TY - JOUR A1 - Smaczniak, Cezary A1 - Muino, Jose M. A1 - Chen, Dijun A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Differences in DNA Binding Specificity of Floral Homeotic Protein Complexes Predict Organ-Specific Target Genes JF - The plant cell N2 - Floral organ identities in plants are specified by the combinatorial action of homeotic master regulatory transcription factors. However, how these factors achieve their regulatory specificities is still largely unclear. Genome-wide in vivo DNA binding data show that homeotic MADS domain proteins recognize partly distinct genomic regions, suggesting that DNA binding specificity contributes to functional differences of homeotic protein complexes. We used in vitro systematic evolution of ligands by exponential enrichment followed by high-throughput DNA sequencing (SELEX-seq) on several floral MADS domain protein homo-and heterodimers to measure their DNA binding specificities. We show that specification of reproductive organs is associated with distinct binding preferences of a complex formed by SEPALLATA3 and AGAMOUS. Binding specificity is further modulated by different binding site spacing preferences. Combination of SELEX-seq and genome-wide DNA binding data allows differentiation between targets in specification of reproductive versus perianth organs in the flower. We validate the importance of DNA binding specificity for organ-specific gene regulation by modulating promoter activity through targeted mutagenesis. Our study shows that intrafamily protein interactions affect DNA binding specificity of floral MADS domain proteins. Differential DNA binding of MADS domain protein complexes plays a role in the specificity of target gene regulation. Y1 - 2017 U6 - https://doi.org/10.1105/tpc.17.00145 SN - 1040-4651 SN - 1532-298X VL - 29 SP - 1822 EP - 1835 PB - American Society of Plant Physiologists CY - Rockville ER - TY - GEN A1 - Pajoro, Alice A1 - Madrigal, Pedro A1 - Muiño, Jose M. A1 - Matus, José Tomás A1 - Jin, Jian A1 - Mecchia, Martin A. A1 - Debernardi, Juan M. A1 - Palatnik, Javier F. A1 - Balazadeh, Salma A1 - Arif, Muhammad A1 - Ó’Maoiléidigh, Diarmuid S. A1 - Wellmer, Frank A1 - Krajewski, Pawel A1 - Riechmann, José-Luis A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development T2 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe N2 - 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. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 1327 KW - flower development KW - floral organ KW - floral meristem KW - chromatin accessibility KW - growth regulate factor Y1 - 2014 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-431139 SN - 1866-8372 VL - 15 ER - TY - JOUR A1 - Pajoro, Alice A1 - Madrigal, Pedro A1 - Muino, Jose M. A1 - Tomas Matus, Jose A1 - Jin, Jian A1 - Mecchia, Martin A. A1 - Debernardi, Juan M. A1 - Palatnik, Javier F. A1 - Balazadeh, Salma A1 - Arif, Muhammad A1 - Wellmer, Frank A1 - Krajewski, Pawel A1 - Riechmann, Jose-Luis A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development JF - Genome biology : biology for the post-genomic era N2 - 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. KW - Flower Development KW - Floral Organ KW - Floral Meristem KW - Chromatin Accessibility KW - Growth Regulate Factor Y1 - 2014 U6 - https://doi.org/10.1186/gb-2014-15-3-r41 SN - 1465-6906 SN - 1474-760X VL - 15 PB - BioMed Central CY - London ER - TY - JOUR A1 - Muiño, Jose M. A1 - de Bruijn, Suzanne A1 - Pajoro, Alice A1 - Geuten, Koen A1 - Vingron, Martin A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Evolution of DNA-Binding Sites of a Floral Master Regulatory Transcription Factor JF - Molecular biology and evolution : MBE N2 - lower development is controlled by the action of key regulatory transcription factors of the MADS-domain family. The function of these factors appears to be highly conserved among species based on mutant phenotypes. However, the conservation of their downstream processes is much less well understood, mostly because the evolutionary turnover and variation of their DNA-binding sites (BSs) among plant species have not yet been experimentally determined. Here, we performed comparative ChIP (chromatin immunoprecipitation)-seq experiments of the MADS-domain transcription factor SEPALLATA3 (SEP3) in two closely related Arabidopsis species: Arabidopsis thaliana and A. lyrata which have very similar floral organ morphology. We found that BS conservation is associated with DNA sequence conservation, the presence of the CArG-box BS motif and on the relative position of the BS to its potential target gene. Differences in genome size and structure can explain that SEP3 BSs in A. lyrata can be located more distantly to their potential target genes than their counterparts in A. thaliana. In A. lyrata, we identified transposition as a mechanism to generate novel SEP3 binding locations in the genome. Comparative gene expression analysis shows that the loss/gain of BSs is associated with a change in gene expression. In summary, this study investigates the evolutionary dynamics of DNA BSs of a floral key-regulatory transcription factor and explores factors affecting this phenomenon. KW - MADS-domain transcription factor KW - plant development KW - cis-regulatory evolution Y1 - 2015 U6 - https://doi.org/10.1093/molbev/msv210 SN - 1537-1719 SN - 0737-4038 VL - 33 IS - 1 PB - Oxford University Press CY - Oxford ER - TY - GEN A1 - Muiño, Jose M. A1 - de Bruijn, Suzanne A1 - Pajoro, Alice A1 - Geuten, Koen A1 - Vingron, Martin A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Evolution of DNA-Binding Sites of a Floral Master Regulatory