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Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome.

Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L - BMC Genomics (2009)

Bottom Line: Some drought-related genes were expressed at lower level (or not expressed) in Creso (which lacks the D genome) or in the CS_5AL-10 deletion line compared to CS.Genes involved in ABA, proline, glycine-betaine and sorbitol pathways were found up-regulated by drought stress.When a genomic stress (deletion of a chromosomal region) was combined with low water availability, a molecular response based on the activation of transposons and retrotransposons was observed.

View Article: PubMed Central - HTML - PubMed

Affiliation: CRA-Genomic Research Centre, Fiorenzuola d'Arda, Piacenza, Italy. alessio.aprile@libero.it

ABSTRACT

Background: Water stress during grain filling has a marked effect on grain yield, leading to a reduced endosperm cell number and thus sink capacity to accumulate dry matter. The bread wheat cultivar Chinese Spring (CS), a Chinese Spring terminal deletion line (CS_5AL-10) and the durum wheat cultivar Creso were subjected to transcriptional profiling after exposure to mild and severe drought stress at the grain filling stage to find evidences of differential stress responses associated to different wheat genome regions.

Results: The transcriptome analysis of Creso, CS and its deletion line revealed 8,552 non redundant probe sets with different expression levels, mainly due to the comparisons between the two species. The drought treatments modified the expression of 3,056 probe sets. Besides a set of genes showing a similar drought response in Creso and CS, cluster analysis revealed several drought response features that can be associated to the different genomic structure of Creso, CS and CS_5AL-10. Some drought-related genes were expressed at lower level (or not expressed) in Creso (which lacks the D genome) or in the CS_5AL-10 deletion line compared to CS. The chromosome location of a set of these genes was confirmed by PCR-based mapping on the D genome (or the 5AL-10 region). Many clusters were characterized by different level of expression in Creso, CS and CS_AL-10, suggesting that the different genome organization of the three genotypes may affect plant adaptation to stress. Clusters with similar expression trend were grouped and functional classified to mine the biological mean of their activation or repression. Genes involved in ABA, proline, glycine-betaine and sorbitol pathways were found up-regulated by drought stress. Furthermore, the enhanced expression of a set of transposons and retrotransposons was detected in CS_5AL-10.

Conclusion: Bread and durum wheat genotypes were characterized by a different physiological reaction to water stress and by a substantially different molecular response. The genome organization accounted for differences in the expression level of hundreds of genes located on the D genome or controlled by regulators located on the D genome. When a genomic stress (deletion of a chromosomal region) was combined with low water availability, a molecular response based on the activation of transposons and retrotransposons was observed.

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Brief overview of the ABA pathway (inferred by KEGG, [45]). On the left side the β-carotene biosynthesis steps. On the right the ABA-dedicated enzymatic reactions. Several probe sets related to ABA synthesis enzymes (PSY, LYC- β, β-OHase, NCED) were up-regulated by drought stress. Their expression levels based on array data are showed in the corresponding histograms. 2.5.1.32 = Phytoene synthase (PSY); 1.14.99.-= Phytoene desaturase (PDS); 1.14.99.30 = ζ-carotene desaturase (ZDS); 1.14.-.-= Lycopene β-cyclase (LYC-β); 1.14.13.- = β-carotene hydroxylase (β-OHase); 1.10.99.3 = Violaxanthin de-epoxidase (NPQ1); 1.14.13.90 = Zeaxanthin epoxidase (ZEP); 1.13.11.51 = 9-cis-epoxycarotenoid dioxygenase (NCED); 1.1.1.288 = xanthoxin dehydrogenase (ABA2); 1.2.3.14 = Abscisic aldehyde oxidase (AAO).
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Figure 4: Brief overview of the ABA pathway (inferred by KEGG, [45]). On the left side the β-carotene biosynthesis steps. On the right the ABA-dedicated enzymatic reactions. Several probe sets related to ABA synthesis enzymes (PSY, LYC- β, β-OHase, NCED) were up-regulated by drought stress. Their expression levels based on array data are showed in the corresponding histograms. 2.5.1.32 = Phytoene synthase (PSY); 1.14.99.-= Phytoene desaturase (PDS); 1.14.99.30 = ζ-carotene desaturase (ZDS); 1.14.-.-= Lycopene β-cyclase (LYC-β); 1.14.13.- = β-carotene hydroxylase (β-OHase); 1.10.99.3 = Violaxanthin de-epoxidase (NPQ1); 1.14.13.90 = Zeaxanthin epoxidase (ZEP); 1.13.11.51 = 9-cis-epoxycarotenoid dioxygenase (NCED); 1.1.1.288 = xanthoxin dehydrogenase (ABA2); 1.2.3.14 = Abscisic aldehyde oxidase (AAO).

