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Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.).

Laudencia-Chingcuanco D, Ganeshan S, You F, Fowler B, Chibbar R, Anderson O - BMC Genomics (2011)

Bottom Line: We compared the expression of genes in winter-habit (winter Norstar and winter Manitou) and spring-habit (spring Manitou and spring Norstar)) cultivars, wherein the locus for the vernalization gene Vrn-A1 was swapped between the parental winter Norstar and spring Manitou in the derived near-isogenic lines winter Manitou and spring Norstar.Functional assignments using GO annotations showed that genes involved in transport, oxidation-reduction, and stress response were highly represented.The results support the developmental model of LT tolerance gene regulation and demonstrate the complex genotype by environment interactions that determine LT adaptation in winter annual cereals.

View Article: PubMed Central - HTML - PubMed

Affiliation: Genomics and Gene Discovery Unit, USDA-ARS WRRC, Albany, CA 94710, USA. debbie.laudencia@ars.usda.gov

ABSTRACT

Background: To identify the genes involved in the development of low temperature (LT) tolerance in hexaploid wheat, we examined the global changes in expression in response to cold of the 55,052 potentially unique genes represented in the Affymetrix Wheat Genome microarray. We compared the expression of genes in winter-habit (winter Norstar and winter Manitou) and spring-habit (spring Manitou and spring Norstar)) cultivars, wherein the locus for the vernalization gene Vrn-A1 was swapped between the parental winter Norstar and spring Manitou in the derived near-isogenic lines winter Manitou and spring Norstar. Global expression of genes in the crowns of 3-leaf stage plants cold-acclimated at 6°C for 0, 2, 14, 21, 38, 42, 56 and 70 days was examined.

Results: Analysis of variance of gene expression separated the samples by genetic background and by the developmental stage before or after vernalization saturation was reached. Using gene-specific ANOVA we identified 12,901 genes (at p < 0.001) that change in expression with respect to both genotype and the duration of cold-treatment. We examined in more detail a subset of these genes (2,771) where expression was highly influenced by the interaction between these two main factors. Functional assignments using GO annotations showed that genes involved in transport, oxidation-reduction, and stress response were highly represented. Clustering based on the pattern of transcript accumulation identified genes that were up or down-regulated by cold-treatment. Our data indicate that the cold-sensitive lines can up-regulate known cold-responsive genes comparable to that of cold-hardy lines. The levels of expression of these genes were highly influenced by the initial rate and the duration of the gene's response to cold. We show that the Vrn-A1 locus controls the duration of gene expression but not its initial rate of response to cold treatment. Furthermore, we provide evidence that Ta.Vrn-A1 and Ta.Vrt1 originally hypothesized to encode for the same gene showed different patterns of expression and therefore are distinct.

Conclusion: This study provides novel insight into the underlying mechanisms that regulate the expression of cold-responsive genes in wheat. The results support the developmental model of LT tolerance gene regulation and demonstrate the complex genotype by environment interactions that determine LT adaptation in winter annual cereals.

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Clustering of expression profiles of genes that show 2-fold or more change in expression in Norstar and their comparative profiles in other genotypes. The x-axis in each frame represents duration of cold treatment from 0 to 70 days. The y-axis in each frame represents median centered relative gene expression in log 2. Relative expression was calculated by determining the difference between the maximum and minimum level of expression in the time-series. Cluster ID is indicated by the number on the upper left corner of each frame. The number of genes in each cluster is indicated on the lower right corner of each frame.
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Figure 5: Clustering of expression profiles of genes that show 2-fold or more change in expression in Norstar and their comparative profiles in other genotypes. The x-axis in each frame represents duration of cold treatment from 0 to 70 days. The y-axis in each frame represents median centered relative gene expression in log 2. Relative expression was calculated by determining the difference between the maximum and minimum level of expression in the time-series. Cluster ID is indicated by the number on the upper left corner of each frame. The number of genes in each cluster is indicated on the lower right corner of each frame.

Mentions: Analysis of the expression levels of the 2,771 genes with strong GxT interaction (Table 4) showed that more genes in the spring habit genotypes had a higher frequency of 2-fold or more change in gene expression (61-62%) compared to the winter habit genotypes (41-45%). This suggests that the vrn-A1 allele had a dampening effect on LT response. The k-means clustering method was used to identify genes with 2-fold or more change in expression that had similar up- or down-regulation patterns during cold treatment. These genes were grouped into 8 clusters for each genotype. The expression profiles for the 1,137 winter Norstar genes (Figure 5) show that a majority in Cluster 1 are gradually up-regulated and peaked at the later time points. Genes in Clusters 3 and 6 were rapidly up-regulated during the early stage of cold treatment and remained highly expressed. The genes in cluster 7 were also rapidly up-regulated during the initial cold-treatment but showed modulated response thereafter. The genes in Clusters 2, 4, 5, and 8 were down-regulated during the early stage of cold treatment and had different dynamics at later stages. The modulated expression of genes in Cluster 8 was a mirror image of the expression profiles of the genes in Cluster 7.


Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.).

