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Cytoplasmic genome substitution in wheat affects the nuclear-cytoplasmic cross-talk leading to transcript and metabolite alterations.

Crosatti C, Quansah L, Maré C, Giusti L, Roncaglia E, Atienza SG, Cattivelli L, Fait A - BMC Genomics (2013)

Bottom Line: Metabolic profiling showed a comparable response of the central metabolism of the alloplasmic and euplasmic lines to light, while exposing larger metabolite alterations in the H. chilense alloplasmic line as compared with the Aegilops lines, in agreement with the transcriptomic data.Several stress-related metabolites, remarkably raffinose, were altered in content in the H. chilense alloplasmic line when exposed to high light, while amino acids, as well as organic acids were significantly decreased.Alterations in the levels of transcript, related to raffinose, and the photorespiration-related metabolisms were associated with changes in the level of related metabolites.

View Article: PubMed Central - HTML - PubMed

Affiliation: Jacob Blaustein Institutes for Desert Research, French Associates Institute for Agriculture and Biotechnology of Drylands, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990 Sde Boqer, Israel. luigi.cattivelli@entecra.it.

ABSTRACT

Background: Alloplasmic lines provide a unique tool to study nuclear-cytoplasmic interactions. Three alloplasmic lines, with nuclear genomes from Triticum aestivum and harboring cytoplasm from Aegilops uniaristata, Aegilops tauschii and Hordeum chilense, were investigated by transcript and metabolite profiling to identify the effects of cytoplasmic substitution on nuclear-cytoplasmic signaling mechanisms.

Results: In combining the wheat nuclear genome with a cytoplasm of H. chilense, 540 genes were significantly altered, whereas 11 and 28 genes were significantly changed in the alloplasmic lines carrying the cytoplasm of Ae. uniaristata or Ae. tauschii, respectively. We identified the RNA maturation-related process as one of the most sensitive to a perturbation of the nuclear-cytoplasmic interaction. Several key components of the ROS chloroplast retrograde signaling, together with the up-regulation of the ROS scavenging system, showed that changes in the chloroplast genome have a direct impact on nuclear-cytoplasmic cross-talk. Remarkably, the H. chilense alloplasmic line down-regulated some genes involved in the determination of cytoplasmic male sterility without expressing the male sterility phenotype. Metabolic profiling showed a comparable response of the central metabolism of the alloplasmic and euplasmic lines to light, while exposing larger metabolite alterations in the H. chilense alloplasmic line as compared with the Aegilops lines, in agreement with the transcriptomic data. Several stress-related metabolites, remarkably raffinose, were altered in content in the H. chilense alloplasmic line when exposed to high light, while amino acids, as well as organic acids were significantly decreased. Alterations in the levels of transcript, related to raffinose, and the photorespiration-related metabolisms were associated with changes in the level of related metabolites.

Conclusion: The replacement of a wheat cytoplasm with the cytoplasm of a related species affects the nuclear-cytoplasmic cross-talk leading to transcript and metabolite alterations. The extent of these modifications was limited in the alloplasmic lines with Aegilops cytoplasm, and more evident in the alloplasmic line with H. chilense cytoplasm. We consider that, this finding might be linked to the phylogenetic distance of the genomes.

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Metabolic pathway map for the alloplasmic genotype TH237 (H. chilense cytoplasm) subjected to high light treatment. Each data point is the fold change of the alloplasmic genotype on the euplasmic control. Circles and rectangles denote measured metabolites and metabolic genes, respectively. Blue, red and grey points indicate significant (p ≤ 0.05) increases, decreases and no change of metabolite and enzyme levels, respectively. Metabolic genes measured are mapped and indicated with enzyme EC numbers: arginine decarboxylase (4.1.1.19), asparaginase (3.5.1.1), glutamine synthetase (6.3.1.3), aspartyl-phosphate (2.7.2.4), threonine synthase (4.2.3.1), sucrose synthase (2.4.1.13), phospho-glucomutase (5.4.2.2), and β-fructofuranosidase (3.2.1.26).
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Figure 8: Metabolic pathway map for the alloplasmic genotype TH237 (H. chilense cytoplasm) subjected to high light treatment. Each data point is the fold change of the alloplasmic genotype on the euplasmic control. Circles and rectangles denote measured metabolites and metabolic genes, respectively. Blue, red and grey points indicate significant (p ≤ 0.05) increases, decreases and no change of metabolite and enzyme levels, respectively. Metabolic genes measured are mapped and indicated with enzyme EC numbers: arginine decarboxylase (4.1.1.19), asparaginase (3.5.1.1), glutamine synthetase (6.3.1.3), aspartyl-phosphate (2.7.2.4), threonine synthase (4.2.3.1), sucrose synthase (2.4.1.13), phospho-glucomutase (5.4.2.2), and β-fructofuranosidase (3.2.1.26).

Mentions: The direct comparison between the transcriptomic and metabolomic data in the H. chilense alloplasmic line exposed to HL allows the identification of some correspondences between changes in the expression of genes coding for enzymes and the corresponding metabolites (Figure 8). The most clear was the up-regulation of phospho-glucomutase (EC 5.4.2.2), sucrose synthase (EC 2.4.1.13) and β-fructofuranosidase (3.2.1.26) mRNAs that were associated with an increased accumulation of sugars and sugar phosphates.


