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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: 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.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.

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

Distribution of paralogs in groups of co-expressed genes. The percentage of paralogs in each cluster of co-expressed genes (black bars) was determined as described in Methods. To identify clusters with a significant enrichment of paralogous genes, the mean percentage of paralogs was determined in equally sized groups of genes randomly selected from the dataset of 7,405 DEGs (gray bars) and from the Arabidopsis genome (white bars), respectively. Error bars indicate one standard deviation calculated based on the results of 100 iterations
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Fig7: Distribution of paralogs in groups of co-expressed genes. The percentage of paralogs in each cluster of co-expressed genes (black bars) was determined as described in Methods. To identify clusters with a significant enrichment of paralogous genes, the mean percentage of paralogs was determined in equally sized groups of genes randomly selected from the dataset of 7,405 DEGs (gray bars) and from the Arabidopsis genome (white bars), respectively. Error bars indicate one standard deviation calculated based on the results of 100 iterations

Mentions: In plants, duplicated genes that are retained in a genome are often functionally redundant, although sub- or neofunctionalization may lead to paralogous genes that have only partially overlapping activities or that are employed in entirely different developmental processes, respectively [54]. Shared activities of paralogous genes typically go along with overlapping expression patterns. Therefore, one would expect to find in the clusters of co-expressed genes that paralogs are enriched relative to their genome-wide distribution. In fact, it has been shown previously that paralogous genes are over-represented in some but not all groups of genes with predominant expression at certain stages of early flower development [9]. To test whether this unequal distribution of paralogs extends to intermediate or late stages of flower development, we determined paralogs in each of the 15 clusters described in Fig. 3 (for paralogs identified in the clusters, see Additional file 7). As expected, we found that the percentage of paralogs was significantly (i.e., beyond three standard deviations) increased in all clusters relative to their genome-wide distribution and to a lesser extent (and with the exception of cluster 13) relative to their distribution within the 7,405 DEGs as well (Fig. 7). Notably, the enrichment of paralogs within the clusters varied considerably, with clusters 5, 11-12, and 15 having the highest enrichment values (Table S3 in Additional file 1). In agreement with the idea that genes involved in floral organ development exhibit an increased level of genetic redundancy [9], the genes in these clusters have in common that they are activated during early or intermediate (cluster 15) stages of flower development and many of them have known functions in floral organ morphogenesis and in the control of floral meristem determinacy (Fig. 5). In sum, our results further highlight the varying degree to which paralogous genes contribute to different processes during flower development. Whether such an unequal distribution of paralogs among groups of co-expressed genes extends to other processes during plant development is currently unknown.Fig. 7


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)

Distribution of paralogs in groups of co-expressed genes. The percentage of paralogs in each cluster of co-expressed genes (black bars) was determined as described in Methods. To identify clusters with a significant enrichment of paralogous genes, the mean percentage of paralogs was determined in equally sized groups of genes randomly selected from the dataset of 7,405 DEGs (gray bars) and from the Arabidopsis genome (white bars), respectively. Error bars indicate one standard deviation calculated based on the results of 100 iterations
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig7: Distribution of paralogs in groups of co-expressed genes. The percentage of paralogs in each cluster of co-expressed genes (black bars) was determined as described in Methods. To identify clusters with a significant enrichment of paralogous genes, the mean percentage of paralogs was determined in equally sized groups of genes randomly selected from the dataset of 7,405 DEGs (gray bars) and from the Arabidopsis genome (white bars), respectively. Error bars indicate one standard deviation calculated based on the results of 100 iterations
Mentions: In plants, duplicated genes that are retained in a genome are often functionally redundant, although sub- or neofunctionalization may lead to paralogous genes that have only partially overlapping activities or that are employed in entirely different developmental processes, respectively [54]. Shared activities of paralogous genes typically go along with overlapping expression patterns. Therefore, one would expect to find in the clusters of co-expressed genes that paralogs are enriched relative to their genome-wide distribution. In fact, it has been shown previously that paralogous genes are over-represented in some but not all groups of genes with predominant expression at certain stages of early flower development [9]. To test whether this unequal distribution of paralogs extends to intermediate or late stages of flower development, we determined paralogs in each of the 15 clusters described in Fig. 3 (for paralogs identified in the clusters, see Additional file 7). As expected, we found that the percentage of paralogs was significantly (i.e., beyond three standard deviations) increased in all clusters relative to their genome-wide distribution and to a lesser extent (and with the exception of cluster 13) relative to their distribution within the 7,405 DEGs as well (Fig. 7). Notably, the enrichment of paralogs within the clusters varied considerably, with clusters 5, 11-12, and 15 having the highest enrichment values (Table S3 in Additional file 1). In agreement with the idea that genes involved in floral organ development exhibit an increased level of genetic redundancy [9], the genes in these clusters have in common that they are activated during early or intermediate (cluster 15) stages of flower development and many of them have known functions in floral organ morphogenesis and in the control of floral meristem determinacy (Fig. 5). In sum, our results further highlight the varying degree to which paralogous genes contribute to different processes during flower development. Whether such an unequal distribution of paralogs among groups of co-expressed genes extends to other processes during plant development is currently unknown.Fig. 7

Bottom Line: 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.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.

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