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.
Highlights
Due to factors such as global population growth and climate change, food security is a major challenge which can be partly addressed by breeding new crop traits
Using the Plant Transcription Factor (TF) Database (Pérez-Rodríguez et al, 2010), we found a total of 1,353 annotated TFs of which 382 (28.2%)— belonging to several different TF families (Supplementary Table 8)—were differentially expressed in at least one stage or tissue comparison. 140 of these were expressed in anther tissues and not in germinating embryos
Sequencing of small RNAs (sRNAs) and DNA methylation, as done in maize by Dukowic-Schulze et al (2016), in anther and meiocyte at pre-meiosis to leptotene– zygotene stages with the strongest transcriptomic changes will enhance the full picture of these interconnecting gene regulation mechanisms
Summary
Due to factors such as global population growth and climate change, food security is a major challenge which can be partly addressed by breeding new crop traits. Breeding relies almost entirely upon meiosis, a specialized form of cell division which generates haploid gametes from diploid parental meiocytes. During the first of two cell divisions in meiosis, parental homologous chromosomes condense, pair, synapse, and undergo recombination within a meiosis-specific protein complex called the synaptonemal complex (SC) (Osman et al, 2011; Naranjo, 2012; Zickler and Kleckner, 2015). In the life cycle of flowering plants, this pivotal event occurs within specialized reproductive male (stamens) and female (carpel) organs. These reproductive organs are almost entirely composed of vegetative tissues embedding a small
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