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

Abstract

BackgroundDevelopment 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.ResultsWe 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.ConclusionsOur 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.

MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution

“…This may explain the observed removal of the H3K27me3 inhibitory histone mark and, consequently, activation of SEP3, possibly by antagonizing Polycomb Group (PcG)-mediated transcriptional repression (Smaczniak et al, 2012b). It was also shown that AP1 and SEP3 bind to enhancer sites very early during flower development and that chromatin accessibility changes only subsequently, suggesting that SEP3 acts as a pioneer transcription factor (PTF, see Glossary, Box 1) that modifies chromatin accessibility (Pajoro et al, 2014). PTFs are by definition able to bind to inaccessible, nucleosome-associated DNA sites, thus creating an open chromatin environment that is permissive for the binding of non-pioneer factors that can only bind to accessible sites (termed 'settlers' if they almost always bind to sites matching their DNA-binding motif, and 'migrants' if they are more selective, e.g.…”

Determinants of nucleosome positioning and their influence on plant gene expression

“…5D, bottom) that may act as repressors (Richter et al 2010;Franco-Zorrilla et al 2014). Alternatively, some trans-acting factors may bind to their binding sites regardless of chromatin status as shown in studies of A. thaliana APETALA1 and SEPALLATA3 (Pajoro et al 2014). Some TFs have also been shown to preferentially bind nucleosome-occupied regions (Teif et al 2012;Ballare et al 2013).…”

Genome-Wide Targets Regulated by the OsMADS1 Transcription Factor Reveals Its DNA Recognition Properties

“…We find that the rice AP2-like factor gene Os04g55560 is directly and negatively regulated by OsMADS1. Whereas Arabidopsis AP2 locus is bound by SEP3, it is apparently not transcriptionally regulated (Pajoro et al, 2014b). We suggest that the rice AP2-like and PLETHORA-like factors are OsMADS1 targets in an intricate gene regulatory network.…”

“…Its closest Arabidopsis ortholog is ANT, which plays important roles in floral meristems, organ patterning, and particularly ovule and gametophyte development (Krizek, 2009;Klucher et al, 1996;Yamaguchi et al, 2016). Moreover, Arabidopsis SEP3 also directly influences ANT expression in differentiating Arabidopsis floral organs (Pajoro et al, 2014b). Rice has five genes closely related to Arabidopsis AP2 (Tang et al, 2007), including SUPERNUMERARY BRACT and INDETERMINATE SPIKELET1, mutants of which indicate critical roles in rice FM specification and floret organ development (Lee and An, 2012).…”