Role of small RNAs in epigenetic reprogramming during plant sexual reproduction
Introduction
The formation of viable gametes and their fusion during fertilization are key processes in the life cycle of sexually reproducing species. Plant sexual reproduction initiates with the formation of meiotic competent cells during sporogenesis, which is followed by gametogenesis where the products of meiosis undergo mitotic divisions to form multicellular gametophytes containing gametic cells that are competent to fuse during fertilization [1]. Functional gametes contain the genetic and epigenetic genome information inherited from their parents and are equipped with mechanisms that help them assess their compatibility with their sexual counterpart at fertilization [2]. Intensive research during the last years revealed that there are different RNA silencing pathways active during sporogenesis, gametogenesis and after fertilization that have essential roles to ensure reproductive success. Substantial progress has been achieved by combining classical cellular biology techniques with the use of high-throughput sequencing and purification of gametes and their accessory cells that allowed determining the populations of sRNAs, genome-wide cytosine methylation and distinct histone profiles in different reproductive cells [3, 4, 5, 6•]. As in somatic tissues, two major groups of sRNAs are predominantly present in reproductive cells: miRNAs and siRNAs, although their proportions differ substantially from other tissues [2, 7]. Plant miRNAs and siRNAs have distinct functions and are mainly associated with developmental regulation and genome protection, respectively (Box 1 and Ref. [8]), although the boundaries begin to blur as we discuss below. Here, we review current knowledge of sRNAs during angiosperm sexual reproduction and hypothesize on their functional roles in this process.
Section snippets
Regulation of sporogenesis by small RNAs
Male and female germline specification in plants takes place as the culmination of their adult development, which is a major difference to animals where the germline is established during early embryogenesis. Male and female meiosis-competent cells (pollen mother cells (PMCs) and megaspore mother cells (MMCs), respectively) have reduced heterochromatin content, correlating with removal of the linker histone H1 [9, 10•] and transposable element (TE) transcriptional reactivation [9, 10•, 11, 12].
Small RNAs associated with genome reprogramming during gametogenesis
The products of meiosis are spores that undergo mitotic divisions to form gamete-containing gametophytes. Angiosperms have the most reduced gametophytes in the plant kingdom, consisting of only few cells. The male gametophyte consists of a haploid vegetative cell (VC) that will form the pollen tube and two haploid sperm cells (SCs) that are the functional gametes [20]. In most angiosperms the female gametophyte is a seven-celled structure surrounded by maternal sporophytic tissues containing
Small RNAs in post-fertilization events
Despite accumulation of 21/22-nt siRNAs in SCs [4], their level of de novo CHH methylation is low [5, 23]. There are no genome-wide methylation data available for the EC, however, early embryos have low levels of de novo DNA methylation that increases during embryo development, indicating a process of re-methylation taking place after fertilization [35]. Correlating with this re-methylation is the accumulation of Pol IV-dependent 24-nt siRNAs in the Arabidopsis endosperm that at early stages
Potential role of gametophytic sRNAs
Notwithstanding recent progress in identifying the functional roles of sRNAs during angiosperm sexual reproduction, there remain substantial knowledge gaps to be filled. In this section of the manuscript we hypothesize about the potential roles of gametophytic sRNAs by drawing parallels to the roles of these sRNAs during reproduction in other species or in somatic tissues (Figure 2).
One important question to be addressed concerns the strikingly different sRNA profiles in male and female
Conclusions
The last years have witnessed an enormous progress in our understanding of the role of sRNAs during angiosperm sexual reproduction that has been made possible by the advance of sequencing technologies and new methods to isolate-specific cell types. What we are lacking thus far is information on the epigenomic landscape and associated sRNAs in female gametes, since the isolation of those cells remains a challenge that awaits to be tackled. We furthermore lack information on whether sRNAs have a
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This research was supported by a European Research Council Starting Independent Researcher grant (to C.K.) and a grant from the Swedish Science Foundation (to C.K.).
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