Mentions: Thirty-two probe sets related to ten enzymes of carotenoid-ABA biosynthesis are present on the Affymetrix wheat microarray. Figure 4 illustrates a schematic representation of the biosynthetic pathway [45,46] with indication of the probe sets corresponding to the enzymes modified during drought treatment. In the additional file 2 (ABA-related probe sets) all probe sets corresponding to ABA biosynthetic enzymes are listed with their expression level. The transcripts encoding NCED were the most significantly up-regulated in response to drought in all genotypes (Figure 4). In other species, a detailed study of NCED expression during water stress has shown a tight correlation between mRNA expression, protein level, and ABA content in dehydrated leaves and roots, indicating a regulatory role of NCED in ABA biosynthesis [47]. Furthermore, over-expression of NCED in tomato plants results in the over-production of ABA [48]. The microarray carries 12 NCED-related probe sets (additional file 2: ABA-related probe sets): four were not expressed, four were expressed and not modulated during dehydration treatment, while four probe sets (Ta.12813.1.S1_x_at, Ta.12813.2.S1_x_at, TaAffx.13292.1.S1_at and TaAffx.13292.1.S1_s_at) were differentially expressed with a cluster 3-related expression profile (the more severe the stress, the higher the expression level in all genotypes). These data support the hypothesis that, like in other plants, wheat ABA synthesis is regulated mainly through transcriptional induction of NCED.


Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome.

Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L - BMC Genomics (2009)

Brief overview of the ABA pathway (inferred by KEGG, [45]). On the left side the β-carotene biosynthesis steps. On the right the ABA-dedicated enzymatic reactions. Several probe sets related to ABA synthesis enzymes (PSY, LYC- β, β-OHase, NCED) were up-regulated by drought stress. Their expression levels based on array data are showed in the corresponding histograms. 2.5.1.32 = Phytoene synthase (PSY); 1.14.99.-= Phytoene desaturase (PDS); 1.14.99.30 = ζ-carotene desaturase (ZDS); 1.14.-.-= Lycopene β-cyclase (LYC-β); 1.14.13.- = β-carotene hydroxylase (β-OHase); 1.10.99.3 = Violaxanthin de-epoxidase (NPQ1); 1.14.13.90 = Zeaxanthin epoxidase (ZEP); 1.13.11.51 = 9-cis-epoxycarotenoid dioxygenase (NCED); 1.1.1.288 = xanthoxin dehydrogenase (ABA2); 1.2.3.14 = Abscisic aldehyde oxidase (AAO).
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Figure 4: Brief overview of the ABA pathway (inferred by KEGG, [45]). On the left side the β-carotene biosynthesis steps. On the right the ABA-dedicated enzymatic reactions. Several probe sets related to ABA synthesis enzymes (PSY, LYC- β, β-OHase, NCED) were up-regulated by drought stress. Their expression levels based on array data are showed in the corresponding histograms. 2.5.1.32 = Phytoene synthase (PSY); 1.14.99.-= Phytoene desaturase (PDS); 1.14.99.30 = ζ-carotene desaturase (ZDS); 1.14.-.-= Lycopene β-cyclase (LYC-β); 1.14.13.- = β-carotene hydroxylase (β-OHase); 1.10.99.3 = Violaxanthin de-epoxidase (NPQ1); 1.14.13.90 = Zeaxanthin epoxidase (ZEP); 1.13.11.51 = 9-cis-epoxycarotenoid dioxygenase (NCED); 1.1.1.288 = xanthoxin dehydrogenase (ABA2); 1.2.3.14 = Abscisic aldehyde oxidase (AAO).
Mentions: Thirty-two probe sets related to ten enzymes of carotenoid-ABA biosynthesis are present on the Affymetrix wheat microarray. Figure 4 illustrates a schematic representation of the biosynthetic pathway [45,46] with indication of the probe sets corresponding to the enzymes modified during drought treatment. In the additional file 2 (ABA-related probe sets) all probe sets corresponding to ABA biosynthetic enzymes are listed with their expression level. The transcripts encoding NCED were the most significantly up-regulated in response to drought in all genotypes (Figure 4). In other species, a detailed study of NCED expression during water stress has shown a tight correlation between mRNA expression, protein level, and ABA content in dehydrated leaves and roots, indicating a regulatory role of NCED in ABA biosynthesis [47]. Furthermore, over-expression of NCED in tomato plants results in the over-production of ABA [48]. The microarray carries 12 NCED-related probe sets (additional file 2: ABA-related probe sets): four were not expressed, four were expressed and not modulated during dehydration treatment, while four probe sets (Ta.12813.1.S1_x_at, Ta.12813.2.S1_x_at, TaAffx.13292.1.S1_at and TaAffx.13292.1.S1_s_at) were differentially expressed with a cluster 3-related expression profile (the more severe the stress, the higher the expression level in all genotypes). These data support the hypothesis that, like in other plants, wheat ABA synthesis is regulated mainly through transcriptional induction of NCED.

