Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis

Walker, James W.; Gao, Hongbo; Zhang, Jingyi; Aldridge, Billy; Vickers, Martin; Higgins, James D.; Feng, Xiaoqi

doi:10.1038/s41588-017-0008-5

Cited by 158 publications

(182 citation statements)

References 52 publications

(32 reference statements)

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“…CDKG1 has previously been shown to be involved in the splicing of the CalS5 gene in the tapetal cells affecting pollen fertility (Huang et al ., ). In addition, a recent survey of transcripts in the male sexual lineage has shown that mis‐splicing of the MPS1 gene leads to meiotic defects (Walker et al ., ). Taken together, these observations suggest that splicing is an important regulatory mechanism during meiotic cell divisions.…”

Section: Discussionmentioning

confidence: 97%

The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of ArabidopsisATU2AF65A

et al. 2018

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SummaryThe ability to adapt growth and development to temperature variations is crucial to generate plant varieties resilient to predicted temperature changes. However, the mechanisms underlying plant response to progressive increases in temperature have just started to be elucidated. Here, we report that the cyclin‐dependent kinase G1 (CDKG1) is a central element in a thermo‐sensitive mRNA splicing cascade that transduces changes in ambient temperature into differential expression of the fundamental spliceosome component, ATU2AF65A. CDKG1 is alternatively spliced in a temperature‐dependent manner. We found that this process is partly dependent on both the cyclin‐dependent kinase G2 (CDKG2) and the interacting co‐factor CYCLIN L1 (CYCL1), resulting in two distinct messenger RNAs. The relative abundance of both CDKG1 transcripts correlates with ambient temperature and possibly with different expression levels of the associated protein isoforms. Both CDKG1 alternative transcripts are necessary to fully complement the expression of ATU2AF65A across the temperature range. Our data support a previously unidentified temperature‐dependent mechanism based on the alternative splicing (AS) of CDKG1 and regulated by CDKG2 and CYCL1. We propose that changes in ambient temperature affect the relative abundance of CDKG1 transcripts, and this in turn translates into differential CDKG1 protein expression coordinating the AS of ATU2AF65A.

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Section: Discussionmentioning

confidence: 97%

The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of ArabidopsisATU2AF65A

et al. 2018

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“…However, further analysis of these pathways and their target loci is needed to fully describe their role in meiotic development. One such function has been demonstrated in a recent study by Walker et al (2018) showing that de novo RNA-directed DNA methylation (RdDM) induces cell-lineage-specific epigenetic marks regulating meiotic gene expression in Arabidopsis .…”

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

Preprint

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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, SHH1-mediated recruitment only accounts for about half of known RdDM loci, suggesting that additional mechanisms of Pol IV recruitment remain to be identified. Other examples of organ-specific RdDM suggest that regulated expression of Pol IV activity, perhaps through tissue-specific epigenetic modification, is an underexplored developmental mechanism Walker et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Abundant expression of maternal siRNAs is a conserved feature of seed development

Grover

Burgess

Kendall

et al. 2019

Preprint

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Small RNAs are abundant in plant reproductive tissues, especially 24-nt short interfering (si)RNAs. Most 24-nt siRNAs are dependent on RNA Pol IV and RDR2, and establish DNA methylation at thousands of genomic loci in a process called RNA-directed DNA methylation (RdDM). In Brassica rapa, RdDM is required in the maternal sporophyte for successful seed development. Here we demonstrate that a small number of siRNA loci account for over 90% of siRNA expression during B. rapa seed development. These loci exhibit unique characteristics with regard to their copy number and association with genomic features, but they resemble canonical 24-nt siRNA loci in their dependence on RNA Pol IV/RDR2 and role in RdDM. These loci are expressed in ovules before fertilization and in the seed coat, embryo, and endosperm following fertilization. We observed a similar pattern of 24-nt siRNA expression in diverse angiosperms despite rapid sequence evolution at siren loci. In the endosperm, siren siRNAs show a marked maternal bias, and siren expression in maternal sporophytic tissues is required for siren siRNA accumulation. Together these results demonstrate that seed development occurs under the influence of abundant maternal siRNAs that might be transported to, and function in, filial tissues.

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Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis

Cited by 158 publications

References 52 publications

The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of ArabidopsisATU2AF65A

The cyclin‐dependent kinase G group defines a thermo‐sensitive alternative splicing circuit modulating the expression of ArabidopsisATU2AF65A

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

Abundant expression of maternal siRNAs is a conserved feature of seed development

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