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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.

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