DNA methylation dynamics of sperm cell lineage development in tomato

Abstract

SUMMARY During the sexual reproduction of higher plants, DNA methylation and transcription are broadly changed to reshape a microspore into two sperm cells (SCs) and a vegetative cell (VC). However, when and how the DNA methylation of SCs is established remains not fully understood. Here we investigate the DNA methylation (5 mC) dynamics of SC lineage and the VC in tomato using whole‐genome bisulfite sequencing. We find the asymmetric division of the microspore gives its two daughter cells differential methylome. Compared with the generative cell (GC), the VC is hypomethylated at CG sites while hypermethylated at CHG and CHH sites, with the majority of differentially methylation regions targeted to transposable elements (TEs). SCs have a nearly identical DNA methylome to the GC, suggesting that the methylation landscape in SCs may be pre‐established following the asymmetric division or inherited from the GC. The random forest classifier for predicting gene and TE expression shows that methylation within the gene body is a more powerful predictor for gene expression. Among all tested samples, gene and TE expression in the microspore may be more predictable by DNA methylation. Our results depict an intact DNA methylome landscape of SC lineage in higher plants, and reveal that the impact of DNA methylation on transcription is variant in different cell types.

Fifty years of sperm cell isolations: from structural to omic studies

“…These differences could be linked to the activity of the chromatin remodeller DDM1 and the DNA methyltransferase MET1, which are both largely restricted to sperm cells ( Calarco et al , 2012 ; Ibarra et al , 2012 ). Similar differences were reported in sperm cells and vegetative cell nuclei of S. lycopersicum ( Lu et al ., 2021 ) and O. sativa ( Kim et al , 2019 ; Zhou et al , 2021 ). DNA glycosylases play a central role in establishing these differences, as has been shown for Arabidopsis and rice ( Schoft et al , 2011 ; Ibarra et al , 2012 ; Kim et al , 2019 ; Zhou et al , 2021 ).…”

DNA demethylases remodel DNA methylation in rice gametes and zygote and are required for reproduction

“…The egg is fertilized by one sperm to form a zygote to initiate embryogenesis, and the binuclear central cell is fertilized by the other sperm to generate the triploid endosperm, a nutrient tissue that supports growth of the embryo or the seedling. Genome-wide DNA methylation profiling of sperm and vegetative cells of the mature pollen has revealed dynamic DNA methylation changes during male gametogenesis in Arabidopsis, rice, and tomato (Calarco et al, 2012;Ibarra et al, 2012;Hsieh et al, 2016;Walker et al, 2018;Kim et al, 2019;Li et al, 2020a;Lu et al, 2021). DNA methylation analysis has also been performed on egg and central cells isolated from Arabidopsis and rice (Park et al, 2016;Li et al, 2020a).…”

Find your identity – methylation dynamics in the sperm cell lineage

“…Recently, the research group of Tai Wang developed a method to isolate high numbers of generative cells, sperm cells, and vegetative nuclei from tomato ( Solanum lycopersicum ) pollen (Lu et al , 2015). In this issue, they created a methylome of all three cell types using bisulfite sequencing (Lu et al , 2020). By pairwise comparison of the methylation patterns, they found that there were millions of differentially methylated sites between the microspore and the generative cell, as well as between the microspore and the vegetative cell nucleus.…”