Laudencia-Chingcuanco D, Ganeshan S, You F, Fowler B, Chibbar R, Anderson O - BMC Genomics (2011)

Clustering of expression profiles of genes that show 2-fold or more change in expression in Norstar and their comparative profiles in other genotypes. The x-axis in each frame represents duration of cold treatment from 0 to 70 days. The y-axis in each frame represents median centered relative gene expression in log 2. Relative expression was calculated by determining the difference between the maximum and minimum level of expression in the time-series. Cluster ID is indicated by the number on the upper left corner of each frame. The number of genes in each cluster is indicated on the lower right corner of each frame.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3141665&req=5

Figure 5: Clustering of expression profiles of genes that show 2-fold or more change in expression in Norstar and their comparative profiles in other genotypes. The x-axis in each frame represents duration of cold treatment from 0 to 70 days. The y-axis in each frame represents median centered relative gene expression in log 2. Relative expression was calculated by determining the difference between the maximum and minimum level of expression in the time-series. Cluster ID is indicated by the number on the upper left corner of each frame. The number of genes in each cluster is indicated on the lower right corner of each frame.
Mentions: Analysis of the expression levels of the 2,771 genes with strong GxT interaction (Table 4) showed that more genes in the spring habit genotypes had a higher frequency of 2-fold or more change in gene expression (61-62%) compared to the winter habit genotypes (41-45%). This suggests that the vrn-A1 allele had a dampening effect on LT response. The k-means clustering method was used to identify genes with 2-fold or more change in expression that had similar up- or down-regulation patterns during cold treatment. These genes were grouped into 8 clusters for each genotype. The expression profiles for the 1,137 winter Norstar genes (Figure 5) show that a majority in Cluster 1 are gradually up-regulated and peaked at the later time points. Genes in Clusters 3 and 6 were rapidly up-regulated during the early stage of cold treatment and remained highly expressed. The genes in cluster 7 were also rapidly up-regulated during the initial cold-treatment but showed modulated response thereafter. The genes in Clusters 2, 4, 5, and 8 were down-regulated during the early stage of cold treatment and had different dynamics at later stages. The modulated expression of genes in Cluster 8 was a mirror image of the expression profiles of the genes in Cluster 7.

Bottom Line: We compared the expression of genes in winter-habit (winter Norstar and winter Manitou) and spring-habit (spring Manitou and spring Norstar)) cultivars, wherein the locus for the vernalization gene Vrn-A1 was swapped between the parental winter Norstar and spring Manitou in the derived near-isogenic lines winter Manitou and spring Norstar.Functional assignments using GO annotations showed that genes involved in transport, oxidation-reduction, and stress response were highly represented.The results support the developmental model of LT tolerance gene regulation and demonstrate the complex genotype by environment interactions that determine LT adaptation in winter annual cereals.

View Article: PubMed Central - HTML - PubMed

Affiliation: Genomics and Gene Discovery Unit, USDA-ARS WRRC, Albany, CA 94710, USA. debbie.laudencia@ars.usda.gov

ABSTRACT

Background: To identify the genes involved in the development of low temperature (LT) tolerance in hexaploid wheat, we examined the global changes in expression in response to cold of the 55,052 potentially unique genes represented in the Affymetrix Wheat Genome microarray. We compared the expression of genes in winter-habit (winter Norstar and winter Manitou) and spring-habit (spring Manitou and spring Norstar)) cultivars, wherein the locus for the vernalization gene Vrn-A1 was swapped between the parental winter Norstar and spring Manitou in the derived near-isogenic lines winter Manitou and spring Norstar. Global expression of genes in the crowns of 3-leaf stage plants cold-acclimated at 6°C for 0, 2, 14, 21, 38, 42, 56 and 70 days was examined.

Results: Analysis of variance of gene expression separated the samples by genetic background and by the developmental stage before or after vernalization saturation was reached. Using gene-specific ANOVA we identified 12,901 genes (at p < 0.001) that change in expression with respect to both genotype and the duration of cold-treatment. We examined in more detail a subset of these genes (2,771) where expression was highly influenced by the interaction between these two main factors. Functional assignments using GO annotations showed that genes involved in transport, oxidation-reduction, and stress response were highly represented. Clustering based on the pattern of transcript accumulation identified genes that were up or down-regulated by cold-treatment. Our data indicate that the cold-sensitive lines can up-regulate known cold-responsive genes comparable to that of cold-hardy lines. The levels of expression of these genes were highly influenced by the initial rate and the duration of the gene's response to cold. We show that the Vrn-A1 locus controls the duration of gene expression but not its initial rate of response to cold treatment. Furthermore, we provide evidence that Ta.Vrn-A1 and Ta.Vrt1 originally hypothesized to encode for the same gene showed different patterns of expression and therefore are distinct.

Conclusion: This study provides novel insight into the underlying mechanisms that regulate the expression of cold-responsive genes in wheat. The results support the developmental model of LT tolerance gene regulation and demonstrate the complex genotype by environment interactions that determine LT adaptation in winter annual cereals.

Show MeSH