SDG2-Mediated H3K4me3 Is Crucial for Chromatin Condensation and Mitotic Division during Male Gametogenesis in Arabidopsis

Abstract

Epigenetic reprogramming occurring during reproduction is crucial for both animal and plant development. Histone H3 Lys 4 trimethylation (H3K4me3) is an evolutionarily conserved epigenetic mark of transcriptional active euchromatin. While much has been learned in somatic cells, H3K4me3 deposition and function in gametophyte is poorly studied. Here, we demonstrate that SET DOMAIN GROUP2 (SDG2)-mediated H3K4me3 deposition participates in epigenetic reprogramming during Arabidopsis male gametogenesis. We show that loss of SDG2 barely affects meiosis and cell fate establishment of haploid cells. However, we found that SDG2 is critical for postmeiotic microspore development. Mitotic cell division progression is partly impaired in the loss-of-function sdg2-1 mutant, particularly at the second mitosis setting up the two sperm cells. We demonstrate that SDG2 is involved in promoting chromatin decondensation in the pollen vegetative nucleus, likely through its role in H3K4me3 deposition, which prevents ectopic heterochromatic H3K9me2 speckle formation. Moreover, we found that derepression of the LTR retrotransposon ATLANTYS1 is compromised in the vegetative cell of the sdg2-1 mutant pollen. Consistent with chromatin condensation and compromised transcription activity, pollen germination and pollen tube elongation, representing the key function of the vegetative cell in transporting sperm cells during fertilization, are inhibited in the sdg2-1 mutant. Taken together, we conclude that SDG2-mediated H3K4me3 is an essential epigenetic mark of the gametophyte chromatin landscape, playing critical roles in gamete mitotic cell cycle progression and pollen vegetative cell function during male gametogenesis and beyond.

Evidence for a specific and critical role of mitogen‐activated protein kinase 20 in uni‐to‐binucleate transition of microgametogenesis in tomato

“…Mutation of AtMGT4, a magnesium transporter led to pollen abortion at the binucleate stage (Li et al ., ). SET DOMAIN GROUP2 (SDG2)‐mediated H3K4me3 plays roles in gamete mitotic cell cycle progression (Pinon et al ., ). Emerging evidence also points to the essential roles of sugar metabolism and jasmonic acid (JA) in pollen maturation (Song et al ., ; Wang & Ruan, ).…”

Phylogenetic Analyses of the Trithorax Homologs and Related Proteins in Cicer arietinum

“…ATXR3/SDG2 has a more important and strong role in H3K4me3 deposition. The knockdown atxr3 plants exhibit pleiotropic phenotypes, which include impaired development of male/female gametophyte and dwarfism (Berr et al, 2010;Guo et al, 2010;Pinon et al, 2017). ATXR7/SDG25 play important role for the regulation of Flowering Locus C (Berr et al, 2009).…”

Ultrastructure of spermiogenesis and the distribution of spermatozoal nuclear histones in the Japanese mantis shrimp, Oratosquilla oratoria (Crustacea: Stomatopoda)

“…The noncondensed nucleus may be caused by remanent acetylated histone H4 accompanied by chromatin fibers in Fenneropenaeus chinensis (Ge et al, ). Additionally, histone H3 methylation is important for sperm functioning and embryonic development, and histone H3 lysine 4 trimethylation (H3K4me3) plays a critical role in chromatin condensation and mitotic division during male gametogenesis (Pinon, Yao, Dong, & Shen, ; Song et al, ; Spina et al, ; Verma et al, ). These histone acetylations, together with methylations, may assist in achieving a more open chromatin configuration.…”