Distinct dynamics of HISTONE3 variants between the two fertilization products in plants

Sexual reproduction involves epigenetic reprogramming [1] comprising DNA methylation [2] and histone modifications [3-6]. In addition, dynamics of HISTONE3 (H3) variant H3.3 upon fertilization are conserved in animals, suggesting an essential role [7-9]. In contrast to H3, H3.3 marks actively transcribed regions of the genome and can be deposited in a replication-independent manner [10, 11]. Although H3 variants are conserved in plants, their dynamics during fertilization have remained unexplored. We overcame technical limitations to live imaging of the fertilization process in Arabidopsis thaliana and studied dynamics of the male-gamete-specific H3.3 [12] and the centromeric Histone Three Related 12 (HTR12) [13]. The double-fertilization process in plants produces the zygote and the embryo-nourishing endosperm [14]. We show that the zygote is characterized by replication-independent removal of paternal H3.3 and homogeneous incorporation of parental chromatin complements. In the endosperm, the paternal H3.3 is passively diluted by replication while the paternal chromatin remains segregated apart from the maternal chromatin (gonomery). Hence epigenetic regulations distinguish the two products of fertilization in plants. H3.3-replication-independent dynamics and gonomery also mark the first zygotic divisions in animal species [5, 15]. We thus propose the convergent selection of parental epigenetic imbalance involving H3 variants in sexually reproducing organisms.