Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I

Abstract

In flowering plants, successful germinal cell development and meiotic recombination depend upon a combination of environmental and genetic factors. To gain insights into this specialized reproductive development program 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 in anthers occur at the transition from pre-meiosis to leptotene–zygotene, which is followed by increasingly stable transcript abundance throughout prophase I into metaphase I–tetrad. Our analysis reveals that the pre-meiotic anthers 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 orthologs showed differential transcript abundance in at least one stage or tissue comparison. Argonautes, E3 ubiquitin ligases, and lys48 specific de-ubiquitinating enzymes were enriched in prophase I meiocyte samples. These developmental, time-resolved transcriptomes demonstrate remarkable stability in transcript abundance in meiocytes throughout prophase I after the initial and substantial reprogramming at meiosis entry and the complexity of the regulatory networks involved in early meiotic processes.

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

“…It is possible that they could relate to gene expression regulation as reported in Drosophila where large introns can promote alternative splicing ( Kandul and Noor, 2009 ) although only 16 such large introns (>5kbp) were found in Arabidopsis ( Chang et al, 2017 ). Although we detected eight RTEL1 transcripts in barley anther and meiocyte transcriptome ( Barakate et al, 2021 ), only one isoform was expressed. Interestingly, we detected several AS events of partial exon skipping (exon 10, exon 12, and exon 21) and intron retention in all samples.…”

“…Based on transcriptomic data from 16 different tissues and developmental stages of barley ( International Barley Genome Sequencing Consortium, 2012 ), RTEL1 is most highly expressed in young inflorescences compared to other vegetative tissues ( Figure 1B ). Expression was also detected in the transcriptomic data of isolated barley anthers and meiocytes ( Barakate et al, 2021 ). Although RTEL1 is expressed during all meiotic stages (and in germinating embryos), the highest transcript level was detected in anthers at the pre-meiosis stage ( Figure 1C ).…”

“…In vitro biochemical characterisation of the Arabidopsis SRS2 homolog demonstrated its 3′- to 5′-helicase activity and its involvement in processing different recombination intermediates ( Blanck et al, 2009 ). Barley SRS2 (BAnTr.GP.2HG007838, HORVU2Hr1G051300) is expressed in different tissues including anthers and meiocytes ( Barakate et al, 2021 ; Milne et al, 2021 ) but its role in meiosis remains to be studied.…”

The Formation of Bivalents and the Control of Plant Meiotic Recombination

“…Though sex-specific transcriptomes have been obtained in various plant species ( Dukowic-Schulze et al, 2020 ; Liu et al, 2020 ; Barakate et al, 2021 ), a systematic comparison between male and female meiotic transcriptomes has not yet been performed.…”

Genome-Wide Identification of Barley Long Noncoding RNAs and Analysis of Their Regulatory Interactions during Shoot and Grain Development

“…For instance, Unver and Tombuloglu [14] analyzed the expression pattern of novel lncRNAs under excessive boron treatment, and Chen et al [15] identified 487 low nitrogen stress responsive lncRNAs in a barley landrace. Recently, Barakte et al [16] revealed the potential role of lncRNAs at the meiotic phase in anther. Although the role of lncRNAs in the stress response is very important, there is a lack of genome-wide studies of lncRNA regulation during barley development.…”