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Title: A genome-wide regulatory framework identifies maize Pericarp Color1 (P1) controlled genes

Author
item MOROHASHI, KENGO - The Ohio State University
item CASAS, MARIA - The Ohio State University
item FALCONE-FERREYRA, LORENA - National University Of Rosario
item YILMAZ, ALPER - The Ohio State University
item POURCEL, LUCILLE - University Of Geneva
item GUERRA, MARIA - The Ohio State University
item McMullen, Michael
item GROTEWOLD, ERICH - The Ohio State University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/2/2012
Publication Date: 7/20/2012
Citation: Morohashi, K., Casas, M., Falcone-Ferreyra, L., Yilmaz, A., Pourcel, L., Guerra, M., McMullen, M.D., Grotewold, E. 2012. A genome-wide regulatory framework identifies maize Pericarp Color1 (P1) controlled genes. The Plant Cell. 24:2745-2764.

Interpretive Summary: The P1 gene encodes a regulatory protein responsible for the accumulation of insecticidal flavones in maize silks and red pigments in specific tissues of maize kernels. Using genome-wide expression analyses in pericarps (outer kernel layer) and silks of plants with contrasting functional P1 genes combined with global chromatin binding experiments it was shown that that the regulatory functions of P1 are much broader than the activation of genes corresponding to enzymes in a branch of flavonoid biosynthesis leading to the red pigments and flavones. P1 modulates the expression of several thousand genes, and ~1,500 of them were identified as P1 direct DNA binding targets. These results indicate that P1 is the major regulator for a set of genes involved in flavonoid biosynthesis, and a minor modulator of the expression of a much larger gene set, which includes both primary metabolism as well as other specialized compounds. This result is important to geneticists and plant breeders in showing how regulators of specific pathways may impact gene expression in many other pathways potentially affecting trait expression.

Technical Abstract: P1 encodes an R2R3-MYB transcription factor responsible for the accumulation of insecticidal flavones in maize silks and red phlobaphene pigments in pericarps and other floral tissues. Using genome-wide expression analyses (RNA-Seq) in pericarps and silks of plants with contrasting P1 alleles combined with chromatin immunoprecipitation coupled with high throughput sequencing (ChIP-Seq), we show here that the regulatory functions of P1 are much broader than the activation of genes corresponding to enzymes in a branch of flavonoid biosynthesis. P1 modulates the expression of several thousand genes, and ~1,500 of them were identified as P1 direct targets. Among these genes, we identified ZmF2H1, corresponding to a P450 enzyme that converts naringenin into 2-hydroxynaringenin, a key branch point in the P1-controlled pathway and the first step in the formation of insecticidal C-glycosylflavones. P1 also directly controls the expression of many transcription factors, suggesting that it functions both high and low in a hierarchical gene regulatory network. Our results indicate that P1 is the major regulator for a set of genes involved in flavonoid biosynthesis, and a minor modulator of the expression of a much larger gene set, which includes both primary metabolism as well as other specialized compounds.