A Common Histone Modification Code on C4 Genes in Maize and Its Conservation in Sorghum and Setaria italica      

Abstract

C4 photosynthesis evolved more than 60 times independently in different plant lineages. Each time, multiple genes were recruited into C4 metabolism. The corresponding promoters acquired new regulatory features such as high expression, light induction, or cell typespecific expression in mesophyll or bundle sheath cells. We have previously shown that histone modifications contribute to the regulation of the model C4 phosphoenolpyruvate carboxylase (C4-Pepc) promoter in maize (Zea mays). We here tested the light-and cell type-specific responses of three selected histone acetylations and two histone methylations on five additional C4 genes (C4-Ca, C4-Ppdk, C4-Me, C4-Pepck, and C4-RbcS2) in maize. Histone acetylation and nucleosome occupancy assays indicated extended promoter regions with regulatory upstream regions more than 1,000 bp from the transcription initiation site for most of these genes. Despite any detectable homology of the promoters on the primary sequence level, histone modification patterns were highly coregulated. Specifically, H3K9ac was regulated by illumination, whereas H3K4me3 was regulated in a cell type-specific manner. We further compared histone modifications on the C4-Pepc and C4-Me genes from maize and the homologous genes from sorghum (Sorghum bicolor) and Setaria italica. Whereas sorghum and maize share a common C4 origin, C4 metabolism evolved independently in S. italica. The distribution of histone modifications over the promoters differed between the species, but differential regulation of light-induced histone acetylation and cell type-specific histone methylation were evident in all three species. We propose that a preexisting histone code was recruited into C4 promoter control during the evolution of C4 metabolism.

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

“…We verified this observation for five of the six genes by comparing ChIP-Seq data from this study with previously published chromatin immunoprecipitationquantitative polymerase chain reaction (ChIP-qPCR) data from our laboratory Heimann et al, 2013). An exemplary profile for ME is shown in Figure 6A, and data for four other genes are shown in Supplemental Figure S2.…”

Evolutionary Convergence of Cell-Specific Gene Expression in Independent Lineages of C4 Grasses

“…Because this sequence element is present in orthologous genes of C 3 Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa), the most parsimonious explanation is that these elements have repeatedly been coopted from an unknown ancestral function into generating BS specificity in C 4 leaves. Furthermore, the same chromatin marks have been documented on PEPC and NADP-ME genes in M and BS cells of both maize and Setaria italica (Heimann et al, 2013), showing that separate C 4 lineages regulate the expression of genes in either the M or BS cells via the same mechanisms in cis. However, the extent to which the expression of other genes and pathways in these cells resemble each other is not clear, nor is it known whether the same mechanisms in trans have been coopted by multiple C 4 lineages.…”

Histone Modification Patterns and Their Responses to Environment

“…With a recent large set of ChIP-seq data on humans and mice, similar approaches may be used to identify species-specific or conserved histone modification patterns in response to environmental factors. In plants, ChIP-qPCR results in H3K9ac showed similar dynamic patterns in maize and sorghum in response to light at the promoter regions of genes related to C4 metabolism despite no detectable homology at the DNA level [73]. D. Histone changes in short-term response vs. long-term response Highly dynamic changes in protein synthesis and gene expression are critical for organisms to respond promptly to deleterious environmental factors.…”