Business Unit Bioscience

Wageningen, Netherlands

Business Unit Bioscience

Wageningen, Netherlands
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Pajoro A.,Wageningen University | Madrigal P.,Polish Academy of Sciences | Muino J.M.,Max Planck Institute for Molecular Genetics | Matus J.T.,Center for Research in Agricultural Genomics UAB UB | And 15 more authors.
Genome Biology | Year: 2014

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. © 2014 Pajoro et al.; licensee BioMed Central Ltd.

Czerednik A.,Radboud University Nijmegen | Czerednik A.,University Utrecht | Busscher M.,Business Unit Bioscience | Bielen B.A.M.,Radboud University Nijmegen | And 4 more authors.
Journal of Experimental Botany | Year: 2012

Growth of tomato fruits is determined by cell division and cell expansion, which are tightly controlled by factors that drive the core cell cycle. The cyclin-dependent kinases (CDKs) and their interacting partners, the cyclins, play a key role in the progression of the cell cycle. In this study the role of CDKA1, CDKB1, and CDKB2 in fruit development was characterized by fruit-specific overexpression and down-regulation. CDKA1 is expressed in the pericarp throughout development, but is strongly up-regulated in the outer pericarp cell layers at the end of the growth period, when CDKB gene expression has ceased. Overexpression of the CDKB genes at later stages of development and the down-regulation of CDKA1 result in a very similar fruit phenotype, showing a reduction in the number of cell layers in the pericarp and alterations in the desiccation of the fruits. Expression studies revealed that CDKA1 is down-regulated by the expression of CDKB1/2 in CDKB1 and CDKB2 overexpression mutants, suggesting opposite roles for these types of CDK proteins in tomato pericarp development. © 2012 The Author.

Karlova R.,University Utrecht | Karlova R.,Wageningen University | Chapman N.,University of Nottingham | David K.,University of Auckland | And 5 more authors.
Journal of Experimental Botany | Year: 2014

Fleshy fruits have evolved to be attractive to frugivores in order to enhance seed dispersal, and have become an indispensable part of the human diet. Here we review the recent advances in the understanding of transcriptional regulation of fleshy fruit development and ripening with a focus on tomato. While aspects of fruit development are probably conserved throughout the angiosperms, including the model plant Arabidopsis thaliana, it is shown that the likely orthologues of Arabidopsis genes have distinct functions in fleshy fruits. The model for the study of fleshy fruit development is tomato, because of the availability of single gene mutants and transgenic knock-down lines. In other species, our knowledge is often incomplete or absent. Tomato fruit size and shape are co-determined by transcription factors acting during formation of the ovary. Other transcription factors play a role in fruit chloroplast formation, and upon ripening impact quality aspects such as secondary metabolite content. In tomato, the transcription factors NON-RIPENING (NOR), COLORLESS NON-RIPENING (CNR), and RIPENING INHIBITOR (MADS-RIN) in concert with ethylene signalling regulate ripening, possibly in response to a developmental switch. Additional components include TOMATO AGAMOUS-LIKE1 (TAGL1), APETALA2a (AP2a), and FRUITFULL (FUL1 and FUL2). The links between this highly connected regulatory network and downstream effectors modulating colour, texture, and flavour are still relatively poorly understood. Intertwined with this network is post-transcriptional regulation by fruit-expressed microRNAs targeting several of these transcription factors. This important developmental process is also governed by changes in DNA methylation levels and possibly chromatin remodelling. © 2014 The Author 2014.

Bemer M.,Radboud University Nijmegen | Bemer M.,University of Zürich | Karlova R.,Business Unit Bioscience | Karlova R.,Wageningen University | And 14 more authors.
Plant Cell | Year: 2012

