The Expression Level of the Chromatin-Associated HMGB1 Protein Influences Growth, Stress Tolerance, and Transcriptome in Arabidopsis

Lildballe, Dorte Launholt; Pedersen, Dorthe Skou; Kalamajka, Rainer; Emmersen, Jeppe; Houben, Andreas; Grasser, Klaus D.

doi:10.1016/j.jmb.2008.09.014

Cited by 42 publications

(44 citation statements)

References 64 publications

(97 reference statements)

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“…bHLH proteins regulate stomatal development, leaf expansion, epidermal cell fate determination, and light responses (43). HMG proteins are involved in germination, seedling growth, and stress response (44,45). The top HMG gene was highly expressed through the entire 192-h time course, suggesting that it regulates multiple processes.…”

Section: Expression Dynamics Of Tf Gene Families During Germination Andmentioning

confidence: 99%

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

Chen²,

Chang³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up-and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development. maize transcriptomes | coexpressed genes | cis binding site M aize (Zea mays) is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, the regulatory network that controls maize leaf development is still not well understood. In fact, the number of known maize transcription factor (TF)-binding sites (TFBSs) is far smaller than that for Arabidopsis thaliana (1-3).To understand better the regulation of maize leaf development, several recent studies used next-generation sequencing (NGS) technologies to survey transcriptomic differences among maize leaf cell types and developmental stages. The first large-scale study was by Li et al. (7) investigated the transcriptomes of Kranz (i.e., the foliar leaf blade) and non-Kranz (the husk leaf sheath) maize leaves to identify cohorts of genes associated with procambium initiation and vascular patterning. Recently, Wang et al. (8) conducted comparative transcriptomic and metabolomic analyses of developing leaves in maize and rice and identified putative structural and regulatory components important for C4 and C3 photosynthesis. These studies provided insights into the regulatory mechanisms underlying the development of Kranz leaf anatomy in maize.In the present study, we obtained nine transcriptomes of the second leaf from 84-192 h post imbibition at 12-h (6:00 AM and 6:00 PM) or 24-h (6:00 PM only) intervals. Together with the 13 SignificanceMaize is a major crop and a model plant for studying C4 leaf development. However, its regulatory network of leaf ...

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Section: Expression Dynamics Of Tf Gene Families During Germination Andmentioning

confidence: 99%

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

Chen²,

Chang³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Histone-enriched protein was isolated as described (Lildballe et al, 2008), and immunoblot analysis was performed with antibodies against H4 symmetric dimethyl Arg 3 (Abcam; catalog number ab5823).…”

Section: Immunoblot Analysismentioning

confidence: 99%

ArabidopsisFloral Initiator SKB1 Confers High Salt Tolerance by Regulating Transcription and Pre-mRNA Splicing through Altering Histone H4R3 and Small Nuclear Ribonucleoprotein LSM4 Methylation

et al. 2011

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Plants adapt their growth and development in response to perceived salt stress. Although DELLA-dependent growth restraint is thought to be an integration of the plant's response to salt stress, little is known about how histone modification confers salt stress and, in turn, affects development. Here, we report that floral initiator Shk1 kinase binding protein1 (SKB1) and histone4 arginine3 (H4R3) symmetric dimethylation (H4R3sme2) integrate responses to plant developmental progress and salt stress. Mutation of SKB1 results in salt hypersensitivity, late flowering, and growth retardation. SKB1 associates with chromatin and thereby increases the H4R3sme2 level to suppress the transcription of FLOWERING LOCUS C (FLC) and a number of stress-responsive genes. During salt stress, the H4R3sme2 level is reduced, as a consequence of SKB1 disassociating from chromatin to induce the expression of FLC and the stress-responsive genes but increasing the methylation of small nuclear ribonucleoprotein Sm-like4 (LSM4). Splicing defects are observed in the skb1 and lsm4 mutants, which are sensitive to salt. We propose that SKB1 mediates plant development and the salt response by altering the methylation status of H4R3sme2 and LSM4 and linking transcription to pre-mRNA splicing.

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“…This finding clearly discriminates the 3xHMG-box proteins from other (plant) HMG-box proteins (e.g. Arabidopsis HMGB proteins and SSRP1) that interact with interphase chromatin but do not associate with mitotic chromosomes Launholt et al, 2006;Lildballe et al, 2008;Pedersen et al, 2010). 3xHMG-box2 generally binds the condensed chromosomes, whereas 3xHMG-box1 associates with specific chromosomal regions, representing the ribosomal DNA loci (Fig.…”

Section: Xhmg-box Proteinsmentioning

confidence: 72%

“…In line with that, plant HMG proteins traditionally were purified from chromatin or isolated nuclei (Spiker, 1984;Grasser et al, 1991). Systematic examination of the subcellular localization of Arabidopsis HMGB1, HMGB5, and HMGB6 proteins as well as of the HMGB-type protein AtHMGB14 by analyzing the distribution of GFP fusions and by immunofluorescence microscopy confirmed the nuclear localization Launholt et al, 2006;Lildballe et al, 2008). In contrast to these findings, recent experiments revealed that Arabidopsis HMGB2/3 and HMGB4, in addition to being found in the nucleus, are detected to different extents in the cytosol.…”

Section: Chromosomal Hmgb Proteinsmentioning

confidence: 89%

“…Transcript profiling of hmgb1 plants compared with control plants revealed that a large number of genes were differentially expressed. Among the downregulated genes, the Gene Ontology category of stressresponsive genes was overrepresented (Lildballe et al, 2008). Exposure of plants to abiotic stress conditions requires a switch in the gene expression program.…”

Section: Chromosomal Hmgb Proteinsmentioning

confidence: 99%

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Plant Proteins Containing High Mobility Group Box DNA-Binding Domains Modulate Different Nuclear Processes

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The Expression Level of the Chromatin-Associated HMGB1 Protein Influences Growth, Stress Tolerance, and Transcriptome in Arabidopsis

Cited by 42 publications

References 64 publications

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

ArabidopsisFloral Initiator SKB1 Confers High Salt Tolerance by Regulating Transcription and Pre-mRNA Splicing through Altering Histone H4R3 and Small Nuclear Ribonucleoprotein LSM4 Methylation

Plant Proteins Containing High Mobility Group Box DNA-Binding Domains Modulate Different Nuclear Processes

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