Abstract
Active DNA demethylation is required for sexual reproduction in plants but the molecular determinants underlying this epigenetic control are not known. Here, we show in Arabidopsis thaliana that the DNA glycosylases DEMETER (DME) and REPRESSOR OF SILENCING 1 (ROS1) act semi-redundantly in the vegetative cell of pollen to demethylate DNA and ensure proper pollen tube progression. Moreover, we identify six pollen-specific genes with increased DNA methylation as well as reduced expression in dme and dme;ros1. We further show that for four of these genes, reinstalling their expression individually in mutant pollen is sufficient to improve male fertility. Our findings demonstrate an essential role of active DNA demethylation in regulating genes involved in pollen function.
Highlights
Active DNA demethylation is required for sexual reproduction in plants but the molecular determinants underlying this epigenetic control are not known
Crosses involving double heterozygous dme/+;ros1/+ fathers confirmed these results, with a reduced transmission of dme to 11.4% when alone and to only 1.4% when combined with ros[1], compared to 25% expected under Mendelian segregation in both cases
Our results reveal that the activity of the DNA glycosylase REPRESSOR OF SILENCING 1 (ROS1) is not confined to somatic tissues, and that it contributes to the demethylation of the genome in the vegetative cell (VC)
Summary
Active DNA demethylation is required for sexual reproduction in plants but the molecular determinants underlying this epigenetic control are not known. The ovule includes two synergids, which play important roles for pollen tube attraction, the central cell (CC), which is globally hypomethylated—again mainly in the CG context—and the egg cell (EC)[11] In both the VC and CC, DNA demethylation mainly depends on the activity of the DNA glycosylase DEMETER (DME)[9]. An alternative possibility is that active DNA demethylation is required in the VC to enable the expression of genes involved in pollen function[14,17]. Our findings indicate that ROS1 acts together with DME in the VC to ensure proper genome-wide DNA demethylation, as well as proper activation of a small number of genes that define a signaling complex critical for pollen tube function
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