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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.

Show MeSH
Expression profiles of known cold-induced genes in winter Norstar and spring Manitou and the near isogenic lines spring Norstar and winter Manitou that showed strong genotype by duration of cold treatment interactions when acclimated at 6°C for 0 to 70 days.
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Figure 8: Expression profiles of known cold-induced genes in winter Norstar and spring Manitou and the near isogenic lines spring Norstar and winter Manitou that showed strong genotype by duration of cold treatment interactions when acclimated at 6°C for 0 to 70 days.

Mentions: The initial rate of response (determined by the slope of the change in relative gene expression between 0 and 2 days of cold treatment) of known cold-induced genes was not influenced by the swapped Vrn1 locus. As shown in Figure 8, the initial rate of response of these cold-induced genes was similar in winter and spring Norstar and in spring and winter Manitou. This reveals the presence of regulatory genes located outside of the swapped Vrn1 locus that control the rate of response of these genes to cold treatment. The initial rate of response to cold treatment greatly influences the level of expression of cold-induced genes and genes that exhibit faster rate of up-regulation by acclimation were usually associated with greater cold tolerance (Figure 1). This close relationship among rates of up-regulation of the known cold-induced genes and LT tolerance should not be unexpected as this is likely the reason why they were originally selected for study.


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)

Expression profiles of known cold-induced genes in winter Norstar and spring Manitou and the near isogenic lines spring Norstar and winter Manitou that showed strong genotype by duration of cold treatment interactions when acclimated at 6°C for 0 to 70 days.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Expression profiles of known cold-induced genes in winter Norstar and spring Manitou and the near isogenic lines spring Norstar and winter Manitou that showed strong genotype by duration of cold treatment interactions when acclimated at 6°C for 0 to 70 days.
Mentions: The initial rate of response (determined by the slope of the change in relative gene expression between 0 and 2 days of cold treatment) of known cold-induced genes was not influenced by the swapped Vrn1 locus. As shown in Figure 8, the initial rate of response of these cold-induced genes was similar in winter and spring Norstar and in spring and winter Manitou. This reveals the presence of regulatory genes located outside of the swapped Vrn1 locus that control the rate of response of these genes to cold treatment. The initial rate of response to cold treatment greatly influences the level of expression of cold-induced genes and genes that exhibit faster rate of up-regulation by acclimation were usually associated with greater cold tolerance (Figure 1). This close relationship among rates of up-regulation of the known cold-induced genes and LT tolerance should not be unexpected as this is likely the reason why they were originally selected for study.

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