Clearance of maternal barriers by paternal miR159 to initiate endosperm nuclear division in Arabidopsis

Abstract

Sperm entry triggers central cell division during seed development, but what factors besides the genome are inherited from sperm, and the mechanism by which paternal factors regulate early division events, are not understood. Here we show that sperm-transmitted miR159 promotes endosperm nuclear division by repressing central cell-transmitted miR159 targets. Disruption of paternal miR159 causes approximately half of the seeds to abort as a result of defective endosperm nuclear divisions. In wild-type plants, MYB33 and MYB65, two miR159 targets, are highly expressed in the central cell before fertilization, but both are rapidly abolished after fertilization. In contrast, loss of paternal miR159 leads to retention of MYB33 and MYB65 in the central cell after fertilization. Furthermore, ectopic expression of a miR159-resistant version of MYB33 (mMYB33) in the endosperm significantly inhibits initiation of endosperm nuclear division. Collectively, these results show that paternal miR159 inhibits its maternal targets to promote endosperm nuclear division, thus uncovering a previously unknown paternal effect on seed development.

Intercellular delivery of small RNAs in plant gametes

“…Disruption of paternal miR159 caused arrested and/or delayed endosperm nuclear divisions, resulting from the retention of maternal targets, MYB33 and MYB65, after fertilization (Zhao et al, 2018). Ectopic expression of a miR159resistant version of MYB33 in the endosperm significantly inhibited initiation of endosperm nuclear divisions (Zhao et al, 2018). This suggests that a sperm-enriched miRNA initiates an early division event by removing the roadblock comprising maternal factors.…”

“…Using both genetic and cell biological approaches, Zhao et al . () showed that sperm‐transmitted miR159 promotes endosperm nuclear divisions by repressing central cell‐transmitted miR159 targets. Disruption of paternal miR159 caused arrested and/or delayed endosperm nuclear divisions, resulting from the retention of maternal targets, MYB33 and MYB65 , after fertilization (Zhao et al ., ).…”

“…Unexpectedly, DUO1, one of the targets of miR159, specifically accumulates in sperm (Rotman et al, 2005), indicating that sperm-enriched miR159 is not destined to silence its target locally. Using both genetic and cell biological approaches, Zhao et al (2018) showed that sperm-transmitted miR159 promotes endosperm nuclear divisions by repressing central cell-transmitted miR159 targets. Disruption of paternal miR159 caused arrested and/or delayed endosperm nuclear divisions, resulting from the retention of maternal targets, MYB33 and MYB65, after fertilization (Zhao et al, 2018).…”

Reprogramming of 24nt siRNAs in rice gametes

“…miR159a.2 was unique to root, while miR159c, d, and e were enriched in egg, and miR159f was enriched in seedling shoot and egg. In Arabidopsis, miR159 family members repress MYB transcription factors and are expressed in multiple tissues including sperm, and paternal miR159 regulates nuclear division in endosperm (Allen et al 2010;Zhao et al 2018).…”

Conservation and Divergence in the Meiocyte sRNAomes of Arabidopsis, Soybean, and Cucumber

“…Plant miRNAs are typically 20-22 nt in length, and function in posttranscriptional gene silencing through mRNA cleavage or translational repression (Rogers and Chen, 2013). In animals and plants, miRNAs play an important role in male germline and embryonic development (Borges et al, 2011;Conine et al, 2018;Zhao et al, 2018). Another large group of sRNAs in plants constitute the 20 to 24 nt siRNAs, which function primarily in transcriptional gene silencing of viral DNA, transgenes, and transposable elements (TEs; Borges and Martienssen, 2015) through the RNA-directed DNA methylation pathway.…”