A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica

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Authors

  • Louisa Heimann
  • Ina Horst
  • Renke Perduns
  • Björn Dreesen
  • Sascha Offermann
  • Christoph Peterhansel

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Details

Original languageEnglish
Pages (from-to)456-69
Number of pages14
JournalPlant physiology
Volume162
Issue number1
Publication statusPublished - May 2013

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 type-specific 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.

Keywords

    Acetylation, Gene Expression Regulation, Plant, Histone Code, Histones/genetics, Light, Methylation, Plant Proteins/genetics, Promoter Regions, Genetic/genetics, Setaria Plant/genetics, Sorghum/genetics, Species Specificity, Zea mays/genetics

Cite this

A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica. / Heimann, Louisa; Horst, Ina; Perduns, Renke et al.
In: Plant physiology, Vol. 162, No. 1, 05.2013, p. 456-69.

Research output: Contribution to journalArticleResearchpeer review

Heimann L, Horst I, Perduns R, Dreesen B, Offermann S, Peterhansel C. A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica. Plant physiology. 2013 May;162(1):456-69. doi: 10.1104/pp.113.216721
Heimann, Louisa ; Horst, Ina ; Perduns, Renke et al. / A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica. In: Plant physiology. 2013 ; Vol. 162, No. 1. pp. 456-69.
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title = "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 type-specific 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.",
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T1 - A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica

AU - Heimann, Louisa

AU - Horst, Ina

AU - Perduns, Renke

AU - Dreesen, Björn

AU - Offermann, Sascha

AU - Peterhansel, Christoph

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N2 - 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 type-specific 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.

AB - 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 type-specific 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.

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KW - Gene Expression Regulation, Plant

KW - Histone Code

KW - Histones/genetics

KW - Light

KW - Methylation

KW - Plant Proteins/genetics

KW - Promoter Regions, Genetic/genetics

KW - Setaria Plant/genetics

KW - Sorghum/genetics

KW - Species Specificity

KW - Zea mays/genetics

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DO - 10.1104/pp.113.216721

M3 - Article

C2 - 23564230

VL - 162

SP - 456

EP - 469

JO - Plant physiology

JF - Plant physiology

SN - 0032-0889

IS - 1

ER -

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