Germline fate in pollen

Huang and Sun explore how germline fate is suppressed in vegetative cells but not in sperm cells of pollen.

By Xiaorong Huang and Meng-Xiang Sun

College of Life Science, State Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, China

Background: The microspore divides asymmetrically to form a larger vegetative cell (VC) and a smaller generative cell (GC). The GC further divides to produce two sperm cells (SCs). Thus, the male gametophyte (pollen) consists of a VC and male germline (MG) cells (GC and SC twins) and is an excellent model for studying cell fate determination. MG cell fate is thought to be specified by the differential distribution of unknown determinants caused by the asymmetric division of the microspore. H3K27me3 is erased specifically in SC chromatin but persists in the VC, and DNA methylation is lost along with H3K9me2 in the VC. Therefore, certain epigenetic factors may determine the cell fate of the two cell lineages in pollen.

Question: How is germline fate suppressed in VCs but established in MG cells, and do histone posttranslational modifications contribute to this process?

Findings: In mature pollen, H3K27me3 appears in VCs, but not in SCs. We generated a transgenic Arabidopsis line that expresses H3K27 demethylase REF6 (hereafter TL) to erase H3K27me3 in VCs. The VC-targeted H3K27me3 removal disturbed VC development. Pollen from strong TLs failed to germinate. The ectopic distribution of MG cell-specific markers indicated that VC-targeted H3K27me3 erasure altered TL VCs and triggered a cell fate transition towards MG cells. Multi-omics and cytological analyses confirmed the occurrence of extensive cell identity transition due to H3K27me3 erasure. Thus, we experimentally reveal that H3K27 methylation plays a critical role in guiding MG cell/VC fate specification.

Next steps: VC-targeted H3K27me3 erasure did not shift all VCs towards the MG cell fate, suggesting that other pathways or epigenetic mechanisms function in cell fate determination during male gametophyte development. How H3K27me3 erasure in the MG is controlled and how the different epigenetic mechanisms are integrated in this process remain to be elucidated.

Xiaorong Huang and Meng-Xiang Sun. (2022). H3K27 methylation regulates the fate of two cell lineages in male gametophytes.