A Quantitative and Dynamic Model of the Arabidopsis Flowering Time Gene Regulatory Network

Various environmental signals integrate into a network of floral regulatory genes leading to the final decision on when to flower. Although a wealth of qualitative knowledge is available on how flowering time genes regulate each other, only a few studies incorporated this knowledge into predictive models. Such models are invaluable as they enable to investigate how various types of inputs are combined to give a quantitative readout. To investigate the effect of gene expression disturbances on flowering time, we developed a dynamic model for the regulation of flowering time in Arabidopsis thaliana. Model parameters were estimated based on expression time-courses for relevant genes, and a consistent set of flowering times for plants of various genetic backgrounds. Validation was performed by predicting changes in expression level in mutant backgrounds and comparing these predictions with independent expression data, and by comparison of predicted and experimental flowering times for several double mutants. Remarkably, the model predicts that a disturbance in a particular gene has not necessarily the largest impact on directly connected genes. For example, the model predicts that SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1) mutation has a larger impact on APETALA1 (AP1), which is not directly regulated by SOC1, compared to its effect on LEAFY (LFY) which is under direct control of SOC1. This was confirmed by expression data. Another model prediction involves the importance of cooperativity in the regulation of APETALA1 (AP1) by LFY, a prediction supported by experimental evidence. Concluding, our model for flowering time gene regulation enables to address how different quantitative inputs are combined into one quantitative output, flowering time

Alternative splicing of barley clock genes in response to low temperature:evidence for alternative splicing conservation

Alternative splicing (AS) is a regulated mechanism that generates multiple transcripts from individual genes. It is widespread in eukaryotic genomes and provides an effective way to control gene expression. At low temperatures, AS regulates Arabidopsis clock genes through dynamic changes in the levels of productive mRNAs. We examined AS in barley clock genes to assess whether temperature-dependent AS responses also occur in a monocotyledonous crop species. We identify changes in AS of various barley core clock genes including the barley orthologues of Arabidopsis AtLHY and AtPRR7 which showed the most pronounced AS changes in response to low temperature. The AS events modulate the levels of functional and translatable mRNAs, and potentially protein levels, upon transition to cold. There is some conservation of AS events and/or splicing behaviour of clock genes between Arabidopsis and barley. In addition, novel temperature-dependent AS of the core clock gene HvPPD-H1 (a major determinant of photoperiod response and AtPRR7 orthologue) is conserved in monocots. HvPPD-H1 showed a rapid, temperature-sensitive isoform switch which resulted in changes in abundance of AS variants encoding different protein isoforms. This novel layer of low temperature control of clock gene expression, observed in two very different species, will help our understanding of plant adaptation to different environments and ultimately offer a new range of targets for plant improvement

Control of Flowering in Strawberries

Strawberries (Fragaria sp.) are small perennial plants capable of both sexual reproduction through seeds and clonal reproduction via runners. Because vegetative and generative developmental programs are tightly connected, the control of flowering is presented here in the context of the yearly growth cycle. The rosette crown of strawberry consists of a stem with short internodes produced from the apical meristem. Each node harbors one trifoliate leaf and an axillary bud. The fate of axillary buds is dictated by environmental conditions; high temperatures and long days (LDs) promote axillary bud development into runners, whereas cool temperature and short days (SDs) favor the formation of branch crowns. SDs and cool temperature also promote flowering; under these conditions, the main shoot apical meristem is converted into a terminal inflorescence, and vegetative growth is continued from the uppermost axillary branch crown. The environmental factors that regulate vegetative and generative development in strawberries have been reasonably well characterized and are reviewed in the first two chapters. The genetic basis of the physiological responses in strawberries is much less clear. To provide a point of reference for the flowering pathways described in strawberries so far, a short review on the molecular mechanisms controlling flowering in the model plant Arabidopsis is given. The last two chapters will then describe the current knowledge on the molecular mechanisms controlling the physiological responses in strawberries.Peer reviewe

Control of flowering by ambient temperature

The timing of flowering is a crucial decision in the life cycle of plants since favourable conditions are needed to maximize reproductive success and, hence, the survival of the species. It is therefore not surprising that plants constantly monitor endogenous and environmental signals, such as day length (photoperiod) and temperature, to adjust the timing of the floral transition. Temperature in particular has been shown to have a tremendous effect on the timing of flowering: the effect of prolonged periods of cold, called the vernalization response, has been extensively studied and the underlying epigenetic mechanisms are reasonably well understood in Arabidopsis thaliana. In contrast, the effect of moderate changes in ambient growth temperature on the progression of flowering, the thermosensory pathway, is only starting to be understood on the molecular level. Several genes and molecular mechanisms underlying the thermosensory pathway have already been identified and characterized in detail. At a time when global temperature is rising due to climate change, this knowledge will be pivotal to ensure crop production in the future

The end of innocence: flowering networks explode in complexity

Substantial recent advances in genome-scale transcription factor target mapping have provided a fresh view of the gene networks governing developmental transitions. In particular, our understanding of the fine-scale spatial and temporal dynamics underlying the floral transition at the shoot apex has seen great advances in the past two years. Single transcription factors are regularly observed to act in complex manners, directly promoting the expression of particular targets while directly repressing the expression of others, based at least partly on defined heterodimerization patterns. For single regulators this behavior reaches into distinct physiological processes, providing compelling evidence that particular transcription factors act to directly integrate diverse processes to orchestrate complex developmental transitions

Regulation of temperature-responsive flowering by MADS-box transcription factor repressors

