@Article{IPB-2160, author = {Ibañez, C. and Delker, C. and Martinez, C. and Bürstenbinder, K. and Janitza, P. and Lippmann, R. and Ludwig, W. and Sun, H. and James, G. V. and Klecker, M. and Grossjohann, A. and Schneeberger, K. and Prat, S. and Quint, M.}, title = {{Brassinosteroids Dominate Hormonal Regulation of Plant Thermomorphogenesis via BZR1}}, year = {2018}, pages = {303-310.e3}, journal = {Curr Biol}, doi = {10.1016/j.cub.2017.11.077}, url = {http://www.cell.com/current-biology/abstract/S0960-9822(17)31602-0}, volume = {28}, abstract = {Thermomorphogenesis is defined as the suite of morphological changes that together are likely to contribute to adaptive growth acclimation to usually elevated ambient temperature [ 1, 2 ]. While many details of warmth-induced signal transduction are still elusive, parallels to light signaling recently became obvious (reviewed in [ 3 ]). It involves photoreceptors that can also sense changes in ambient temperature [ 3–5 ] and act, for example, by repressing protein activity of the central integrator of temperature information PHYTOCHROME-INTERACTING FACTOR 4 (PIF4 [ 6 ]). In addition, PIF4 transcript accumulation is tightly controlled by the evening complex member EARLY FLOWERING 3 [ 7, 8 ]. According to the current understanding, PIF4 activates growth-promoting genes directly but also via inducing auxin biosynthesis and signaling, resulting in cell elongation. Based on a mutagenesis screen in the model plant Arabidopsis thaliana for mutants with defects in temperature-induced hypocotyl elongation, we show here that both PIF4 and auxin function depend on brassinosteroids. Genetic and pharmacological analyses place brassinosteroids downstream of PIF4 and auxin. We found that brassinosteroids act via the transcription factor BRASSINAZOLE RESISTANT 1 (BZR1), which accumulates in the nucleus at high temperature, where it induces expression of growth-promoting genes. Furthermore, we show that at elevated temperature BZR1 binds to the promoter of PIF4, inducing its expression. These findings suggest that BZR1 functions in an amplifying feedforward loop involved in PIF4 activation. Although numerous negative regulators of PIF4 have been described, we identify BZR1 here as a true temperature-dependent positive regulator of PIF4, acting as a major growth coordinator.} } @Article{IPB-2192, author = {Nishiyama, T. and Sakayama, H. and de Vries, J. and Buschmann, H. and Saint-Marcoux, D. and Ullrich, K. K. and Haas, F. B. and Vanderstraeten, L. and Becker, D. and Lang, D. and Vosolsobě, S. and Rombauts, S. and Wilhelmsson, P. K. I. and Janitza, P. and Kern, R. and Heyl, A. and Rümpler, F and Calderón Villalobos, L. I. A. and Clay, J. M. and Skokan, R. and Toyoda, A. and Suzuki, Y. and Kagoshima, H. and Schijlen, E. and Tajeshwar, N. and Catarino, B. and Hetherington, A. J. and Saltykova, A. and Bonnot, C. and Breuninger, H. and Symeonidi, A. and Radhakrishnan, G. V. and Van Nieuwerburgh, F. and Deforce, D. and Chang, C. and Karol, K. G. and Hedrich, R. and Ulvskov, P. and Glöckner, G. and Delwiche, C. F. and Petrášek, J. and Van de Peer, Y. and Friml, J. and Beilby, M. and Dolan, L. and Kohara, Y. and Sugano, S. and Fujiyama, A. and Delaux, P.-M. and Quint, M. and Theißen, G. and Hagemann, M. and Harholt, J. and Dunand, C. and Zachgo, S. and Langdale, J. and Maumus, F. and Van Der Straeten, D. and Gould, S. B. and Rensing, S. A.}, title = {{The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization}}, year = {2018}, pages = {448-464.e24}, journal = {Cell}, doi = {10.1016/j.cell.2018.06.033}, url = {https://www.sciencedirect.com/science/article/pii/S0092867418308018}, volume = {174}, abstract = {Land plants evolved from charophytic algae, among which Charophyceae possess the most complex body plans. We present the genome of Chara braunii; comparison of the genome to those of land plants identified evolutionary novelties for plant terrestrialization and land plant heritage genes. C. braunii employs unique xylan synthases for cell wall biosynthesis, a phragmoplast (cell separation) mechanism similar to that of land plants, and many phytohormones. C. braunii plastids are controlled via land-plant-like retrograde signaling, and transcriptional regulation is more elaborate than in other algae. The morphological complexity of this organism may result from expanded gene families, with three cases of particular note: genes effecting tolerance to reactive oxygen species (ROS), LysM receptor-like kinases, and transcription factors (TFs). Transcriptomic analysis of sexual reproductive structures reveals intricate control by TFs, activity of the ROS gene network, and the ancestral use of plant-like storage and stress protection proteins in the zygote.} } @Article{IPB-2091, author = {Winkler, M. and Niemeyer, M. and Hellmuth, A. and Janitza, P. and Christ, G. and Samodelov, S. L. and Wilde, V. and Majovsky, P. and Trujillo, M. and Zurbriggen, M. D. and Hoehenwarter, W. and Quint, M. and Calderón Villalobos, L. I. A.}, title = {{Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction.}}, year = {2017}, pages = {15706}, journal = { Nature Commun.}, doi = {10.1038/ncomms15706}, url = {https://www.nature.com/articles/ncomms15706}, volume = {8}, abstract = {Auxin is a small molecule morphogen that bridges SCFTIR1/AFB-AUX/IAA co-receptor interactions leading to ubiquitylation and proteasome-dependent degradation of AUX/IAA transcriptional repressors. Here, we systematically dissect auxin sensing by SCFTIR1-IAA6 and SCFTIR1-IAA19 co-receptor complexes, and assess IAA6/IAA19 ubiquitylation in vitro and IAA6/IAA19 degradation in vivo. We show that TIR1-IAA19 and TIR1-IAA6 have distinct auxin affinities that correlate with ubiquitylation and turnover dynamics of the AUX/IAA. We establish a system to track AUX/IAA ubiquitylation in IAA6 and IAA19 in vitro and show that it occurs in flexible hotspots in degron-flanking regions adorned with specific Lys residues. We propose that this signature is exploited during auxin-mediated SCFTIR1-AUX/IAA interactions. We present evidence for an evolving AUX/IAA repertoire, typified by the IAA6/IAA19 ohnologues, that discriminates the range of auxin concentrations found in plants. We postulate that the intrinsic flexibility of AUX/IAAs might bias their ubiquitylation and destruction kinetics enabling specific auxin responses.} } @Article{IPB-1934, author = {Drost, H.-G. and Bellstädt, J. and Ó'Maoiléidigh, D. S. and Silva, A. T. and Gabel, A. and Weinholdt, C. and Ryan, P. T. and Dekkers, B. J. W. and Bentsink, L. and Hilhorst, H. W. M. and Ligterink, W. and Wellmer, F. and Grosse, I. and Quint, M.}, title = {{Post-embryonic Hourglass Patterns Mark Ontogenetic Transitions in Plant Development}}, year = {2016}, pages = {1158-1163}, journal = {Mol Biol Evol}, doi = {10.1093/molbev/msw039}, url = {https://academic.oup.com/mbe/article/33/5/1158/2580081}, volume = {33}, abstract = {The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found postembryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints. } } @Article{IPB-1801, author = {Ryan,P. T. and Ó’Maoiléidigh, D. S. and Drost, H.-G. and Kwaśniewska, D. and Gabel, A. and Grosse, I. and Graciet, E. and Quint, M. and Wellmer, F.}, title = {{Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation}}, year = {2015}, pages = {488 }, journal = {BMC Genomics}, doi = {10.1186/s12864-015-1699-6}, url = { http://www.biomedcentral.com/content/pdf/s12864-015-1699-6.pdf}, volume = {16}, abstract = {Background:The formation of flowers is one of the main model systems to elucidate the molecular mechanisms that control developmental processes in plants. Although several studies have explored gene expression during flower development in the model plant Arabidopsis thalianaon a genome-wide scale, a continuous series of expression data from the earliest floral stages until maturation has been lacking. Here, we used a floral induction system to closethis information gap and to generate a reference dataset for stage-specific gene expression during flower formation.Results:Using a floral induction system, we collected floral buds at 14 different stages from the time of initiation until maturation. Using whole-genome microarray analysis, we identified 7,405 genes that exhibit rapid expression changes during flower development. These genes comprise many known floral regulators and we found that the expression profiles for these regulators match their known expression patterns, thus validating the dataset. We analyzed groups ofco-expressed genes for over-represented cellular and developmental functions through Gene Ontology analysis and found that they could be assigned specific patterns of activities, which are in agreement with the progression of flower development. Furthermore, by mapping binding sites of floral organ identity factors onto our dataset, we were able to identify gene groups that are likely predominantly under control of these transcriptional regulators. We furtherfound that the distribution of paralogs among groups of co-expressed genes varies considerably, with genes expressed predominantly at early and intermediate stages of flower development showing the highest proportion of such genes.Conclusions:Our results highlight and describe the dynamic expression changes undergone by a large numberof genes during flower development. They further provide a comprehensive reference dataset for temporal gene expression during flower formation and we demonstrate that it can be used to integrate data from other genomics approaches such as genome-wide localization studies of transcription factor binding sites.} } @Article{IPB-1850, author = {Drost, H.-G. and Gabel, A. and Grosse, I. and Quint, M.}, title = {{Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis}}, year = {2015}, pages = {1221-1231}, journal = {Mol Biol Evol}, doi = {10.1093/molbev/msv012}, url = {http://mbe.oxfordjournals.org/content/32/5.toc}, volume = {32}, abstract = {The developmental hourglass model has been used to describe the morphological transitions of related species throughout embryogenesis. Recently, quantifiable approaches combining transcriptomic and evolutionary information provided novel evidence for the presence of a phylotranscriptomic hourglass pattern across kingdoms. As its biological function is unknown it remains speculative whether this pattern is functional or merely represents a nonfunctional evolutionary relic. The latter would seriously hamper future experimental approaches designed to test hypotheses regarding its function. Here, we address this question by generating transcriptome divergence index (TDI) profiles across embryogenesis of Danio rerio, Drosophila melanogaster, and Arabidopsis thaliana. To enable meaningful evaluation of the resulting patterns, we develop a statistical test that specifically assesses potential hourglass patterns. Based on this objective measure we find that two of these profiles follow a statistically significant hourglass pattern with the most conserved transcriptomes in the phylotypic periods. As the TDI considers only recent evolutionary signals, this indicates that the phylotranscriptomic hourglass pattern is not a rudiment but possibly actively maintained, implicating the existence of some linked biological function associated with embryogenesis in extant species.} } @Article{IPB-2243, author = {Drost, H.-G. and Bellstädt, J. and Ó'Maoiléidigh, D. S. and Silva, A. T. and Gabel, A. and Weinholdt, C. and Ryan, P. T. and Dekkers, B. J. W. and Bentsink, L. and Hilhorst, H. W. M. and Ligterink, W. and Wellmer, F. and Grosse, I. and Quint, M.}, title = {{Post-embryonic hourglass patterns mark ontogenetic transitions in plant development}}, year = {2015}, journal = {bioRxiv}, doi = {10.1101/035527}, url = {https://doi.org/10.1101/035527}, abstract = {The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found post-embryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints.} } @Article{IPB-1741, author = {Delker, C. and Sonntag, L. and Geo, V. J. and Janitza, P. and Ibañez, C. and Ziermann, H. and Peterson, T. and Denk, K. and Mull, S. and Ziegler, J. and Davis, S. J. and Schneeberger, K. and Quint, M.}, title = {{The DET1-COP1-HY5 Pathway Constitutes a Multipurpose Signaling Module Regulating Plant Photomorphogenesis and Thermomorphogenesis}}, year = {2014}, pages = {1983–1989}, journal = {Cell Rep}, doi = {10.1016/j.celrep.2014.11.043}, url = {http://www.cell.com/cell-reports/abstract/S2211-1247%2814%2901009-2}, volume = {9}, abstract = {Developmental plasticity enables plants to respond to elevated ambient temperatures by adapting their shoot architecture. On the cellular level, the basic-helix-loop-helix (bHLH) transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) coordinates this response by activating hormonal modules that in turn regulate growth. In addition to an unknown temperature-sensing mechanism, it is currently not understood how temperature regulates PIF4 activity. Using a forward genetic approach in Arabidopsis thaliana, we present extensive genetic evidence demonstrating that the DE-ETIOLATED 1 (DET1)-CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)-ELONGATED HYPOCOTYL 5 (HY5)-dependent photomorphogenesis pathway transcriptionally regulates PIF4 to coordinate seedling growth in response to elevated temperature. Our findings demonstrate that two of the most prevalent environmental cues, light and temperature, share a much larger set of signaling components than previously assumed. Similar to the toolbox concept in animal embryonic patterning, multipurpose signaling modules might have evolved in plants to translate various environmental stimuli into adaptational growth processes} } @Article{IPB-1597, author = {Dekkers, B.J.W. and Pearce, S. and van Bolderen-Veldkamp, R.P. and Marshall, A. and Widera, P. and Gilbert, J. and Drost, H.-G. and Basseli, G.W. and Müller, K. and King, J.R. and Wood, A.T.A. and Grosse, I. and Quint, M. and Krasnogor, N. and Leubner-Metzger, G. and Holdsworth, M.J. \& Bentsink, L.}, title = {{Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination}}, year = {2013}, pages = {205-215}, journal = {Plant Physiol}, doi = {10.1104/pp.113.223511}, volume = {163}, abstract = {Seed germination is a critical stage in the plant life cycle and the first step toward successful plant establishment. Therefore, understandinggermination is of important ecological and agronomical relevance. Previous research revealed that different seed compartments (testa,endosperm, and embryo) control germination, but little is known about the underlying spatial and temporal transcriptome changes thatlead to seed germination. We analyzed genome-wide expression in germinating Arabidopsis (Arabidopsis thaliana) seedswith both temporaland spatial detail and provide Web-accessible visualizations of the data reported (vseed.nottingham.ac.uk). We show the potential of this highresolutiondata set for the construction ofmeaningful coexpression networks, which provide insight into the genetic control of germination.The data set reveals two transcriptional phases during germination that are separated by testa rupture. The first phase is marked by largetranscriptome changes as the seed switches from a dry, quiescent state to a hydrated and active state. At the end of this first transcriptionalphase, the number of differentially expressed genes between consecutive time points drops. This increases again at testa rupture, the start ofthe second transcriptional phase. Transcriptome data indicate a role for mechano-induced signaling at this stage and subsequently highlightthe fates of the endosperm and radicle: senescence and growth, respectively. Finally, using a phylotranscriptomic approach, we show thatexpression levels of evolutionarily young genes drop during the first transcriptional phase and increase during the second phase.Evolutionarily old genes show an opposite pattern, suggesting a more conserved transcriptome prior to the completion of germination.} } @Article{IPB-1442, author = {Quint, M. and Drost, H.-G. and Gabel, A. and Ullrich, K. K. and Bönn, M. and Grosse, I.}, title = {{A transcriptomic hourglass in plant embryogenesis}}, year = {2012}, pages = {98-101}, journal = {Nature}, doi = {10.1038/nature11394}, url = {http://www.nature.com/nature/journal/v490/n7418/full/nature11394.html}, volume = {490}, abstract = {Animal and plant development starts with a constituting phase called embryogenesis, which evolved independently in both lineages1. Comparative anatomy of vertebrate development—based on the Meckel-Serrès law2 and von Baer’s laws of embryology3 from the early nineteenth century—shows that embryos from various taxa appear different in early stages, converge to a similar form during mid-embryogenesis, and again diverge in later stages. This morphogenetic series is known as the embryonic ‘hourglass’4,5, and its bottleneck of high conservation in mid-embryogenesis is referred to as the phylotypic stage6. Recent analyses in zebrafish and Drosophila embryos provided convincing molecular support for the hourglass model, because during the phylotypic stage the transcriptome was dominated by ancient genes7 and global gene expression profiles were reported to be most conserved8. Although extensively explored in animals, an embryonic hourglass has not been reported in plants, which represent the second major kingdom in the tree of life that evolved embryogenesis. Here we provide phylotranscriptomic evidence for a molecular embryonic hourglass in Arabidopsis thaliana, using two complementary approaches. This is particularly significant because the possible absence of an hourglass based on morphological features in plants suggests that morphological and molecular patterns might be uncoupled. Together with the reported developmental hourglass patterns in animals, these findings indicate convergent evolution of the molecular hourglass and a conserved logic of embryogenesis across kingdoms.} } @Article{IPB-1454, author = {Janitza, P. and Ullrich, K. K. and Quint, M.}, title = {{Toward a comprehensive phylogenetic reconstruction of the evolutionary history of mitogen-activated protein kinases in the plant kingdom}}, year = {2012}, pages = {271}, journal = {Front Plant Sci}, doi = {10.3389/fpls.2012.00271}, url = {https://dx.doi.org/10.3389/fpls.2012.00271}, volume = {3}, abstract = {The mitogen-activated protein kinase (MAPK) pathway is a three-tier signaling cascade that transmits cellular information from the plasma membrane to the cytoplasm where it triggers downstream responses. The MAPKs represent the last step in this cascade and are activated when both tyrosine and threonine residues in a conserved TxY motif are phosphorylated by MAPK kinases, which in turn are themselves activated by phosphorylation by MAPK kinase kinases. To understand the molecular evolution of MAPKs in the plant kingdom, we systematically conducted a Hidden-Markov-Model based screen to identify MAPKs in 13 completely sequenced plant genomes. In this analysis, we included green algae, bryophytes, lycophytes, and several mono- and eudicotyledonous species covering \>800 million years of evolution. The phylogenetic relationships of the 204 identified MAPKs based on Bayesian inference facilitated the retraction of the sequence of emergence of the four major clades that are characterized by the presence of a TDY or TEY-A/TEY-B/TEY-C type kinase activation loop. We present evidence that after the split of TDY- and TEY-type MAPKs, initially the TEY-C clade emerged. This was followed by the TEY-B clade in early land plants until the TEY-A clade finally emerged in flowering plants. In addition to these well characterized clades, we identified another highly conserved clade of 45 MAPK-likes, members of which were previously described as Mak-homologous kinases. In agreement with their essential functions, molecular population genetic analysis of MAPK genes in Arabidopsis thaliana accessions reveal that purifying selection drove the evolution of the MAPK family, implying strong functional constraints on MAPK genes. Closely related MAPKs most likely subfunctionalized, a process in which differential transcriptional regulation of duplicates may be involved.} }