Long non-coding RNAs are major contributors to transcriptome changes in sunflower meiocytes with different recombination rates

Abstract

BackgroundMeiosis is a form of specialized cell division that marks the transition from diploid meiocyte to haploid gamete, and provides an opportunity for genetic reassortment through recombination. Experimental data indicates that, relative to their wild ancestors, cultivated sunflower varieties show a higher recombination rate during meiosis. To better understand the molecular basis for this difference, we compared gene expression in male sunflower meiocytes in prophase I isolated from a domesticated line, a wild relative, and a F1 hybrid of the two.ResultsOf the genes that showed differential expression between the wild and domesticated genotypes, 63.62 % could not be identified as protein-coding genes, and of these genes, 70.98 % passed stringent filters to be classified as long non-coding RNAs (lncRNAs). Compared to the sunflower somatic transcriptome, meiocytes express a higher proportion of lncRNAs, and the majority of genes with exclusive expression in meiocytes were lncRNAs. Around 40 % of the lncRNAs showed sequence similarity with small RNAs (sRNA), while 1.53 % were predicted to be sunflower natural antisense transcripts (NATs), and 9.18 % contained transposable elements (TE). We identified 6895 lncRNAs that are exclusively expressed in meiocytes, these lncRNAs appear to have higher conservation, a greater degree of differential expression, a higher proportion of sRNA similarity, and higher TE content relative to lncRNAs that are also expressed in the somatic transcriptome.ConclusionslncRNAs play important roles in plant meiosis and may participate in chromatin modification processes, although other regulatory functions cannot be excluded. lncRNAs could also be related to the different recombination rates seen for domesticated and wild sunflowers.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2776-1) contains supplementary material, which is available to authorized users.

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

“…The number DEGs in staged anther tissues declines from its highest level between leptotene–zygotene and pre-meiosis with the largest down-regulation of genes of any comparison. This supports previous studies in Arabidopsis (Chen et al , 2010; Yang et al , 2011), maize (Dukowic-Schulze et al , 2014) and sunflower (Flórez-Zapata et al , 2014; Flórez-Zapata et al , 2016) showing large scale transcriptional re-organisation at meiosis entry. A strikingly large component of differentially expressed genes at this transition were lncRNAs—98% of which were expressed in anthers but not in germinating embryos.…”

“…High expression of lncRNAs in plant reproductive tissues has been described in both sunflower (Flórez-Zapata et al , 2016) and in maize (Li et al , 2014). Flórez-Zapata et al (2016) reported large scale differential expression of lncRNAs in sunflower meiocytes when contrasted with somatic tissues; and between meiocytes in comparison of genotypes exhibiting significantly different recombination rates. Our results indicate that, similar to sunflower, meiocyte specific lncRNAs may indeed play an important role in prophase I in barley.…”

“…Different classes of phased small-interfering RNAs (phasiRNAs), for example, have been shown to be enriched in maize anthers at different meiotic stages (Zhai et al , 2015) and shown to be present in most angiosperms (Xia et al , 2019). Deep sequencing technologies have enabled global analysis of meiotic sRNA in sunflower showing sequence similarity to 40% of lncRNAs (Flórez-Zapata et al , 2016). In Arabidopsis , Huang et al (2019) revealed different meiotic and mitotic sRNA landscapes and found that meiocyte-specific sRNAs (ms-sRNAs) are significantly enriched in genic regions contrary to somatic small interfering RNAs that are enriched in intergenic regions.…”

“…Using laser microdissection, microarray expression profiling, and mass spectrometry, Yuan et al (2018) conducted analysis of pre-meiotic germinal cell development within maize anthers, and demonstrated that many meiotic genes are both transcribed and translated prior to entry into meiotic prophase I. Mirroring Yuan et al (2018), Nelms and Walbot (2019) investigated transcriptional dynamics in maize anther meiocytes at the point of entry into prophase I using single-cell RNA sequencing, identifying a further two-step transcriptional reorganisation at leptotene. Analysis of the meiocyte transcriptome of domesticated and wild sunflowers revealed a potential regulatory role for long non-coding RNAs (lncRNAs) in meiotic recombination (Flórez-Zapata et al , 2016).…”

Conservation and Divergence in the Meiocyte sRNAomes of Arabidopsis, Soybean, and Cucumber

“…On the other hand, mutants of Arabidopsis miRNAmachinery genes have a relaxed meiotic chromatin conformation (Oliver et al, 2017), confirming a broad role for miRNAs in plant meiosis. Previous work in maize (Dukowic-Schulze et al, 2016) and sunflower (Helianthus annuus;Flórez-Zapata et al, 2016) meiocytes, and our results have revealed conserved miRNAs that are preferentially expressed in meiocytes, including miR390 and miR167 (Fig. 2, A-C), and the phasiRNA pathway-related soybean-specific miR4392 (Fig.…”