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Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation.

Ryan PT, Ó'Maoiléidigh DS, Drost HG, Kwaśniewska K, Gabel A, Grosse I, Graciet E, Quint M, Wellmer F - BMC Genomics (2015)

Bottom Line: 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 further found 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.Our results highlight and describe the dynamic expression changes undergone by a large number of genes during flower development.

View Article: PubMed Central - PubMed

Affiliation: Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

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 thaliana on 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 close this 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 of co-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 further found 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 number of 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.

No MeSH data available.


Related in: MedlinePlus

Analysis of temporal gene expression during flower development. a-j Inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants a before dexamethasone treatment (0 d time-point) , and b 1 d, c 2 d, d 3 d, e 4 d, f 5 d, g 7 d, h 9 d, i 11 d, and j 13 d after treatment with a solution containing 10 μM dexamethasone. The development of flowers on a given inflorescence was largely synchronous until day 7. For later time-points (h-j), flowers were harvested from the tip of the inflorescences (arrowheads) after phenotypic assessment. k Experimental set-up used for this study. Floral buds were collected from the inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants at 14 time-points immediately before and after treatment with a dexamethasone (‘DEX’)-containing solution, which induces flower development by activating the AP1-GR fusion protein. Floral buds from the time of initiation until anthesis (corresponding to stage 13) were sampled
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Fig1: Analysis of temporal gene expression during flower development. a-j Inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants a before dexamethasone treatment (0 d time-point) , and b 1 d, c 2 d, d 3 d, e 4 d, f 5 d, g 7 d, h 9 d, i 11 d, and j 13 d after treatment with a solution containing 10 μM dexamethasone. The development of flowers on a given inflorescence was largely synchronous until day 7. For later time-points (h-j), flowers were harvested from the tip of the inflorescences (arrowheads) after phenotypic assessment. k Experimental set-up used for this study. Floral buds were collected from the inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants at 14 time-points immediately before and after treatment with a dexamethasone (‘DEX’)-containing solution, which induces flower development by activating the AP1-GR fusion protein. Floral buds from the time of initiation until anthesis (corresponding to stage 13) were sampled

Mentions: To identify patterns of gene expression during flower development from the time of initiation to maturation (stage 13; stages according to [7]), we employed a previously described floral induction system, which allows the collection of hundreds of floral buds from a single plant [9, 13, 24, 25]. This system is based on the expression of the floral meristem identity factor APETALA1 (AP1) fused to the hormone-binding domain of the rat glucocorticoid receptor (GR) from the AP1 regulatory region (AP1pro) in an ap1 cauliflower (cal) double-mutant background. Ap1 cal plants accumulate inflorescence-like meristems at their shoot apices [26, 27], and activation of the AP1-GR fusion protein in this background through treatment of the plants with the steroid hormone dexamethasone results in the transformation of these meristems into floral primordia, which subsequently develop in a largely synchronized manner. However, at intermediate stages, this synchronization is gradually lost likely due to space constraints [9]. Despite this overall loss of synchronization, we noticed that flowers at the very tip of the inflorescence heads remained fairly synchronized throughout flower development perhaps due to a larger degree of curvature in his area, which may allow floral buds to develop without coming into contact with neighboring flowers. For the gene expression profiling experiments, we therefore collected older floral buds (days 9 to 13 after dexamethasone treatment, corresponding to stages 9-10 to 13, respectively) from this region alone, while younger flowers were harvested more liberally from the inflorescences of AP1pro:AP1-GR ap1 cal plants (Fig. 1a-j). To obtain expression data for a large number of distinct floral stages, we collected floral buds at 14 different time-points either immediately before (referred to as 0 d time-point) or from 1 to 13 d after the induction of flower development through treatment with dexamethasone (Fig. 1k). Because early flower development is characterized by dramatic changes in morphology [7] and involves a large number of transcriptional regulators that control important processes such as floral patterning and floral organ specification [4], we collected most samples at those stages with intervals in-between time-points ranging from 0.5 to 1 d. At later stages of development, the intervals for sample collection were extended to 2 d (Fig. 1k).Fig. 1


Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation.