Tomato (Solanum lycopersicum) contains two close homologs of the Arabidopsis thaliana MADS domain transcription factor FRUITFULL (FUL), FUL1 (previously called TDR4) and FUL2 (previously MBP7). Both proteins interact with the ripening regulator RIPENING INHIBITOR (RIN) and are expressed during fruit ripening. To elucidate their function in tomato, we characterized single and double FUL1 and FUL2 knockdown lines. Whereas the single lines only showed very mild alterations in fruit pigmentation, the double silenced lines exhibited an orange-ripe fruit phenotype due to highly reduced lycopene levels, suggesting that FUL1 and FUL2 have a redundant function in fruit ripening. More detailed analyses of the phenotype, transcriptome, and metabolome of the fruits silenced for both FUL1 and FUL2 suggest that the genes are involved in cell wall modification, the production of cuticle components and volatiles, and glutamic acid (Glu) accumulation. Glu is responsible for the characteristic umami taste of the present-day cultivated tomato fruit. In contrast with previously identified ripening regulators, FUL1 and FUL2 do not regulate ethylene biosynthesis but influence ripening in an ethylene-independent manner. Our data combined with those of others suggest that FUL1/2 and TOMATO AGAMOUS-LIKE1 regulate different subsets of the known RIN targets, probably in a protein complex with the latter. © 2012 American Society of Plant Biologists.

Kaufmann K.,Business Unit Bioscience | Nagasaki M.,Tokyo Medical University | Jauregui R.,BIOBASE GmbH
In Silico Biology | Year: 2010

We present a dynamical model of the gene network controlling flower development in Arabidopsis thaliana. The network is centered at the regulation of the floral organ identity genes (AP1, AP2, AP3, PI and AG) and ends with the transcription factor complexes responsible for differentiation of floral organs. We built and simulated the regulatory interactions that determine organ specificity using an extension of hybrid Petri nets as implemented in Cell Illustrator. The network topology is characterized by two main features: (1) the presence of multiple autoregulatory feedback loops requiring the formation of protein complexes, and (2) the role of spatial regulators determining floral patterning. The resulting network shows biologically coherent expression patterns for the involved genes, and simulated mutants produce experimentally validated changes in organ expression patterns. The requirement of heteromeric higher-order protein complex formation for positive autoregulatory feedback loops attenuates stochastic fluctuations in gene expression, enabling robust organ-specific gene expression patterns. If autoregulation is mediated by monomers or homodimers of proteins, small variations in initial protein levels can lead to biased production of homeotic proteins, ultimately resulting in homeosis. We also suggest regulatory feedback loops involving miRNA loci by which homeotic genes control the activity of their spatial regulators. © 2010-IOS Press and Bioinformation Systems e.V. and the authors. All rights reserved.

Karlova R.,Wageningen University | Karlova R.,Business Unit Bioscience | Karlova R.,University Utrecht | Van Haarst J.C.,Business Unit Bioscience | And 12 more authors.
Journal of Experimental Botany | Year: 2013

MicroRNAs (miRNAs) play important roles in plant development through regulation of gene expression by mRNA degradation or translational inhibition. Despite the fact that tomato (Solanum lycopersicum) is the model system for studying fleshy fruit development and ripening, only a few experimentally proven miRNA targets are known, and the role of miRNA action in these processes remains largely unknown. Here, by using parallel analysis of RNA ends (PARE) for global identification of miRNA targets and comparing four different stages of tomato fruit development, a total of 119 target genes of miRNAs were identified. Of these, 106 appeared to be new targets. A large part of the identified targets (56) coded for transcription factors. Auxin response factors, as well as two known ripening regulators, COLORLESS NON-RIPENING (CNR) and APETALA2a (SlAP2a), with developmentally regulated degradation patterns were identified. The levels of the intact messenger of both CNR and AP2a are actively modulated during ripening, by miR156/157 and miR172, respectively. Additionally, two TAS3-mRNA loci were identified as targets of miR390. Other targets such as ARGONAUTE 1 (AGO1), shown to be involved in miRNA biogenesis in other plant species, were identified, which suggests a feedback loop regulation of this process. In this study, it is shown that miRNA-guided cleavage of mRNAs is likely to play an important role in tomato fruit development and ripening. © The Author(s) [2013].

