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Alterations of histone modifications at the senescence-associated gene HvS40 in barley during senescence

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Abstract

The barley gene HvS40, encoding a putative regulator of leaf senescence, is strongly induced during leaf senescence. As shown by chromatin immunoprecipitation, euchromatic histone modification H3K9ac is added at promoter close to ATG and coding sequence of HvS40 after onset of senescence. In parallel, level of heterochromatic H3K9me2 decreases at this gene. Bisulfite sequencing revealed no DNA-methylation in this region, but a heavily methylated DNA-island, starting 664 bp upstream from translational start site in both, mature and senescent leaves. A decrease in DNA methylation in senescing leaves could be shown at one specific CpG motif at the end of this methylation island. In addition, global changes in chromatin structure during senescence were analyzed via immunocytology, revealing senescence-associated changes in spatial distribution of heterochromatic H3K9me2 patterns in the nuclei. Our results prove a senescence-specific mechanism, altering histone modification marks at distinct sequences of the senescence-associated gene HvS40 and altering distribution of heterochromatic areas in the nuclei.

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Acknowledgments

We thank Katrin Kittlaus and Carola Kretschmer for her technical support during the sequencing procedure of the bisulfite clones. This work was supported by the German Research Foundation (DFG, Hu 376/13-2 and SFB 648).

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    Authors and Affiliations

    1. Department of Plant Physiology, Institute of Biology, Martin-Luther University Halle-Wittenberg, Weinbergweg 10, 06120, Halle, Germany

      Nicole Ay, Bianka Janack & Klaus Humbeck

    2. Department of Genetics, Institute of Biology, Martin-Luther University Halle-Wittenberg, Weinbergweg 10, 06120, Halle, Germany

      Andreas Fischer & Gunter Reuter

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    Correspondence to Klaus Humbeck.

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    Nicole Ay and Bianka Janack have contributed equally to the work.

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    Figure S1

    Immunohistochemical analyses of senescence-specific nuclear distribution of the euchromatic H3K9ac histone modification during senescence in Arabidopsis thaliana. Nuclei were isolated of three different developmental stages as described in Ay et al. (2009). Representative DAPI-stained nuclei are shown in the upper part. The green fluorescence of the immunodecorated histone modification H3K9ac in these nuclei is shown in the middle part. The corresponding merged DAPI and immunofluorescence pictures are shown in the lower part. Scale bars: 10 µm (JPEG 145 kb)

    Figure S2

    DNA methylation pattern of the HvS40 fragment S40-asP in mature and senescent barley primary leaves. Position of the S40-asP fragment analyzed via bisulfite sequencing at the antisense strand of the distal promoter region of HvS40 is shown in the upper part. DNA methylation pattern of the S40-asP fragment in both investigated developmental stages is shown in the lower part. Ten representative clones from two technical replicates are shown. Each line represents one unique ‘‘non-sister’’ individual bisulfite sequencing result. Only cytosines are depicted. Red circles, blue rectangles and green triangles represent cytosines in the CpG, CpHpG or the CpHpH context, respectively. Methylated cytosines are depicted as filled and non-methylated cytosines as unfilled symbols. The numbers below give the Position of the cytosines in the analyzed fragment (JPEG 1243 kb)

    Figure S3

    DNA methylation pattern of the HvS40 fragment S40-sPII in mature and senescent barley primary leaves. Position of the S40-sPII fragment analyzed via bisulfite sequencing at the sense strand of the promoter region of HvS40 is shown in the upper part. DNA methylation pattern of the S40-sPII fragment in both investigated developmental stages is shown in the lower part. Ten representative clones from two technical replicates are shown. Each line represents one unique ‘‘non-sister’’ individual bisulfite sequencing result. Only cytosines are depicted. Red circles, blue rectangles and green triangles represent cytosines in the CpG, CpHpG or the CpHpH context, respectively. Methylated cytosines are depicted as filled and non-methylated cytosines as unfilled symbols. The numbers below give the Position of the cytosines in the analyzed fragment (JPEG 1208 kb)

    Figure S4

    DNA methylation pattern of the HvS40 fragment S40-sC in mature and senescent barley primary leaves. Position of the S40-sC fragment analyzed via bisulfite sequencing at the sense strand of HvS40 is shown in the upper part. DNA methylation pattern of the S40-sC fragment is shown for both investigated developmental stages and also for non-methylated plasmid DNA (Control) in the lower part. Ten representative clones from either four (M and S2) or two (Control) biological replicates are shown. Each line represents one unique ‘‘non-sister’’ individual bisulfite sequencing result. Only cytosines are depicted. Red circles, blue rectangles and green triangles represent cytosines in the CpG, CpHpG or the CpHpH context, respectively. Methylated cytosines are depicted as filled and non-methylated cytosines as unfilled symbols. The numbers below give the Position of the cytosines in the analyzed fragment (JPEG 1774 kb)

    Figure S5

    DNA methylation pattern of the hordein gene HvHOR2 (Acc.no X03103) promoter fragment in mature and senescent barley primary leaves. Position of the HvHOR2 fragment analyzed via bisulfite sequencing at the sense strand of the distal promoter region of HvHOR2 is shown in the upper part. DNA methylation pattern of the HvHOR2 fragment is shown for both investigated developmental stages and also for non-methylated plasmid DNA (Control) in the lower part. Ten representative clones from either four (M and S2) or two (Control) biological replicates are shown. Each line represents one unique ‘‘non-sister’’ individual bisulfite sequencing result. Only cytosines are depicted. Red circles, blue rectangles and green triangles represent cytosines in the CpG, CpHpG or the CpHpH context, respectively. Methylated cytosines are depicted as filled and non-methylated cytosines as unfilled symbols. The numbers below give the Position of the cytosines in the analyzed fragment (JPEG 1570 kb)

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    Ay, N., Janack, B., Fischer, A. et al. Alterations of histone modifications at the senescence-associated gene HvS40 in barley during senescence. Plant Mol Biol 89, 127–141 (2015). https://doi.org/10.1007/s11103-015-0358-2

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