Photosynthetic Genes and Genes Associated with the C4 Trait in Maize Are Characterized by a Unique Class of Highly Regulated Histone Acetylation Peaks on Upstream Promoters  

Abstract

Histone modifications contribute to gene regulation in eukaryotes. We analyzed genome-wide histone H3 Lysine (Lys) 4 trimethylation and histone H3 Lys 9 acetylation (two modifications typically associated with active genes) in meristematic cells at the base and expanded cells in the blade of the maize (Zea mays) leaf. These data were compared with transcript levels of associated genes. For individual genes, regulations (fold changes) of histone modifications and transcript levels were much better correlated than absolute intensities. When focusing on regulated histone modification sites, we identified highly regulated secondary H3 Lys 9 acetylation peaks on upstream promoters (regulated secondary upstream peaks [R-SUPs]) on 10% of all genes. R-SUPs were more often found on genes that were up-regulated toward the blade than on down-regulated genes and specifically, photosynthetic genes. Among those genes, we identified six genes encoding enzymes of the C4 cycle and a significant enrichment of genes associated with the C4 trait derived from transcriptomic studies. On the DNA level, R-SUPs are frequently associated with ethylene-responsive elements. Based on these data, we suggest coevolution of epigenetic promoter elements during the establishment of C4 photosynthesis.

Characterization of maize leaf pyruvate orthophosphate dikinase using high throughput sequencing

“…In addition to the considerable information with respect to the biochemical action of the C 4 PPDK enzyme, recent work identified amino acid residues important in the regulation of C 4 PPDK activity (Chastain et al ; Chastain et al ; Chastain et al ; Chen et al ). On a different level, few studies have focused on mechanisms that control PPDK gene expression (Heimann et al ; Perduns et al ). In our work, we have identified a ppdk loss‐of‐function mutant with a transposon element inserted in an exon of both the C 4 PPDK and cyPPDKZm1 maize genes (Figure ).…”

“…Recent reports suggested histone modifications to play a role in the light response and cell type‐specific response of C 4 genes in monocots (Heimann et al ; Perduns et al ). Also, the importance of UTRs has been reported for cell type‐specific accumulation of carbonic anhydrase, PPDK and NADP‐ME in C 4 Cleome gynandra and Flaveria (Williams et al ).…”

Chromatin and Epigenetics

“…Interestingly, it was the breadth of the H3K4me3 islands that increased over time, indicating spreading of the mark out of the gene body as transcriptional activity increased. Monitoring the same two marks during the development of maize leaves, Perduns et al (2015) found that changes in transcript levels and histone marks were better correlated than absolute values. They also identified secondary histone H3 Lys-9 acetylation peaks farther upstream in the promoter regions that were strongly up-regulated in the leaf blade compared with the leaf base and occurred preferentially in genes with functions in C4 photosynthesis.…”

Emerging Roles and Landscape of Translating mRNAs in Plants

“…Several stress studies have used light measures and photosynthetic efficiency as a first point to understand plant responses to stress ( Dunaeva and Adamska, 2001 ; Soitamo et al, 2008 ). Previously, wide arrays of genes have been profiled in response to light stress in model and non-model species and attempts made to reveal the light-based regulation and evolution of C3–C4 biosynthetic cycle ( Perduns et al, 2015 ). Light-regulated responses occur diurnally with alternative light- and dark- phases.…”