Bottom Line: Some drought-related genes were expressed at lower level (or not expressed) in Creso (which lacks the D genome) or in the CS_5AL-10 deletion line compared to CS.Genes involved in ABA, proline, glycine-betaine and sorbitol pathways were found up-regulated by drought stress.When a genomic stress (deletion of a chromosomal region) was combined with low water availability, a molecular response based on the activation of transposons and retrotransposons was observed.

View Article: PubMed Central - HTML - PubMed

Affiliation: CRA-Genomic Research Centre, Fiorenzuola d'Arda, Piacenza, Italy. alessio.aprile@libero.it

ABSTRACT

Background: Water stress during grain filling has a marked effect on grain yield, leading to a reduced endosperm cell number and thus sink capacity to accumulate dry matter. The bread wheat cultivar Chinese Spring (CS), a Chinese Spring terminal deletion line (CS_5AL-10) and the durum wheat cultivar Creso were subjected to transcriptional profiling after exposure to mild and severe drought stress at the grain filling stage to find evidences of differential stress responses associated to different wheat genome regions.

Results: The transcriptome analysis of Creso, CS and its deletion line revealed 8,552 non redundant probe sets with different expression levels, mainly due to the comparisons between the two species. The drought treatments modified the expression of 3,056 probe sets. Besides a set of genes showing a similar drought response in Creso and CS, cluster analysis revealed several drought response features that can be associated to the different genomic structure of Creso, CS and CS_5AL-10. Some drought-related genes were expressed at lower level (or not expressed) in Creso (which lacks the D genome) or in the CS_5AL-10 deletion line compared to CS. The chromosome location of a set of these genes was confirmed by PCR-based mapping on the D genome (or the 5AL-10 region). Many clusters were characterized by different level of expression in Creso, CS and CS_AL-10, suggesting that the different genome organization of the three genotypes may affect plant adaptation to stress. Clusters with similar expression trend were grouped and functional classified to mine the biological mean of their activation or repression. Genes involved in ABA, proline, glycine-betaine and sorbitol pathways were found up-regulated by drought stress. Furthermore, the enhanced expression of a set of transposons and retrotransposons was detected in CS_5AL-10.

Conclusion: Bread and durum wheat genotypes were characterized by a different physiological reaction to water stress and by a substantially different molecular response. The genome organization accounted for differences in the expression level of hundreds of genes located on the D genome or controlled by regulators located on the D genome. When a genomic stress (deletion of a chromosomal region) was combined with low water availability, a molecular response based on the activation of transposons and retrotransposons was observed.

Show MeSH
Related in: MedlinePlus