Abstract
DNA methylation is a crucial regulatory mechanism in many biological processes. However, limited studies have dissected the contribution of DNA methylation to sexual differentiation in dioecious plants. In this study, we investigated the variances in methylation and transcriptional patterns of male and female flowers of garden asparagus. Compared with male flowers, female flowers at the same stages showed higher levels of DNA methylation. Both male and female flowers gained DNA methylation globally from the premeiotic to meiotic stages. Detailed analysis revealed that the increased DNA methylation was largely due to increased CHH methylation. Correlation analysis of differentially expressed genes and differentially methylated regions suggested that DNA methylation might not have contributed to the expression variation of the sex-determining genes SOFF and TDF1 but probably played important roles in sexual differentiation and flower development of garden asparagus. The upregulated genes AoMS1, AoLAP3, AoAMS, and AoLAP5 with varied methylated CHH regions might have been involved in sexual differentiation and flower development of garden asparagus. Plant hormone signaling genes and transcription factor genes also participated in sexual differentiation and flower development with potential epigenetic regulation. In addition, the CG and CHG methylation levels in the Y chromosome were notably higher than those in the X chromosome, implying that DNA methylation might have been involved in Y chromosome evolution. These data provide insights into the epigenetic modification of sexual differentiation and flower development and improve our understanding of sex chromosome evolution in garden asparagus.
Highlights
As an essential epigenetic regulatory mechanism in eukaryotic species, DNA methylation contributes greatly to transposon silencing, heterochromatin organization, genome integrity maintenance, and gene expression regulation[1,2,3,4]
A similar tendency was observed between the pairwise comparisons of M_pre vs. M_mei and F_pre vs. F_mei (Fig. 2d). These results indicate that dynamic methylation patterns are potentially responsible for garden asparagus sexual differentiation and distinct flower development
To investigate whether the sexual differentiation process in garden asparagus was associated with DNA methylation, we focused on analyzing Differentially methylated regions (DMRs)-related genes by comparing F_mei and M_mei flowers because the meiotic stage is the critical stage of sexual differentiation[24,29]
Summary
As an essential epigenetic regulatory mechanism in eukaryotic species, DNA methylation contributes greatly to transposon silencing, heterochromatin organization, genome integrity maintenance, and gene expression regulation[1,2,3,4]. DNA methylation usually exists in CG, CHG, and CHH (where H represents A, T, or C) sequence contexts[5]. The genomes of different plants show distinct DNA methylation profiles[6]. The DNA methylation ratio and level change dynamically in different plant tissues at diverse developmental stages[7,8]. Accumulating reports have suggested that DNA methylation is a key modulator of numerous aspects of plant development, such as fruit ripening[7,9], seed germination and development[8], and stress responses[10]. The possible role of DNA methylation in sexual differentiation and unisexual flower development in dioecious plants is largely unclear. Approximately 6% of angiosperm species are dioecious; that is, each individual harbors only male or female flowers[11]
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