HEIP1 regulates crossover formation during meiosis in rice

Li, Yafei; Qin, Baoxiang; Shen, Yi; Zhang, Fanfan; Liu, Changzhen; You, Hanli; Du, Guijie; Tang, Ding; Cheng, Zhukuan

doi:10.1073/pnas.1807871115

Cited by 38 publications

(47 citation statements)

References 45 publications

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“…In addition, under our immunolocalisation conditions and as seen by others (Hurel et al, 2018;Li et al, 2018), HEI10 also localises to synapsed chromosome axes, emphasising that the partial synapsis observed in a single cdkg1-1 mutant is restored in a cdkg1-1fancm-1 double mutant (Supplemental Figure 2).…”

Section: Synapsis and Co Formation Are Restored In The Cdkg1-1 Fancm-supporting

confidence: 85%

CDKG1 Is Required for Meiotic and Somatic Recombination Intermediate Processing in Arabidopsis

et al. 2020

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Short title: The role of CDKG1 in recombinationOne-sentence summary: The cyclin-dependent kinase CDKG1 stabilises recombination intermediates during male meiosis and DNA damage-induced somatic homologous recombination. ABSTRACTThe Arabidopsis thaliana cyclin-dependent kinase G1 (CDKG1) is necessary for recombination and synapsis during male meiosis at high ambient temperature. In the cdkg1-1 mutant, synapsis is impaired and there is a dramatic reduction in the number of class I crossovers resulting in univalents at metaphase I and pollen sterility. Here we demonstrate that CDKG1 is necessary for the processing of recombination intermediates in the canonical ZMM recombination pathway and that loss of CDKG1 results in increased class II crossovers. While synapsis and events associated with class I crossovers are severely compromised in a cdkg1-1 mutant, they can be restored by increasing the number of recombination intermediates in the double cdkg1-1 fancm-1 mutant. Despite this, recombination intermediates are not correctly resolved, leading to the formation of chromosome aggregates at metaphase I. Our results show that CDKG1 acts early in the recombination process and is necessary to stabilize recombination intermediates. Finally, we show that the effect on recombination is not restricted to meiosis and that CDKG1 is also required for normal levels of DNA damage-induced homologous recombination in somatic tissues. . Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. The Plant Journal 55, 629-638. Dangel, N.J., Knoll, A., and Puchta, H. (2014). MHF1 plays Fanconi anaemia complementation group M protein (FANCM)-dependent and FANCM-independent roles in DNA repair and homologous recombination in plants.

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Section: Synapsis and Co Formation Are Restored In The Cdkg1-1 Fancm-supporting

confidence: 85%

CDKG1 Is Required for Meiotic and Somatic Recombination Intermediate Processing in Arabidopsis

et al. 2020

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“…Interestingly, the HEI10 protein might not work alone during ubiquitylation processes. In plants, the newly identified HEI10-interacting protein, HEIP1, is necessary for the formation of interfering COs and colocalizes with the site of COs represented by late HEI10 foci (Li et al 2018). Besides its interaction with HEI10, HEIP1 interacts with both ZIP4 and MSH5, suggesting that this new putative ZMM member may regulate CO formation by bridging multiple pro-CO factors in order to modify them by ubiquitin activities and progressively shape meiotic recombination intermediates towards the pro-CO state (Li et al 2018).…”

Section: New Additions To the Zmm Groupmentioning

confidence: 99%

“…In plants, the newly identified HEI10-interacting protein, HEIP1, is necessary for the formation of interfering COs and colocalizes with the site of COs represented by late HEI10 foci (Li et al 2018). Besides its interaction with HEI10, HEIP1 interacts with both ZIP4 and MSH5, suggesting that this new putative ZMM member may regulate CO formation by bridging multiple pro-CO factors in order to modify them by ubiquitin activities and progressively shape meiotic recombination intermediates towards the pro-CO state (Li et al 2018). Similarly, the Tetrahymena protein Sa15 interacts with Zhp3, the Zip3 ortholog, and is required for wild-type CO levels and localizes to meiotic chromosomes (Shodhan et al 2017).…”

