SCC3 is an axial element essential for homologous chromosome pairing and synapsis
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eLife assessment
This important study elucidates the function of the cohesin subunit SCC3 in impeding DNA repair between inter-sister chromatids in rice. The observation of sterility in the SCC3 weak mutant prompted an investigation of abnormal chromosome behavior during anaphase I through karyotype analysis. While the evidence presented is largely solid, the strength of support can be substantially improved in some aspects, leaving room for further investigation. This research contributes to our understanding of meiosis in rice and attracts cell biologists, reproductive biologists, and plant geneticists.
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Abstract
Cohesin is a multi-subunit protein that plays a pivotal role in holding sister chromatids together during cell division. Sister chromatid cohesion 3 (SCC3), constituents of cohesin complex, is highly conserved from yeast to mammals. Since the deletion of individual cohesin subunit always causes lethality, it is difficult to dissect its biological function in both mitosis and meiosis. Here, we obtained scc3 weak mutants using CRISPR-Cas9 system to explore its function during rice mitosis and meiosis. The scc3 weak mutants displayed obvious vegetative defects and complete sterility, underscoring the essential roles of SCC3 in both mitosis and meiosis. SCC3 is localized on chromatin from interphase to prometaphase in mitosis. However, in meiosis, SCC3 acts as an axial element during early prophase I and subsequently situates onto centromeric regions following the disassembly of the synaptonemal complex. The loading of SCC3 onto meiotic chromosomes depends on REC8. scc3 shows severe defects in homologous pairing and synapsis. Consequently, SCC3 functions as an axial element that is essential for maintaining homologous chromosome pairing and synapsis during meiosis.
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eLife assessment
This important study elucidates the function of the cohesin subunit SCC3 in impeding DNA repair between inter-sister chromatids in rice. The observation of sterility in the SCC3 weak mutant prompted an investigation of abnormal chromosome behavior during anaphase I through karyotype analysis. While the evidence presented is largely solid, the strength of support can be substantially improved in some aspects, leaving room for further investigation. This research contributes to our understanding of meiosis in rice and attracts cell biologists, reproductive biologists, and plant geneticists.
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Reviewer #1 (Public Review):
Summary:
The manuscript describes the identification and characterization of rice SCC3, including the generation and characterization of plants containing apparently lethal null mutations in SCC3 as well as mutant plants containing a c-terminal frame-shift mutation. The weak scc3 mutants showed both vegetative and reproductive defects. Specifically, mitotic chromosomes appeared to partially separate during prometaphase, while meiotic chromosomes were diffuse during early meiosis and showed alterations in sister chromatid cohesion, homologous chromosome pairing, and recombination. The authors suggest that SCC3 acts as a cohesin subunit in mitosis and meiosis, but also plays more functions other than just cohesion.Strengths:
The manuscript contains a large amount of generally high-quality data.Weaknesses:
Reviewer #1 (Public Review):
Summary:
The manuscript describes the identification and characterization of rice SCC3, including the generation and characterization of plants containing apparently lethal null mutations in SCC3 as well as mutant plants containing a c-terminal frame-shift mutation. The weak scc3 mutants showed both vegetative and reproductive defects. Specifically, mitotic chromosomes appeared to partially separate during prometaphase, while meiotic chromosomes were diffuse during early meiosis and showed alterations in sister chromatid cohesion, homologous chromosome pairing, and recombination. The authors suggest that SCC3 acts as a cohesin subunit in mitosis and meiosis, but also plays more functions other than just cohesion.Strengths:
The manuscript contains a large amount of generally high-quality data.Weaknesses:
Several of the conclusions drawn in the manuscript are not supported by the data. There are many examples where the authors either draw conclusions or make statements that are just not justified based on the data presented or present a conclusion as a new finding, which has already been demonstrated in the past by others. For example, they claim that SCC3 functions in the maintenance of replication. From my reading of the manuscript, nowhere did the authors examine DNA replication. Likewise, several of the conclusions drawn are in direct contrast with what is known about SCC3 in other organisms. Therefore, the conclusions are either groundbreaking or incorrect. -
Reviewer #2 (Public Review):
Summary:
This manuscript shows detailed evidence of the role of cohesin regulators in rice meiosis and mitosis.Strengths:
There is a very clear mechanism for its role during replication. The strength of the evidence and its novelty is very high. This paper makes a significant contribution to the body of knowledge on meiotic cohesion in a valuable plant model.Weaknesses:
The authors did not consider creating heterozygous mutants for the replication fork.
Moderate English language editing may be required. -
Reviewer #3 (Public Review):
Summary:
Prior research on SCC3, a cohesin subunit protein, in yeast and Arabidopsis has underscored its vital role in cell division. This study investigated into the specific functions of SCC3 in rice mitosis and meiosis. In a weakened SCC3 mutant, sister chromatids separating was observed in anaphase I, resulting in 24 univalents and subsequent sterility. The authors meticulously documented SCC3's loading and degradation dynamics on chromosomes, noting its impact on DNA replication. Despite the loss of homologous chromosome pairing and synapsis in the mutant, chromosomes retained double-strand breaks without fragmenting. Consequently, the authors inferred that in the scc3 mutant, DNA repair more frequently relies on sister chromatids as templates compared to the wild type.Strengths:
The study presents …Reviewer #3 (Public Review):
Summary:
Prior research on SCC3, a cohesin subunit protein, in yeast and Arabidopsis has underscored its vital role in cell division. This study investigated into the specific functions of SCC3 in rice mitosis and meiosis. In a weakened SCC3 mutant, sister chromatids separating was observed in anaphase I, resulting in 24 univalents and subsequent sterility. The authors meticulously documented SCC3's loading and degradation dynamics on chromosomes, noting its impact on DNA replication. Despite the loss of homologous chromosome pairing and synapsis in the mutant, chromosomes retained double-strand breaks without fragmenting. Consequently, the authors inferred that in the scc3 mutant, DNA repair more frequently relies on sister chromatids as templates compared to the wild type.Strengths:
The study presents exceptionally well-executed research in the field of rice cytogenetics.Weaknesses:
While the paper's conclusions are generally well-supported, further substantiation is needed for the claim that SCC3 inhibits template choice for sister chromatids. To bolster this conclusion, I recommend that the authors perform whole-genome sequencing on parental and F1 individuals from two rice variants, subsequently calculating the allele frequencies at heterozygous sites in the F1 individuals. If SCC3 indeed inhibits inter-sister chromatid repair in the wild type, we would anticipate a higher frequency of inter-homologous chromosome repair (i.e., gene conversion). This should be manifested as a bias away from the Mendelian inheritance ratio (50:50) in the offspring of the wild type compared to the offspring of the scc3+/- mutant. -