Interplay between Pds5 and Rec8 in regulating chromosome axis length and crossover frequency

Song, Meihui; Zhai, Binyuan; Yang, Xiao; Tan, Taicong; Wang, Ying; Yang, Xuan; Tan, Yingjin; Chu, Tingting; Cao, Yanding; Song, Yulong; Wang, Shunxin; Zhang, Liangran

doi:10.1126/sciadv.abe7920

Cited by 25 publications

(50 citation statements)

References 62 publications

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“…In all three cases, axis/SC lengths are increased when compared to wild type, indicating a change in the loop/axis relationship. Similar increased axis length has previously been reported in mutants lacking meiosis-specific cohesins SMC1Beta and Rec8, as well as other axis components like Spo76/Pds5, which all play key roles in the loop/axis relationship (e.g., Viera et al, 2020 ; Song et al, 2021 ). Several hypotheses could explain the observed changes in axis lengths.…”

Section: Discussionsupporting

confidence: 83%

“…As a primary function of RNAi is to regulate gene expression, one hypothesis could be that Dicer and Argonaute proteins are involved in fine tuning of the expression of genes coding for proteins involved in meiotic chromosome axis morphogenesis. In F. graminearum , expression of Rec8 is strongly reduced in the Fgdlc1 mutant ( Zeng et al, 2018 ) and lower Rec8 expression is accompanied by shorter chromosome axes in S. cerevisiae ( Song et al, 2021 ) and with defects in SC organization in mouse ( Murdoch et al, 2013 ).…”

Section: Discussionmentioning

confidence: 99%

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RNAi-Related Dicer and Argonaute Proteins Play Critical Roles for Meiocyte Formation, Chromosome-Axes Lengths and Crossover Patterning in the Fungus Sordaria macrospora

Girard

Budin

Boisnard

et al. 2021

Front. Cell Dev. Biol.

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RNA interference (RNAi) is a cellular process involving small RNAs that target and regulate complementary RNA transcripts. This phenomenon has well-characterized roles in regulating gene and transposon expression. In addition, Dicer and Argonaute proteins, which are key players of RNAi, also have functions unrelated to gene repression. We show here that in the filamentous Ascomycete Sordaria macrospora, genes encoding the two Dicer (Dcl1 and Dcl2) and the two Argonaute (Sms2 and Qde2) proteins are dispensable for vegetative growth. However, we identified roles for all four proteins in the sexual cycle. Dcl1 and Sms2 are essential for timely and successful ascus/meiocyte formation. During meiosis per se, Dcl1, Dcl2, and Qde2 modulate, more or less severely, chromosome axis length and crossover numbers, patterning and interference. Additionally, Sms2 is necessary both for correct synaptonemal complex formation and loading of the pro-crossover E3 ligase-protein Hei10. Moreover, meiocyte formation, and thus meiotic induction, is completely blocked in the dcl1 dcl2 and dcl1 sms2 null double mutants. These results indicate complex roles of the RNAi machinery during major steps of the meiotic process with newly uncovered roles for chromosomes-axis length modulation and crossover patterning regulation.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

RNAi-Related Dicer and Argonaute Proteins Play Critical Roles for Meiocyte Formation, Chromosome-Axes Lengths and Crossover Patterning in the Fungus Sordaria macrospora

Girard

Budin

Boisnard

et al. 2021

Front. Cell Dev. Biol.

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“…Indeed, the concomitant depletion of the cohesin regulators PDS5A and PDS5B leads to a severe shortening of axial elements, despite the presence of all tested cohesin subunits in those spermatocytes ( Viera et al, 2020 ). This role of Pds5 in controlling axis length as also been observed in S. cerevisiae ( Jin et al, 2009 ; Song et al, 2021 ) and even in the absence of the sister chromatid ( Hong et al, 2019 ). Although this may indicate an increase in loop lengths, this may result from the consequences of the absence of Pds5 on loop expansion and on sister chromatid cohesion as clearly observed by HiC in yeast vegetative cells ( Dauban et al, 2020 ).…”

Section: Functional Roles Of the Meiotic Axis Organization In Early Meiotic Prophase Isupporting

confidence: 67%

Chromosome Organization in Early Meiotic Prophase

Grey

Massy

2021

Front. Cell Dev. Biol.

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One of the most fascinating aspects of meiosis is the extensive reorganization of the genome at the prophase of the first meiotic division (prophase I). The first steps of this reorganization are observed with the establishment of an axis structure, that connects sister chromatids, from which emanate arrays of chromatin loops. This axis structure, called the axial element, consists of various proteins, such as cohesins, HORMA-domain proteins, and axial element proteins. In many organisms, axial elements are required to set the stage for efficient sister chromatid cohesion and meiotic recombination, necessary for the recognition of the homologous chromosomes. Here, we review the different actors involved in axial element formation in Saccharomyces cerevisiae and in mouse. We describe the current knowledge of their localization pattern during prophase I, their functional interdependence, their role in sister chromatid cohesion, loop axis formation, homolog pairing before meiotic recombination, and recombination. We also address further challenges that need to be resolved, to fully understand the interplay between the chromosome structure and the different molecular steps that take place in early prophase I, which lead to the successful outcome of meiosis I.

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“…Chromosome axis length was determined as previously described ( 58 ). During pachytene, homologs are tightly connected from end to end by SC and axis length can be determined by measurement of Zip1 or Rec8 lines.…”

Section: Methodsmentioning

confidence: 99%

ESA1 regulates meiotic chromosome axis and crossover frequency via acetylating histone H4

Wang

Zhai

Tan

et al. 2021

Nucleic Acids Research

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Meiotic recombination is integrated into and regulated by meiotic chromosomes, which is organized as loop/axis architecture. However, the regulation of chromosome organization is poorly understood. Here, we show Esa1, the NuA4 complex catalytic subunit, is constitutively expressed and localizes on chromatin loops during meiosis. Esa1 plays multiple roles including homolog synapsis, sporulation efficiency, spore viability, and chromosome segregation in meiosis. Detailed analyses show the meiosis-specific depletion of Esa1 results in decreased chromosome axis length independent of another axis length regulator Pds5, which further leads to a decreased number of Mer2 foci, and consequently a decreased number of DNA double-strand breaks, recombination intermediates, and crossover frequency. However, Esa1 depletion does not impair the occurrence of the obligatory crossover required for faithful chromosome segregation, or the strength of crossover interference. Further investigations demonstrate Esa1 regulates chromosome axis length via acetylating the N-terminal tail of histone H4 but not altering transcription program. Therefore, we firstly show a non-chromosome axis component, Esa1, acetylates histone H4 on chromatin loops to regulate chromosome axis length and consequently recombination frequency but does not affect the basic meiotic recombination process. Additionally, Esa1 depletion downregulates middle induced meiotic genes, which probably causing defects in sporulation and chromosome segregation.

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Interplay between Pds5 and Rec8 in regulating chromosome axis length and crossover frequency

Cited by 25 publications

References 62 publications

RNAi-Related Dicer and Argonaute Proteins Play Critical Roles for Meiocyte Formation, Chromosome-Axes Lengths and Crossover Patterning in the Fungus Sordaria macrospora

RNAi-Related Dicer and Argonaute Proteins Play Critical Roles for Meiocyte Formation, Chromosome-Axes Lengths and Crossover Patterning in the Fungus Sordaria macrospora

Chromosome Organization in Early Meiotic Prophase

ESA1 regulates meiotic chromosome axis and crossover frequency via acetylating histone H4

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