Transcription Factor N2 - Flower development is controlled by the action of key regulatory transcription factors of the MADS-domain family. The function of these factors appears to be highly conserved among species based on mutant phenotypes. However, the conservation of their downstream processes is much less well understood, mostly because the evolutionary turnover and variation of their DNA-binding sites (BSs) among plant species have not yet been experimentally determined. Here, we performed comparative ChIP (chromatin immunoprecipitation)-seq experiments of the MADS-domain transcription factor SEPALLATA3 (SEP3) in two closely related Arabidopsis species: Arabidopsis thaliana and A. lyrata which have very similar floral organ morphology. We found that BS conservation is associated with DNA sequence conservation, the presence of the CArG-box BS motif and on the relative position of the BS to its potential target gene. Differences in genome size and structure can explain that SEP3 BSs in A. lyrata can be located more distantly to their potential target genes than their counterparts in A. thaliana. In A. lyrata, we identified transposition as a mechanism to generate novel SEP3 binding locations in the genome. Comparative gene expression analysis shows that the loss/gain of BSs is associated with a change in gene expression. In summary, this study investigates the evolutionary dynamics of DNA BSs of a floral key-regulatory transcription factor and explores factors affecting this phenomenon. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 261 KW - MADS-domain transcription factor KW - cis-regulatory evolution KW - plant development Y1 - 2015 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-96580 SP - 1225 EP - 1245 ER - TY - JOUR A1 - Muino, Jose M. A1 - de Bruijn, Suzanne A1 - Pajoro, Alice A1 - Geuten, Koen A1 - Vingron, Martin A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Evolution of DNA-Binding Sites of a Floral Master Regulatory Transcription Factor JF - Molecular biology and evolution N2 - Flower development is controlled by the action of key regulatory transcription factors of the MADS-domain family. The function of these factors appears to be highly conserved among species based on mutant phenotypes. However, the conservation of their downstream processes is much less well understood, mostly because the evolutionary turnover and variation of their DNA-binding sites (BSs) among plant species have not yet been experimentally determined. Here, we performed comparative ChIP (chromatin immunoprecipitation)-seq experiments of the MADS-domain transcription factor SEPALLATA3 (SEP3) in two closely related Arabidopsis species: Arabidopsis thaliana and A. lyrata which have very similar floral organ morphology. We found that BS conservation is associated with DNA sequence conservation, the presence of the CArG-box BS motif and on the relative position of the BS to its potential target gene. Differences in genome size and structure can explain that SEP3 BSs in A. lyrata can be located more distantly to their potential target genes than their counterparts in A. thaliana. In A. lyrata, we identified transposition as a mechanism to generate novel SEP3 binding locations in the genome. Comparative gene expression analysis shows that the loss/gain of BSs is associated with a change in gene expression. In summary, this study investigates the evolutionary dynamics of DNA BSs of a floral key-regulatory transcription factor and explores factors affecting this phenomenon. KW - MADS-domain transcription factor KW - cis-regulatory evolution KW - plant development Y1 - 2016 U6 - https://doi.org/10.1093/molbev/msv210 SN - 0737-4038 SN - 1537-1719 VL - 33 SP - 185 EP - 200 PB - Oxford Univ. Press CY - Oxford ER - TY - JOUR A1 - Bemer, Marian A1 - van Mourik, Hilda A1 - Muino, Jose M. A1 - Ferrandiz, Cristina A1 - Kaufmann, Kerstin A1 - Angenent, Gerco C. T1 - FRUITFULL controls SAUR10 expression and regulates Arabidopsis growth and architecture JF - Journal of experimental botany N2 - MADS-domain transcription factors are well known for their roles in plant development and regulate sets of downstream genes that have been uncovered by high-throughput analyses. A considerable number of these targets are predicted to function in hormone responses or responses to environmental stimuli, suggesting that there is a close link between developmental and environmental regulators of plant growth and development. Here, we show that the Arabidopsis MADS-domain factor FRUITFULL (FUL) executes several functions in addition to its noted role in fruit development. Among the direct targets of FUL, we identified SMALL AUXIN UPREGULATED RNA 10 (SAUR10), a growth regulator that is highly induced by a combination of auxin and brassinosteroids and in response to reduced R:FR light. Interestingly, we discovered that SAUR10 is repressed by FUL in stems and inflorescence branches. SAUR10 is specifically expressed at the abaxial side of these branches and this localized activity is influenced by hormones, light conditions and by FUL, which has an effect on branch angle. Furthermore, we identified a number of other genes involved in hormone pathways and light signalling as direct targets of FUL in the stem, demonstrating a connection between developmentally and environmentally regulated growth programs. KW - Architecture KW - auxin KW - branching KW - FRUITFULL KW - growth KW - hormones KW - light response KW - MADS-box transcription factor KW - SAUR Y1 - 2017 U6 - https://doi.org/10.1093/jxb/erx184 SN - 0022-0957 SN - 1460-2431 VL - 68 SP - 3391 EP - 3403 PB - Oxford Univ. Press CY - Oxford ER -