Changes in ambient temperature affect flowering time in plants; understanding this phenomenon will be crucial for buffering agricultural systems from the effects of climate change. Here, we show that levels of FLM-β, an alternatively spliced form of the flowering repressor FLOWERING LOCUS M, increase at lower temperatures, repressing flowering. FLM-β interacts with SHORT VEGETATIVE PHASE (SVP); SVP is degraded at high temperatures, reducing the abundance of the SVP-FLM-β repressor complex and, thus, allowing the plant to flower. The svp and flm mutants show temperature-insensitive flowering in different temperature ranges. Control of SVP-FLM-β repressor complex abundance via transcriptional and splicing regulation of FLM and posttranslational regulation of SVP protein stability provides an efficient, rapid mechanism for plants to respond to ambient temperature changes

Temperature-dependent alternative splicing of FLM controls flowering in Arabidopsis thaliana

How plants control the transition to flowering in response to ambient temperature is only beginning to be understood. In Arabidopsis thaliana, the MADS-box transcription factor genes FLOWERING LOCUS M (FLM) and SHORT VEGETATIVE PHASE (SVP) have key roles in this process. FLM is subject to temperature-dependent alternative splicing, producing two splice variants, FLM-β and FLM-δ, which compete for interaction with the floral repressor SVP. The SVP/FLM-β complex is predominately formed at low temperatures and prevents precocious flowering. In contrast, the competing SVP FLM-δ complex is impaired in DNA binding and acts as a dominant negative activator of flowering at higher temperatures. Our results demonstrate the importance of temperature-dependent alternative splicing in modulating the timing of the floral transition in response to environmental change. Overall design ChIP-seq A. thaliana FLM (3 replicates for gFLM and 2 replicates for FLM splice variants

Temperature-dependent regulation of flowering by antagonistic FLM variants

The appropriate timing of flowering is crucial for plant reproductive success. It is therefore not surprising that intricate genetic networks have evolved to perceive and integrate both endogenous and environmental signals, such as carbohydrate and hormonal status, photoperiod and temperature. In contrast to our detailed understanding of the vernalization pathway, little is known about how flowering time is controlled in response to changes in the ambient growth temperature. In Arabidopsis thaliana, the MADS-box transcription factor genes FLOWERING LOCUS M (FLM) and SHORT VEGETATIVE PHASE (SVP) have key roles in this process. FLM is subject to temperature-dependent alternative splicing. Here we report that the two main FLM protein splice variants, FLM-β and FLM-δ, compete for interaction with the floral repressor SVP. The SVP-FLM-β complex is predominately formed at low temperatures and prevents precocious flowering. By contrast, the competing SVP-FLM-δ complex is impaired in DNA binding and acts as a dominant-negative activator of flowering at higher temperatures. Our results show a new mechanism that controls the timing of the floral transition in response to changes in ambient temperature. A better understanding of how temperature controls the molecular mechanisms of flowering will be important to cope with current changes in global climate

Modulation of ambient temperature-dependent flowering in <em>Arabidopsis thaliana</em> by natural variation of <em>FLOWERING LOCUS M</em>.

Plants integrate seasonal cues such as temperature and day length to optimally adjust their flowering time to the environment. Compared to the control of flowering before and after winter by the vernalization and day length pathways, mechanisms that delay or promote flowering during a transient cool or warm period, especially during spring, are less well understood. Due to global warming, understanding this ambient temperature pathway has gained increasing importance. In Arabidopsis thaliana, FLOWERING LOCUS M (FLM) is a critical flowering regulator of the ambient temperature pathway. FLM is alternatively spliced in a temperature-dependent manner and the two predominant splice variants, FLM-&szlig; and FLM-&delta;, can repress and activate flowering in the genetic background of the A. thaliana reference accession Columbia-0. The relevance of this regulatory mechanism for the environmental adaptation across the entire range of the species is, however, unknown. Here, we identify insertion polymorphisms in the first intron of FLM as causative for accelerated flowering in many natural A. thaliana accessions, especially in cool (15&deg;C) temperatures. We present evidence for a potential adaptive role of this structural variation and link it specifically to changes in the abundance of FLM-&szlig;. Our results may allow predicting flowering in response to ambient temperatures in the Brassicaceae

Temperature-dependent regulation of flowering by antagonistic FLM variants

The appropriate timing of flowering is crucial for plant reproductive success. It is therefore not surprising that intricate genetic networks have evolved to perceive and integrate both endogenous and environmental signals, such as carbohydrate and hormonal status, photoperiod and temperature1,2. In contrast to our detailed understanding of the vernalization pathway, little is known about how flowering time is controlled in response to changes in the ambient growth temperature. In Arabidopsis thaliana, the MADSbox transcription factor genesFLOWERING LOCUSM (FLM) and SHORTVEGETATIVEPHASE (SVP)have key roles in this process3,4. FLM is subject to temperature-dependent alternative splicing3. Here we report that the two mainFLMprotein splice variants,FLM-b and FLM-d, compete for interaction with the floral repressor SVP. The SVP–FLM-b complex is predominately formed at low temperatures and prevents precocious flowering. By contrast, the competingSVP–FLM-d complex is impaired in DNA binding and acts as a dominant-negative activator of flowering at higher temperatures. Our results show a new mechanism that controls the timing of the floral transition in response to changes in ambient temperature. A better understanding of how temperature controls the molecular mechanismsof flowering will be important to cope with current changes in global climate5,6