RNA polymerase mapping in plants identifies enhancers enriched in causal variants

Authors: LOZANO, ROBERTO - Cornell University; BOOTH, GREGORY - Cornell University; OMAR, BILAN - Montpellier Supagro – International Center For High Education In Agricultural Sciences; LI, BO - Chinese Academy Of Sciences; Buckler, Edward - Ed; LIS, JOHN - Cornell University; Jannink, Jean-Luc; PINO DEL CARPIO, DUNIA - Agribiotech

Submitted to: bioRxiv
Publication Type: Review Article
Publication Acceptance Date: 7/24/2018
Publication Date: 7/24/2018
Citation: Lozano, R., Booth, G.T., Omar, B.Y., Li, B., Buckler IV, E.S., Lis, J.T., Jannink, J., Pino Del Carpio, D. 2018. RNA polymerase mapping in plants identifies enhancers enriched in causal variants. bioRxiv. https://doi.org/10.1101/376640.

Interpretive Summary: Arabidopsis, a flowering plant from the mustard family, has been widely studied by plant scientists because it is similar to crop plants, yet it is inexpensive to grow and produces many seeds. Scientists assumed that the transcription mechanisms (how information from a gene is used to construct a functional product, such as a protein) in Arabdopsis would be similar to other crops. However, this research shows that the transcription process in cassava and maize is more complex. This information can be used in breeding programs to guide selection and potentially improve the rate of genetic gain.

Technical Abstract: Promoter-proximal pausing and divergent transcription at promoters and enhancers, which are prominent features in animals, have been reported to be absent in plants based on a study of Arabidopsis thaliana. Here, our PRO-Seq analysis in cassava (Manihot esculenta) identified peaks of transcriptionally-engaged RNA polymerase II (Pol2) at both 5' and 3' ends of genes, consistent with paused or slowly-moving Pol2, and divergent transcription at potential intragenic enhancers. A full genome search for bi-directional transcription using an algorithm for enhancer detection developed in mammals (dREG) identified many enhancer candidates. These sites show distinct patterns of methylation and nucleotide variation based on genomic evolutionary rate profiling characteristic of active enhancers. Maize GRO-Seq data showed RNA polymerase occupancy at promoters and enhancers consistent with cassava but not Arabidopsis. Furthermore, putative enhancers in maize identified by dREG significantly overlapped with sites previously identified on the basis of open chromatin, histone marks, and methylation. We show that SNPs within these divergently transcribed intergenic regions predict significantly more variation in fitness and root composition than SNPs in chromosomal segments randomly ascertained from the same intergenic distribution, suggesting a functional importance of these sites on cassava. The findings shed new light on plant transcription regulation and its impact on development and plasticity.