Ryan PT, Ó'Maoiléidigh DS, Drost HG, Kwaśniewska K, Gabel A, Grosse I, Graciet E, Quint M, Wellmer F - BMC Genomics (2015)

Analysis of temporal gene expression during flower development. a-j Inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants a before dexamethasone treatment (0 d time-point) , and b 1 d, c 2 d, d 3 d, e 4 d, f 5 d, g 7 d, h 9 d, i 11 d, and j 13 d after treatment with a solution containing 10 μM dexamethasone. The development of flowers on a given inflorescence was largely synchronous until day 7. For later time-points (h-j), flowers were harvested from the tip of the inflorescences (arrowheads) after phenotypic assessment. k Experimental set-up used for this study. Floral buds were collected from the inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants at 14 time-points immediately before and after treatment with a dexamethasone (‘DEX’)-containing solution, which induces flower development by activating the AP1-GR fusion protein. Floral buds from the time of initiation until anthesis (corresponding to stage 13) were sampled
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4488132&req=5

Fig1: Analysis of temporal gene expression during flower development. a-j Inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants a before dexamethasone treatment (0 d time-point) , and b 1 d, c 2 d, d 3 d, e 4 d, f 5 d, g 7 d, h 9 d, i 11 d, and j 13 d after treatment with a solution containing 10 μM dexamethasone. The development of flowers on a given inflorescence was largely synchronous until day 7. For later time-points (h-j), flowers were harvested from the tip of the inflorescences (arrowheads) after phenotypic assessment. k Experimental set-up used for this study. Floral buds were collected from the inflorescences of AP1pro:AP1-GR ap1-1 cal-1 plants at 14 time-points immediately before and after treatment with a dexamethasone (‘DEX’)-containing solution, which induces flower development by activating the AP1-GR fusion protein. Floral buds from the time of initiation until anthesis (corresponding to stage 13) were sampled
Mentions: To identify patterns of gene expression during flower development from the time of initiation to maturation (stage 13; stages according to [7]), we employed a previously described floral induction system, which allows the collection of hundreds of floral buds from a single plant [9, 13, 24, 25]. This system is based on the expression of the floral meristem identity factor APETALA1 (AP1) fused to the hormone-binding domain of the rat glucocorticoid receptor (GR) from the AP1 regulatory region (AP1pro) in an ap1 cauliflower (cal) double-mutant background. Ap1 cal plants accumulate inflorescence-like meristems at their shoot apices [26, 27], and activation of the AP1-GR fusion protein in this background through treatment of the plants with the steroid hormone dexamethasone results in the transformation of these meristems into floral primordia, which subsequently develop in a largely synchronized manner. However, at intermediate stages, this synchronization is gradually lost likely due to space constraints [9]. Despite this overall loss of synchronization, we noticed that flowers at the very tip of the inflorescence heads remained fairly synchronized throughout flower development perhaps due to a larger degree of curvature in his area, which may allow floral buds to develop without coming into contact with neighboring flowers. For the gene expression profiling experiments, we therefore collected older floral buds (days 9 to 13 after dexamethasone treatment, corresponding to stages 9-10 to 13, respectively) from this region alone, while younger flowers were harvested more liberally from the inflorescences of AP1pro:AP1-GR ap1 cal plants (Fig. 1a-j). To obtain expression data for a large number of distinct floral stages, we collected floral buds at 14 different time-points either immediately before (referred to as 0 d time-point) or from 1 to 13 d after the induction of flower development through treatment with dexamethasone (Fig. 1k). Because early flower development is characterized by dramatic changes in morphology [7] and involves a large number of transcriptional regulators that control important processes such as floral patterning and floral organ specification [4], we collected most samples at those stages with intervals in-between time-points ranging from 0.5 to 1 d. At later stages of development, the intervals for sample collection were extended to 2 d (Fig. 1k).Fig. 1

Bottom Line: 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 further found 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.Our results highlight and describe the dynamic expression changes undergone by a large number of genes during flower development.

View Article: PubMed Central - PubMed

Affiliation: Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

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 thaliana on 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 close this 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 of co-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 further found 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 number of 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.

No MeSH data available.


Related in: MedlinePlus