TY - JOUR A1 - Sharma, Neha A1 - Ruelens, Philip A1 - Maggen, Thomas A1 - Dochy, Niklas A1 - Torfs, Sanne A1 - Kaufmann, Kerstin A1 - Rohde, Antje A1 - Geuten, Koen T1 - A Flowering Locus C Homolog Is a Vernalization-Regulated Repressor in Brachypodium and Is Cold Regulated in Wheat JF - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants N2 - Winter cereals require prolonged cold to transition from vegetative to reproductive development. This process, referred to as vernalization, has been extensively studied in Arabidopsis (Arabidopsis thaliana). In Arabidopsis, a key flowering repressor called FLOWERING LOCUS C (FLC) quantitatively controls the vernalization requirement. By contrast, in cereals, the vernalization response is mainly regulated by the VERNALIZATION genes, VRN1 and VRN2. Here, we characterize ODDSOC2, a recently identified FLC ortholog in monocots, knowing that it belongs to the FLC lineage. By studying its expression in a diverse set of Brachypodium accessions, we find that it is a good predictor of the vernalization requirement. Analyses of transgenics demonstrated that BdODDSOC2 functions as a vernalization-regulated flowering repressor. In most Brachypodium accessions BdODDSOC2 is down-regulated by cold, and in one of the winter accessions in which this down-regulation was evident, BdODDSOC2 responded to cold before BdVRN1. When stably down-regulated, the mechanism is associated with spreading H3K27me3 modifications at the BdODDSOC2 chromatin. Finally, homoeolog-specific gene expression analyses identify TaAGL33 and its splice variant TaAGL22 as the FLC orthologs in wheat (Triticum aestivum) behaving most similar to Brachypodium ODDSOC2. Overall, our study suggests that ODDSOC2 is not only phylogenetically related to FLC in eudicots but also functions as a flowering repressor in the vernalization pathway of Brachypodium and likely other temperate grasses. These insights could prove useful in breeding efforts to refine the vernalization requirement of temperate cereals and adapt varieties to changing climates. Y1 - 2016 U6 - https://doi.org/10.1104/pp.16.01161 SN - 0032-0889 SN - 1532-2548 VL - 173 IS - 2 SP - 1301 EP - 1315 PB - American Society of Plant Physiologists CY - Rockville 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 - 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 - Ruelens, Philip A1 - de Maagd, Ruud A. A1 - Proost, Sebastian A1 - Theissen, Günther A1 - Geuten, Koen A1 - Kaufmann, Kerstin T1 - FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes JF - Nature Communications N2 - MADS-domain transcription factors have been shown to act as key repressors or activators of the transition to flowering and as master regulators of reproductive organ identities. Despite their important roles in plant development, the origin of several MADS-box subfamilies has remained enigmatic so far. Here we demonstrate, through a combination of genome synteny and phylogenetic reconstructions, the origin of three major, apparently angiosperm-specific MADS-box gene clades: FLOWERING LOCUS C- (FLC-), SQUAMOSA- (SQUA-) and SEPALLATA- (SEP-) -like genes. We find that these lineages derive from a single ancestral tandem duplication in a common ancestor of extant seed plants. Contrary to common belief, we show that FLC- like genes are present in cereals where they can also act as floral repressors responsive to prolonged cold or vernalization. This opens a new perspective on the translation of findings from Arabidopsis to cereal crops, in which vernalization was originally described. Y1 - 2013 U6 - https://doi.org/10.1038/ncomms3280 SN - 2041-1723 VL - 4 IS - 8 PB - Nature Publ. Group CY - London ER - TY - JOUR A1 - Ruelens, Philip A1 - Zhang, Zhicheng A1 - van Mourik, Hilda A1 - Maere, Steven A1 - Kaufmann, Kerstin A1 - Geuten, Koen T1 - The Origin of Floral Organ Identity Quartets JF - The plant cell N2 - The origin of flowers has puzzled plant biologists ever since Darwin referred to their sudden appearance in the fossil record as an abominable mystery. Flowers are considered to be an assembly of protective, attractive, and reproductive male and female leaf-like organs. Their origin cannot be understood by a morphological comparison to gymnosperms, their closest relatives, which develop separate male or female cones. Despite these morphological differences, gymnosperms and angiosperms possess a similar genetic toolbox consisting of phylogenetically related MADS domain proteins. Using ancestral MADS domain protein reconstruction, we trace the evolution of organ identity quartets along the stem lineage of crown angiosperms. We provide evidence that current floral quartets specifying male organ identity, which consist of four types of subunits, evolved from ancestral complexes of two types of subunits through gene duplication and integration of SEPALLATA proteins just before the origin of flowering plants. Our results suggest that protein interaction changes underlying this compositional shift were the result of a gradual and reversible evolutionary trajectory. Modeling shows that such compositional changes may have facilitated the evolution of the perfect, bisexual flower. Y1 - 2017 U6 - https://doi.org/10.1105/tpc.16.00366 SN - 1040-4651 SN - 1532-298X VL - 29 IS - 2 SP - 229 EP - 242 PB - American Society of Plant Physiologists CY - Rockville ER -