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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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Representation of up- and down-regulated genes. The Venn diagrams show the genes up- and down-regulated in the alloplasmic lines developed with the cytoplasm of Ae. uniaristata (T183), Ae. tauschii (T195) and H. chilense (TH237) in comparison with the corresponding euplasmic controls. A single gene, up-regulated in some comparisons and down-regulated in others, has been excluded in this analysis.
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Figure 2: Representation of up- and down-regulated genes. The Venn diagrams show the genes up- and down-regulated in the alloplasmic lines developed with the cytoplasm of Ae. uniaristata (T183), Ae. tauschii (T195) and H. chilense (TH237) in comparison with the corresponding euplasmic controls. A single gene, up-regulated in some comparisons and down-regulated in others, has been excluded in this analysis.

Mentions: A Welch t-test, using a two-fold change cut-off and a false discovery rate correction for multiple testing, identified 562 probe sets, each of them representing a putative gene, differentially modulated in at least one experimental comparison (Additional file 1: Table S1). When the wheat nuclear genome was combined with the cytoplasm of H. chilense, 540 genes significantly altered their expression (295 up- and 245 down-regulated), whereas 11 (2 up- and 9 down-regulated) and 28 (5 up- and 23 down-regulated) genes were significantly modulated in the alloplasmic lines carrying the cytoplasm of Ae. uniaristata and Ae.tauschii, respectively. Two up-regulated (Ta.24245.1.A1_at and TaAffx.57297.1.S1_at annotated as maturase with chloroplast and mitochondrial localization) and five down-regulated genes (TaAffx.6196.2.S1_s_at and TaAffx.6196.1.S1_atannotated as cyt b559, TaAffx.128795.10.S1_x_at annotated as ribosomal protein rps12, TaAffx.128617.1.S1_x_at annotated as NADPH-quinone oxidoreductase and TaAffx.128795.12.S1_x_atannotated as ABC transporter permease) were common in all comparisons (Figure 2), underlining some common responses across all alloplasmic lines. Significantly, the five down-regulated sequences were all encoded by the chloroplast genome.


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)

Representation of up- and down-regulated genes. The Venn diagrams show the genes up- and down-regulated in the alloplasmic lines developed with the cytoplasm of Ae. uniaristata (T183), Ae. tauschii (T195) and H. chilense (TH237) in comparison with the corresponding euplasmic controls. A single gene, up-regulated in some comparisons and down-regulated in others, has been excluded in this analysis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Representation of up- and down-regulated genes. The Venn diagrams show the genes up- and down-regulated in the alloplasmic lines developed with the cytoplasm of Ae. uniaristata (T183), Ae. tauschii (T195) and H. chilense (TH237) in comparison with the corresponding euplasmic controls. A single gene, up-regulated in some comparisons and down-regulated in others, has been excluded in this analysis.
Mentions: A Welch t-test, using a two-fold change cut-off and a false discovery rate correction for multiple testing, identified 562 probe sets, each of them representing a putative gene, differentially modulated in at least one experimental comparison (Additional file 1: Table S1). When the wheat nuclear genome was combined with the cytoplasm of H. chilense, 540 genes significantly altered their expression (295 up- and 245 down-regulated), whereas 11 (2 up- and 9 down-regulated) and 28 (5 up- and 23 down-regulated) genes were significantly modulated in the alloplasmic lines carrying the cytoplasm of Ae. uniaristata and Ae.tauschii, respectively. Two up-regulated (Ta.24245.1.A1_at and TaAffx.57297.1.S1_at annotated as maturase with chloroplast and mitochondrial localization) and five down-regulated genes (TaAffx.6196.2.S1_s_at and TaAffx.6196.1.S1_atannotated as cyt b559, TaAffx.128795.10.S1_x_at annotated as ribosomal protein rps12, TaAffx.128617.1.S1_x_at annotated as NADPH-quinone oxidoreductase and TaAffx.128795.12.S1_x_atannotated as ABC transporter permease) were common in all comparisons (Figure 2), underlining some common responses across all alloplasmic lines. Significantly, the five down-regulated sequences were all encoded by the chloroplast genome.

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