Karlova R.,Wageningen University | Rosin F.M.,Business Unit Bioscience | Rosin F.M.,Harvard University | Busscher-Lange J.,Business Unit Bioscience | And 9 more authors.
Plant Cell | Year: 2011

Fruit ripening in tomato (Solanum lycopersicum) requires the coordination of both developmental cues as well as the plant hormone ethylene. Although the role of ethylene in mediating climacteric ripening has been established, knowledge regarding the developmental regulators that modulate the involvement of ethylene in tomato fruit ripening is still lacking. Here, we show that the tomato APETALA2a (AP2a) transcription factor regulates fruit ripening via regulation of ethylene biosynthesis and signaling. RNA interference (RNAi)-mediated repression of AP2a resulted in alterations in fruit shape, orange ripe fruits, and altered carotenoid accumulation. Microarray expression analyses of the ripe AP2 RNAi fruits showed altered expression of genes involved in various metabolic pathways, such as the phenylpropanoid and carotenoid pathways, as well as in hormone synthesis and perception. Genes involved in chromoplast differentiation and other ripening-associated processes were also differentially expressed, but softening and ethylene biosynthesis occurred in the transgenic plants. Ripening regulators RIPENING-INHIBITOR, NON-RIPENING, and COLORLESS NON-RIPENING (CNR) function upstream of AP2a and positively regulate its expression. In the pericarp of AP2 RNAi fruits, mRNA levels of CNR were elevated, indicating that AP2a and CNR are part of a negative feedback loop in the regulation of ripening. Moreover, we demonstrated that CNR binds to the promoter of AP2a in vitro. © 2011 American Society of Plant Biologists.

Ruelens P.,Catholic University of Leuven | De Maagd R.A.,Business Unit Bioscience | Proost S.,University of Potsdam | Proost S.,Max Planck Institute of Molecular Plant Physiology | And 3 more authors.
Nature Communications | Year: 2013

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. © 2013 Macmillan Publishers Limited. All rights reserved.

Bemer M.,Radboud University Nijmegen | Gordon J.,Ghent University | Weterings K.,Radboud University Nijmegen | Angenent G.C.,Radboud University Nijmegen | Angenent G.C.,Business Unit Bioscience
Molecular Biology and Evolution | Year: 2010

The MADS-box transcription factor family has expanded considerably in plants via gene and genome duplications and can be subdivided into type I and MIKC-type genes. The two gene classes show a different evolutionary history. Whereas the MIKC-type genes originated during ancient genome duplications, as well as during more recent events, the type I loci appear to experience high turnover with many recent duplications. This different mode of origin also suggests a different fate for the type I duplicates, which are thought to have a higher chance to become silenced or lost from the genome. To get more insight into the evolution of the type I MADS-box genes, we isolated nine type I genes from Petunia, which belong to the Mγ subclass, and investigated the divergence of their coding and regulatory regions. The isolated genes could be subdivided into two categories: two genes were highly similar to Arabidopsis Mγ-type genes, whereas the other seven genes showed less similarity to Arabidopsis genes and originated more recently. Two of the recently duplicated genes were found to contain deleterious mutations in their coding regions, and expression analysis revealed that a third paralog was silenced by mutations in its regulatory region. However, in addition to the three genes that were subjected to nonfunctionalization, we also found evidence for neofunctionalization of one of the Petunia Mγ-type genes. Our study shows a rapid divergence of recently duplicated Mγ-type MADS-box genes and suggests that redundancy among type I paralogs may be less common than expected.

Ruyter-Spira C.,Wageningen University | Ruyter-Spira C.,Business Unit Bioscience | Al-Babili S.,Albert Ludwigs University of Freiburg | Al-Babili S.,King Abdullah University of Science and Technology | And 4 more authors.
Trends in Plant Science | Year: 2013

The strigolactones are rhizosphere signaling molecules as well as a new class of plant hormones with a still increasing number of biological functions being uncovered. Here, we review a recent major breakthrough in our understanding of strigolactone biosynthesis, which has revealed the unexpected simplicity of the originally postulated complex pathway. Moreover, the discovery and localization of a strigolactone exporter sheds new light on putative strigolactone fluxes to the rhizosphere as well as within the plant. The combination of these data with information on the expression and regulation of strigolactone biosynthetic and downstream signaling genes provides new insights into how strigolactones control the many different aspects of plant development and how their rhizosphere signaling role may have evolved. © 2012 Elsevier Ltd.

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