Cytoplasmic genome substitution in wheat affects the nuclear-cytoplasmic cross-talk leading to transcript and metabolite alterations.

Crosatti C, Quansah L, Maré C, Giusti L, Roncaglia E, Atienza SG, Cattivelli L, Fait A - BMC Genomics (2013)

Metabolic pathway map for the alloplasmic genotype TH237 (H. chilense cytoplasm) subjected to high light treatment. Each data point is the fold change of the alloplasmic genotype on the euplasmic control. Circles and rectangles denote measured metabolites and metabolic genes, respectively. Blue, red and grey points indicate significant (p ≤ 0.05) increases, decreases and no change of metabolite and enzyme levels, respectively. Metabolic genes measured are mapped and indicated with enzyme EC numbers: arginine decarboxylase (4.1.1.19), asparaginase (3.5.1.1), glutamine synthetase (6.3.1.3), aspartyl-phosphate (2.7.2.4), threonine synthase (4.2.3.1), sucrose synthase (2.4.1.13), phospho-glucomutase (5.4.2.2), and β-fructofuranosidase (3.2.1.26).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4008262&req=5

Figure 8: Metabolic pathway map for the alloplasmic genotype TH237 (H. chilense cytoplasm) subjected to high light treatment. Each data point is the fold change of the alloplasmic genotype on the euplasmic control. Circles and rectangles denote measured metabolites and metabolic genes, respectively. Blue, red and grey points indicate significant (p ≤ 0.05) increases, decreases and no change of metabolite and enzyme levels, respectively. Metabolic genes measured are mapped and indicated with enzyme EC numbers: arginine decarboxylase (4.1.1.19), asparaginase (3.5.1.1), glutamine synthetase (6.3.1.3), aspartyl-phosphate (2.7.2.4), threonine synthase (4.2.3.1), sucrose synthase (2.4.1.13), phospho-glucomutase (5.4.2.2), and β-fructofuranosidase (3.2.1.26).
Mentions: The direct comparison between the transcriptomic and metabolomic data in the H. chilense alloplasmic line exposed to HL allows the identification of some correspondences between changes in the expression of genes coding for enzymes and the corresponding metabolites (Figure 8). The most clear was the up-regulation of phospho-glucomutase (EC 5.4.2.2), sucrose synthase (EC 2.4.1.13) and β-fructofuranosidase (3.2.1.26) mRNAs that were associated with an increased accumulation of sugars and sugar phosphates.

Bottom Line: Metabolic profiling showed a comparable response of the central metabolism of the alloplasmic and euplasmic lines to light, while exposing larger metabolite alterations in the H. chilense alloplasmic line as compared with the Aegilops lines, in agreement with the transcriptomic data.Several stress-related metabolites, remarkably raffinose, were altered in content in the H. chilense alloplasmic line when exposed to high light, while amino acids, as well as organic acids were significantly decreased.Alterations in the levels of transcript, related to raffinose, and the photorespiration-related metabolisms were associated with changes in the level of related metabolites.

View Article: PubMed Central - HTML - PubMed

Affiliation: Jacob Blaustein Institutes for Desert Research, French Associates Institute for Agriculture and Biotechnology of Drylands, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990 Sde Boqer, Israel. luigi.cattivelli@entecra.it.

ABSTRACT

Background: Alloplasmic lines provide a unique tool to study nuclear-cytoplasmic interactions. Three alloplasmic lines, with nuclear genomes from Triticum aestivum and harboring cytoplasm from Aegilops uniaristata, Aegilops tauschii and Hordeum chilense, were investigated by transcript and metabolite profiling to identify the effects of cytoplasmic substitution on nuclear-cytoplasmic signaling mechanisms.

Results: In combining the wheat nuclear genome with a cytoplasm of H. chilense, 540 genes were significantly altered, whereas 11 and 28 genes were significantly changed in the alloplasmic lines carrying the cytoplasm of Ae. uniaristata or Ae. tauschii, respectively. We identified the RNA maturation-related process as one of the most sensitive to a perturbation of the nuclear-cytoplasmic interaction. Several key components of the ROS chloroplast retrograde signaling, together with the up-regulation of the ROS scavenging system, showed that changes in the chloroplast genome have a direct impact on nuclear-cytoplasmic cross-talk. Remarkably, the H. chilense alloplasmic line down-regulated some genes involved in the determination of cytoplasmic male sterility without expressing the male sterility phenotype. Metabolic profiling showed a comparable response of the central metabolism of the alloplasmic and euplasmic lines to light, while exposing larger metabolite alterations in the H. chilense alloplasmic line as compared with the Aegilops lines, in agreement with the transcriptomic data. Several stress-related metabolites, remarkably raffinose, were altered in content in the H. chilense alloplasmic line when exposed to high light, while amino acids, as well as organic acids were significantly decreased. Alterations in the levels of transcript, related to raffinose, and the photorespiration-related metabolisms were associated with changes in the level of related metabolites.

Conclusion: The replacement of a wheat cytoplasm with the cytoplasm of a related species affects the nuclear-cytoplasmic cross-talk leading to transcript and metabolite alterations. The extent of these modifications was limited in the alloplasmic lines with Aegilops cytoplasm, and more evident in the alloplasmic line with H. chilense cytoplasm. We consider that, this finding might be linked to the phylogenetic distance of the genomes.

Show MeSH
Related in: MedlinePlus