA. Sanger sequencing was used to verify the WES results. Periodic acid–Schiff (PAS), immunohistochemistry (IHC) and meiotic chromosomal spread analyses were carried out to evaluate the stage of spermatogenesis arrested in the affected cases.ResultsWe identified compound heterozygous loss of function (LoF) variants of SHOC1 (c.C1582T:p.R528X and c.231_232del:p.L78Sfs*9, respectively) in both affected cases with NOA from family 1. In family 2, homozygous LoF variant in SHOC1 (c.1194delA:p.L400Cfs*7) was identified in the siblings with infertility. PAS, IHC and meiotic chromosomal spread analyses demonstrated that the spermatogenesis was arrested at zygotene stage in the three patients with NOA. Consistent with the autosomal recessive mode of inheritance, all of these SHOC1 variants were inherited from heterozygous parental carriers. Intriguingly, WES of 362 sporadic NOA cases revealed one additional NOA case with a bi-allelic SHOC1 LoF variant (c.1464delT:p.D489Tfs*13).ConclusionTo the best of our knowledge, this is the first report identifying SHOC1 as the causative gene for human NOA. Furthermore, our study showed an autosomal recessive mode of inheritance in the NOA caused by SHOC1 deficiency.

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A Multiprotein Complex Regulates Interference-Sensitive Crossover Formation in Rice

Abstract: Complementation of osshoc1-2For the complementation test, the genomic sequence of OsSHOC1 containing 2505 bp upstream of the start codon, the coding region, and 131 bp downstream 232

Cited by 19 publications

References 67 publications

Rice OsBRCA2 Is Required for DNA Double-Strand Break Repair in Meiotic Cells

Rice OsBRCA2 Is Required for DNA Double-Strand Break Repair in Meiotic Cells

MutS homologue 4 and MutS homologue 5 Maintain the Obligate Crossover in Wheat Despite Stepwise Gene Loss following Polyploidization

Bi-allelic SHOC1 loss-of-function mutations cause meiotic arrest and non-obstructive azoospermia

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