MEIOTIC F-BOX Is Essential for Male Meiotic DNA Double-Strand Break Repair in Rice

He, Yi; Wang, Chong; Higgins, James D.; Yu, Junping; Zong, Jie; Lu, Pingli; Zhang, Dabing; Liang, Wanqi

doi:10.1105/tpc.16.00108

Cited by 54 publications

(45 citation statements)

References 86 publications

(100 reference statements)

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“…From our data and extensive literature we can speculate a model wherein the serine-rich duplicated region destabilizes the ASY3 TD protein and may target the protein for degradation by the proteasome [35, [38][39][40]. A destabilized protein may be hypomorphic to the ancestral ASY3 ND allele as there less protein may be available to bind to the chromosome axes and/or it could be less effective at promoting interhomolog recombination when bound at the axis.…”

Section: Discussionmentioning

confidence: 93%

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Seear

Gregory

Heavens

et al. 2019

Preprint

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In this study we performed a genotype-phenotype association analysis of meiotic stability in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and was associated with segregation of a novel allele orthologous to the budding yeast RED1 chromosome axis protein, Asynapsis3 (ASY3), derived from A. lyrata. The adaptive ASY3 protein possesses a putative in-frame tandem duplication (TD) of a serinerich region upstream of the coiled-coil domain that has arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than plants heterozygous for TD/ND (non-duplicated) ASY3 haplotypes. Chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachtyene that mark class I crossovers was significantly reduced in meiotic nuclei from ASY3 TD homozygous plants compared to ASY3 ND/TD heterozygotes, indicating an adaptive consequence of the ASY3 TD allele.From the ten populations, fifty-eight alleles of these 8 meiosis genes were identified, demonstrating dynamic population variability at these loci which nevertheless exhibit signatures of strong hard selective sweeps. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them. | P a g e Author summaryWhole genome duplication can promote adaptability, but is a dramatic mutation usually resulting in meiotic catastrophe and genome instability. Here we focus on a case of coordinated stabilization of meiotic recombination in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations from the Wachau region and East Austrian Forealps. We fuse population genomic data with a genotype-phenotype association study, concentrating on the effects of eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that a novel allele of the meiotic chromosome axis protein Asynapsis3 that contains an in-frame duplication of a serine-rich region is the major determinant of male meiotic stability. This adaptive restabilisation appears to be achieved by a...

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Section: Discussionmentioning

confidence: 93%

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Seear

Gregory

Heavens

et al. 2019

Preprint

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“…E3 ligases interact with target proteins to facilitate, directly or indirectly, modification of the substrate with ubiquitin—conferring substrate specificity to the ubiquitination cascade (Iconomou and Saunders, 2016). Several E3 ligases, and multi-subunit E3 ligase components, have been described with significant roles in meiosis in Arabidopsis (Yang et al , 1999, Wang and Yang, 2006; Yang et al , 2006), rice (He et al , 2016; Zhang et al , 2017), and wheat (Li et al , 2006; Hong et al , 2013). Further, enrichment of E3 ligases in pre-meiotic pollen mother cells has been reported in both rice (Tang et al , 2010) and maize (Yuan et al , 2018).…”

Section: Discussionmentioning

confidence: 99%

Time-resolved transcriptome of barley anthers and meiocytes reveals robust and largely stable gene expression changes at meiosis entry

Barakate

Orr

Schreiber

et al. 2020

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In flowering plants, successful germinal cell development and meiotic recombination depend upon a combination of environmental and genetic factors. To gain insights into this specialised reproductive development programme we used short- and long-read RNA-sequencing (RNA-seq) to study the temporal dynamics of transcript abundance in immuno-cytologically staged barley (Hordeum vulgare) anthers and meiocytes. We show that the most significant transcriptional changes occur at the transition from pre-meiosis to leptotene–zygotene, which is followed by largely stable transcript abundance throughout prophase I. Our analysis reveals that the developing anthers and meiocytes are enriched in long non-coding RNAs (lncRNAs) and that entry to meiosis is characterized by their robust and significant down regulation. Intriguingly, only 24% of a collection of putative meiotic gene orthologues showed differential transcript abundance in at least one stage or tissue comparison. Changes in the abundance of numerous transcription factors, representatives of the small RNA processing machinery, and post-translational modification pathways highlight the complexity of the regulatory networks involved. These developmental, time-resolved, and dynamic transcriptomes increase our understanding of anther and meiocyte development and will help guide future research.One sentence summaryAnalysis of RNA-seq data from meiotically staged barley anthers and meiocytes highlights the role of lncRNAs within a complex network of transcriptional and post-transcriptional regulation accompanied by a hiatus in differential gene expression during prophase I.The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Robbie Waugh (robbie.waugh@hutton.ac.uk)

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“…However, the ASK1-interacting F-box proteins and their substrates involved in meiosis remain unknown. MOF, another F-box protein required for meiosis, was previously demonstrated to interact with OSK1 in rice (He et al, 2016). Unlike zygo1, however, the mof mutant is female fertile and its male meiocytes are arrested at prophase I.…”

Section: Zygo1 Promotes Bouquet Formation Within An Scf Complexmentioning

confidence: 99%

“…For example, the C. elegans F-box protein PROM-1 and the Arabidopsis SKP1 protein ASK1 have been shown to be required for meiotic progression Jantsch et al, 2007). Moreover, the MEIOTIC F-BOX (MOF) protein in rice (Oryza sativa) was reported to be necessary for male meiotic double-strand break (DSB) repair (He et al, 2016). However, the regulatory function of F-box proteins in zygotene chromosome reorganization and bouquet formation remains enigmatic.…”

Section: Introductionmentioning

confidence: 99%

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

et al. 2017

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Telomere bouquet formation, a highly conserved meiotic event, plays an important role in homologous pairing and therefore progression of meiosis; however, the underlying molecular mechanism remains largely unknown. Here, we identified ZYGOTENE1 (ZYGO1), a novel F-box protein in rice (Oryza sativa), and verified its essential role in bouquet formation during early meiosis. In zygo1 mutants, zygotene chromosome aggregation and telomere clustering failed to occur. The suppressed telomere clustering in homologous pairing aberration in rice meiosis1 (pair1) zygo1 and rice completion of meiotic recombination (Oscom1) zygo1 double mutants, together with the altered localization of OsSAD1 (a SUN protein associated with the nuclear envelope) in zygo1, showed that ZYGO1 has a significant function in bouquet formation. In addition, the interaction between ZYGO1 and rice SKP1-like protein 1 suggested that ZYGO1 might modulate bouquet formation as a component of the SKP1-Cullin1-F-box complex. Although double-strand break formation and early recombination element installation occurred normally, zygo1 mutants showed defects in full-length pairing and synaptonemal complex assembly. Furthermore, crossover (CO) formation was disturbed, and foci of Human enhancer of invasion 10 were restricted to the partially synapsed chromosome regions, indicating that CO reduction might be caused by the failure of full-length chromosome alignment in zygo1. Therefore, we propose that ZYGO1 mediates bouquet formation to efficiently promote homolog pairing, synapsis, and CO formation in rice meiosis.

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MEIOTIC F-BOX Is Essential for Male Meiotic DNA Double-Strand Break Repair in Rice

Cited by 54 publications

References 86 publications

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Time-resolved transcriptome of barley anthers and meiocytes reveals robust and largely stable gene expression changes at meiosis entry

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

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