ZmSSRP1 facilitates the progression of RNA polymerase II and is essential for kernel development in maize

Abstract

Transcript elongation controlled by RNA polymerase II (RNAP II) represents a key regulatory event in numerous cellular processes. However, the precise mechanisms underlying the regulation of RNAP II distribution and progression in plants remain largely elusive. Here, we positionally cloned the causal mutation in the defective kernel 59 (dek59) maize (Zea mays) mutant and demonstrated that Dek59 encodes Structure-Specific Recognition-Protein 1 (ZmSSRP1), a subunit of the Facilitates Chromatin Transcription (FACT) complex that regulates RNAP II. Using genome-wide mapping assays, we determined that ZmSSRP1 binding sites co-localize with those of RNAP II phosphorylated at its serine 2 residue (Ser2P) and are highly enriched within actively transcribed genes. Mutation of ZmSSRP1 resulted in Ser2P accumulation around the +1 nucleosome of genes, affecting gene expression in a gene length-dependent manner. The reduced amount of RNAP II in the dek59 mutant was rescued to wild-type-like levels by inhibiting the proteasome, indicating that arrested RNAP II degradation is proteasome-dependent. These findings reveal the indispensable role of ZmSSRP1 in regulating RNAP II-mediated transcription, which is critical for the proper expression of thousands of genes during maize seed development.