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Open Access Research

Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development

Alice Pajoro1, Pedro Madrigal2, Jose M Muiño3, José Tomás Matus4, Jian Jin4, Martin A Mecchia5, Juan M Debernardi5, Javier F Palatnik5, Salma Balazadeh6, Muhammad Arif6, Diarmuid S Ó’Maoiléidigh7, Frank Wellmer7, Pawel Krajewski2, José-Luis Riechmann48*, Gerco C Angenent19 and Kerstin Kaufmann16*

Author Affiliations

1 Laboratory of Molecular Biology, Wageningen University, 6708PB Wageningen, The Netherlands

2 Institute of Plant Genetics, Polish Academy of Sciences, 60-479 Poznań, Poland

3 Max-Planck Institute for Molecular Genetics, Department of Computational Molecular Biology, Ihnestraße 63-73, 14195 Berlin, Germany

4 Center for Research in Agricultural Genomics-CSIC-IRTA-UAB-UB, Campus UAB, 08193 Bellaterra, Barcelona, Spain

5 IBR (Instituto de Biología Molecular y Celular de Rosario), Facultad de Ciencias Bioquímicas y Farmacéuticas, UNR, Suipacha 531, 2000 Rosario, Argentina

6 Institute of Biochemistry and Biology, University of Potsdam, Potsdam 14476, Germany

7 Trinity College Dublin, Smurfit Institute of Genetics, Dublin 2, Ireland

8 Institució Catalana de Recerca i Estudis Avançats-ICREA, Barcelona 08010, Spain

9 Business Unit Bioscience, Plant Research International, Wageningen 6700AP, The Netherlands

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Genome Biology 2014, 15:R41  doi:10.1186/gb-2014-15-3-r41

Published: 3 March 2014

Abstract

Background

Development of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood.

Results

We characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes.

Conclusions

Our findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility.