Drost, H.-G.; Bellstädt, J.; Ó'Maoiléidigh, D. S.; Silva, A. T.; Gabel, A.; Weinholdt, C.; Ryan, P. T.; Dekkers, B. J. W.; Bentsink, L.; Hilhorst, H. W. M.; Ligterink, W.; Wellmer, F.; Grosse, I.; Quint, M. Post-embryonic Hourglass Patterns Mark Ontogenetic Transitions in Plant Development Mol Biol Evol 33, 1158-1163, (2016) DOI: 10.1093/molbev/msw039
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.
Bücher und Buchkapitel
Tissier, A.; Ziegler, J.; Vogt, T. Specialized Plant Metabolites: Diversity and Biosynthesis (Krauss, G.-J. & Nies, D. H., eds.). 14-37, (2015) ISBN: 978-3-527-31650-2 DOI: 10.1002/9783527686063.ch2
Plant secondary metabolites, also termed
specialized plant metabolites, currently comprise more than 200 000
natural products that are all based on a few biosynthetic pathways and
key primary metabolites. Some pathways like flavonoid and terpenoid
biosynthesis are universally distributed in the plant kingdom, whereas
others like alkaloid or cyanogenic glycoside biosynthesis are restricted
to a limited set of taxa. Diversification is achieved by an array of
mechanisms at the genetic and enzymatic level including gene
duplications, substrate promiscuity of enzymes, cell‐specific regulatory
systems, together with modularity and combinatorial aspects.
Specialized metabolites reflect adaptations to a specific environment.
The observed diversity illustrates the heterogeneity and multitude of
ecological habitats and niches that plants have colonized so far and
constitutes a reservoir of potential new metabolites that may provide
adaptive advantage in the face of environmental changes. The code that
connects the observed chemical diversity to this ecological diversity is
largely unknown. One way to apprehend this diversity is to realize its
tremendous plasticity and evolutionary potential. This chapter presents
an overview of the most widespread and popular secondary metabolites,
which provide a definite advantage to adapt to or to colonize a
particular environment, making the boundary between the “primary” and
the “secondary” old fashioned and blurry.
Ryan,P. T.; Ó’Maoiléidigh, D. S.; Drost, H.-G.; Kwaśniewska, D.; Gabel, A.; Grosse, I.; Graciet, E.; Quint, M.; Wellmer, F. Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation BMC Genomics 16, 488 , (2015) DOI: 10.1186/s12864-015-1699-6
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.
Drost, H.-G.; Gabel, A.; Grosse, I.; Quint, M. Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis Mol Biol Evol 32, 1221-1231, (2015) DOI: 10.1093/molbev/msv012
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.
Drost, H.-G.; Bellstädt, J.; Ó'Maoiléidigh, D. S.; Silva, A. T.; Gabel, A.; Weinholdt, C.; Ryan, P. T.; Dekkers, B. J. W.; Bentsink, L.; Hilhorst, H. W. M.; Ligterink, W.; Wellmer, F.; Grosse, I.; Quint, M. Post-embryonic hourglass patterns mark ontogenetic transitions in plant development bioRxiv (2015) DOI: 10.1101/035527
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
Dekkers, B.J.W.; Pearce, S.; van Bolderen-Veldkamp, R.P.; Marshall, A.; Widera, P.; Gilbert, J.; Drost, H.-G.; Basseli, G.W.; Müller, K.; King, J.R.; Wood, A.T.A.; Grosse, I.; Quint, M.; Krasnogor, N.; Leubner-Metzger, G.; Holdsworth, M.J. & Bentsink, L. Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination Plant Physiol 163, 205-215, (2013) DOI: 10.1104/pp.113.223511
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.
Quint, M.; Drost, H.-G.; Gabel, A.; Ullrich, K. K.; Bönn, M.; Grosse, I. A transcriptomic hourglass in plant embryogenesis Nature 490, 98-101, (2012) DOI: 10.1038/nature11394
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.
