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

Abstract

BackgroundTo 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.ResultsAnalysis 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.ConclusionThis 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.

Evaluation of freezing tolerance of winter wheat (Triticum aestivum L.) under controlled conditions and in the field

“…The duration of LT tolerance is determined by the rate of phenological development and the time to vegetative/reproductive transition . The Vrn-A1 locus is a master switch for pathway that determines the vegetative/reproductive transition and directly influences the duration of LT tolerance Laudencia-Chingcuanco et al, 2011). Laudencia-Chingcuanco et al (2011) have shown that after vegetative/reproductive transition plant continues to lose ability to cold acclimate so that at 70 days after cold treatment the winter-habit genotypes were almost as cold sensitive as the untreated springhabit genotypes.…”

“…The Vrn-A1 locus is a master switch for pathway that determines the vegetative/reproductive transition and directly influences the duration of LT tolerance Laudencia-Chingcuanco et al, 2011). Laudencia-Chingcuanco et al (2011) have shown that after vegetative/reproductive transition plant continues to lose ability to cold acclimate so that at 70 days after cold treatment the winter-habit genotypes were almost as cold sensitive as the untreated springhabit genotypes. Bergjord et al (2008) have noticed a gradual decline of cold tolerance of winter wheat after December.…”

“…Activation of Vrn1 causes the decrease in frost tolerance that begins when plants are fully vernalized . Vrn-A1 region is convergence point for pathway that determines the vegetative/reproductive transition thereby giving it a direct influence on the duration of expression of the rate determining LT tolerance genes Laudencia-Chingcuanco et al, 2011). The Fr-2 locus containing a cluster of C-repeat binding transcription factors is approximately 30 centimorgans proximal to Vrn-1 (Galiba et al, 1995).…”

Optimal Regulation of the Balance between Productivity and Overwintering of Perennial Grasses in a Warmer Climate

“…There are several reports describing de-acclimation and re-acclimation responses in perennial grass species [99][100][101][102][103][104][105], and some of them also report a negative association between freezing resistance and leaf growth during the de-acclimation period. In cereals, it has been shown that both freezing resistance and expression of cold-induced genes are down-regulated in shoot base tissue when the vernalization requirement is saturated, but before any development of the apex is visible in the microscope [106][107][108]. There is an interaction between vernalization and photoperiod on de-acclimation.…”

“…Several studies indicate that there is a negative association between expression level of VRN1 and the expression of cold-induced genes and freezing resistance. Using near-isogenic lines of wheat and barley, and a T. monococcum deletion mutant, it was shown that, under 16 h photoperiod, the VRN1 locus controls expression of VRN1, COR14B, and other cold induced-genes [106][107][108]112,118]. High expression levels of VRN1 were associated with the down-regulation of cold-induced genes and freezing resistance.…”