Section: New Additions To the Zmm Groupmentioning

confidence: 99%

Crossing and zipping: molecular duties of the ZMM proteins in meiosis

2019

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Accurate segregation of homologous chromosomes during meiosis depends on the ability of meiotic cells to promote reciprocal exchanges between parental DNA strands, known as crossovers (COs). For most organisms, including budding yeast and other fungi, mammals, nematodes and plants, the major CO pathway depends on ZMM proteins, a set of molecular actors specifically devoted to recognize and stabilize CO-specific DNA intermediates that are formed during homologous recombination. The progressive implementation of ZMM-dependent COs takes place within the context of the synaptonemal complex (SC), a proteinaceous structure that polymerizes between homologs and participates in close homolog juxtaposition during prophase I of meiosis.While SC polymerization starts from ZMM-bound sites and ZMM proteins are required for SC polymerization in budding yeast and the fungus Sordaria, other organisms differ in their requirement for ZMM in SC elongation. This review provides an overview of ZMM functions and discusses their collaborative tasks for CO formation and SC assembly, based on recent findings and on a comparison of different model organisms.

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“…Total proteins were extracted from rice meiotic panicles (5-7 cm) with an extraction buffer that was previously described (Li et al, 2018). Protein samples were separated by SDS-PAGE on a 12% (v/v) polyacrylamide gel and electroblotted onto polyvinylidene difluoride membranes (GE Healthcare).…”

Section: Western Blottingmentioning

confidence: 99%

The SUN Domain Proteins OsSUN1 and OsSUN2 Play Critical but Partially Redundant Roles in Meiosis

Zhang

et al. 2020

Plant Physiol.

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During meiosis, Sad1/UNC-84 (SUN) domain proteins play conserved roles in promoting telomere bouquet formation and homologous pairing across species. Arabidopsis (Arabidopsis thaliana) AtSUN1 and AtSUN2 have been shown to have overlapping functions in meiosis. However, the role of SUN proteins in rice (Oryza sativa) meiosis and the extent of functional redundancy between them remain elusive. Here, we generated single and double mutants of OsSUN1 and OsSUN2 in rice using genome editing. The Ossun1 Ossun2 double mutant showed severe defects in telomere clustering, homologous pairing, and crossover formation, suggesting that OsSUN1 and OsSUN2 are essential for rice meiosis. When introducing a mutant allele of O. sativa SPORULATION11-1 (OsSPO11-1), which encodes a topoisomerase initiating homologous recombination, into the Ossun1 Ossun2 mutant, we observed a combined Osspo11-1-and Ossun1 Ossun2-like phenotype, demonstrating that OsSUN1 and OsSUN2 promote bouquet formation independent of OsSPO11-1 but regulate pairing and crossover formation downstream of OsSPO11-1. Importantly, the Ossun1 single mutant had a normal phenotype, but meiosis was disrupted in the Ossun2 mutant, indicating that OsSUN1 and OsSUN2 are not completely redundant in rice. Further analyses revealed a genetic dosage-dependent effect and an evolutionary differentiation between OsSUN1 and OsSUN2. These results suggested that OsSUN2 plays a more critical role than OsSUN1 in rice meiosis. Taken together, this work reveals the essential but partially redundant roles of OsSUN1 and OsSUN2 in rice meiosis and demonstrates that functional divergence of SUN proteins has taken place during evolution.

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HEIP1 regulates crossover formation during meiosis in rice

Cited by 38 publications

References 45 publications

CDKG1 Is Required for Meiotic and Somatic Recombination Intermediate Processing in Arabidopsis

CDKG1 Is Required for Meiotic and Somatic Recombination Intermediate Processing in Arabidopsis

Crossing and zipping: molecular duties of the ZMM proteins in meiosis

The SUN Domain Proteins OsSUN1 and OsSUN2 Play Critical but Partially Redundant Roles in Meiosis

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