Fellenberg, C.; Ziegler, J.; Handrick, V.; Vogt, T. Polyamine homeostasis in wild type and phenolamide deficient Arabidopsis thaliana stamens Front Plant Sci 3, 180, (2012) DOI: 10.3389/fpls.2012.00180
Polyamines (PAs) like putrescine, spermidine, and spermine are ubiquitous polycationic molecules that occur in all living cells and have a role in a wide variety of biological processes. High amounts of spermidine conjugated to hydroxycinnamic acids are detected in the tryphine of Arabidopsis thaliana pollen grains. Tapetum localized spermidine hydroxycinnamic acid transferase (SHT) is essential for the biosynthesis of these anther specific tris-conjugated spermidine derivatives. Sht knockout lines show a strong reduction of hydroxycinnamic acid amides (HCAAs). The effect of HCAA-deficient anthers on the level of free PAs was measured by a new sensitive and reproducible method using 9-fluorenylmethyl chloroformate (FMOC) and fluorescence detection by HPLC. PA concentrations can be accurately determined even when very limited amounts of plant material, as in the case of A. thaliana stamens, are available. Analysis of free PAs in wild type stamens compared to sht deficient mutants and transcript levels of key PA biosynthetic genes revealed a highly controlled regulation of PA homeostasis in A. thaliana anthers.
Stumpe, M.; Göbel, C.; Faltin, B.; Beike, A. K.; Hause, B.; Himmelsbach, K.; Bode, J.; Kramell, R.; Wasternack, C.; Frank, W.; Reski, R.; Feussner, I. The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology New Phytol 188 (3), 740-749, (2010) DOI: 10.1111/j.1469-8137.2010.03406.x
Two cDNAs encoding allene oxide cyclases (PpAOC1,
PpAOC2), key enzymes in the formation of jasmonic acid (JA) and its
precursor (9S,13S)‐12‐oxo‐phytodienoic acid (cis‐(+)‐OPDA), were
isolated from the moss Physcomitrella patens.Recombinant PpAOC1 and
PpAOC2 show substrate specificity against the allene oxide derived from
13‐hydroperoxy linolenic acid (13‐HPOTE); PpAOC2 also shows substrate
specificity against the allene oxide derived from 12‐hydroperoxy
arachidonic acid (12‐HPETE).In protonema and gametophores the occurrence
of cis‐(+)‐OPDA, but neither JA nor the isoleucine conjugate of JA nor
that of cis‐(+)‐OPDA was detected.Targeted knockout mutants for PpAOC1
and for PpAOC2 were generated, while double mutants could not be
obtained. The ΔPpAOC1 and ΔPpAOC2 mutants showed reduced fertility,
aberrant sporophyte morphology and interrupted sporogenesis.
Fellenberg, C.; Milkowski, C.; Hause, B.; Lange, P.; Böttcher, C.; Schmidt, J.; Vogt, T. Tapetum-specific location of a cation-dependent O-methyltransferase in Arabidopsis thaliana Plant J 56, 132-145, (2008) DOI: 10.1111/j.1365-313X.2008.03576.x
Cation- and S-adenosyl-l-methionine (AdoMet)-dependent plant natural product methyltransferases are referred to as CCoAOMTs because of their preferred substrate, caffeoyl coenzyme A (CCoA). The enzymes are encoded by a small family of genes, some of which with a proven role in lignin monomer biosynthesis. In Arabidopsis thaliana individual members of this gene family are temporally and spatially regulated. The gene At1g67990 is specifically expressed in flower buds, and is not detected in any other organ, such as roots, leaves or stems. Several lines of evidence indicate that the At1g67990 transcript is located in the flower buds, whereas the corresponding CCoAOMT-like protein, termed AtTSM1, is located exclusively in the tapetum of developing stamen. Flowers of At1g67990 RNAi-suppressed plants are characterized by a distinct flower chemotype with severely reduced levels of the N ′,N ′′-bis-(5-hydroxyferuloyl)-N ′′′-sinapoylspermidine compensated for by N1,N5,N10-tris-(5-hydroxyferuloyl)spermidine derivative, which is characterized by the lack of a single methyl group in the sinapoyl moiety. This severe change is consistent with the observed product profile of AtTSM1 for aromatic phenylpropanoids. Heterologous expression of the recombinant protein shows the highest activity towards a series of caffeic acid esters, but 5-hydroxyferuloyl spermidine conjugates are also accepted substrates. The in vitro substrate specificity and the in vivo RNAi-mediated suppression data of the corresponding gene suggest a role of this cation-dependent CCoAOMT-like protein in the stamen/pollen development of A. thaliana.