Abstract
In plants, each male meiotic product undergoes mitosis, and then one of the resulting cells divides again, yielding a three-celled pollen grain comprised of a vegetative cell and two sperm cells. Several genes have been found to act in this process, and DUO1 (DUO POLLEN 1), a transcription factor, plays a key role in sperm cell formation by activating expression of several germline genes. But how DUO1 itself is activated and how sperm cell formation is initiated remain unknown. To expand our understanding of sperm cell formation, we characterized an ARID (AT-Rich Interacting Domain)-containing protein, ARID1, that is specifically required for sperm cell formation in Arabidopsis. ARID1 localizes within nuclear bodies that are transiently present in the generative cell from which sperm cells arise, coincident with the timing of DUO1 activation. An arid1 mutant and antisense arid1 plants had an increased incidence of pollen with only a single sperm-like cell and exhibited reduced fertility as well as reduced expression of DUO1. In vitro and in vivo evidence showed that ARID1 binds to the DUO1 promoter. Lastly, we found that ARID1 physically associates with histone deacetylase 8 and that histone acetylation, which in wild type is evident only in sperm, expanded to the vegetative cell nucleus in the arid1 mutant. This study identifies a novel component required for sperm cell formation in plants and uncovers a direct positive regulatory role of ARID1 on DUO1 through association with histone acetylation.
Highlights
In contrast to animals, where meiotic products directly become gametes, the germline in plants is established by mitotic divisions after meiosis is completed
No positive element has been reported to regulate DUO POLLEN1 (DUO1) expression but, in addition to the negative regulation mediated by miR159 [12], a putative repressive GRSF (GermlineRestrictive Silencing Factor) binding site was noted in the DUO1 promoter [32]
These results suggest that activation of the DUO1 promoter may depend on transcription factors that bind to the proximal region of the promoter and that are inherited and/or segregated during asymmetric division of the microspore
Summary
In contrast to animals, where meiotic products directly become gametes, the germline in plants is established by mitotic divisions after meiosis is completed. The male germline arises by an asymmetric mitotic division of each meiotic product. The larger vegetative cell is arrested at the G1 phase of the cell cycle, while the smaller generative cell divides mitotically to produce the two male gametes or sperm cells [1]. Several genes have been implicated in sperm cell formation [2,3,4,5,6,7,8]. DUO POLLEN1 (DUO1) encodes a male germ cell–specific R2R3 Myb transcription factor that is necessary for twin sperm cell formation [3]
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