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NUCLEAR RNA POLYMERASE D1 is essential for tomato embryogenesis and desiccation tolerance in seeds

Yixuan Feng,Yiming Wang,Tai Wang,Lingtong Liu

Plant-unique RNA polymerase IV (RNA Pol IV) governs the establishment of small RNA (sRNA)-directed DNA methylation (RdDM). In dicotyledon, elevated RdDM activity is often associated with embryogenesis; however, the loss of RdDM frequently results in indiscernible phenotypes. Here, we report that the absence of SlNRPD1 , encoding the largest subunit of RNA Pol IV, leads to diminished RdDM and abnormal embryogenesis in tomato ( Solanum lycopersicum ). Hypermethylation at pericentric transposable elements (TEs) and a burst of 21/22-nt siRNA from the distal and pericentric genes are observed in slnrpd1 embryos. The specific activation of endoribonuclease Dicer-like 2 ( SlDCL2b / c / d ) is correlated with 21/22-nt sRNA accumulation. Auxin and WUSCHEL-related homeobox (WOX) signaling gene expression is altered by mCHH hypomethylation, which may lead to defective embryos. Due to improper maturation, the slnrpd1 embryos cannot withstand post-harvest desiccation. This study provides insights into how DNA methylation regulates plant embryogenesis.