Open Access Research article

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

Cristina Crosatti2, Lydia Quansah1, Caterina Maré2, Lorenzo Giusti2, Enrica Roncaglia4, Sergio G Atienza3, Luigi Cattivelli2* and Aaron Fait1*

Author Affiliations

1 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

2 Consiglio per la Ricerca e la Sperimentazione in Agricoltura -Genomics Research Centre, via S. Protaso 302, 29017 Fiorenzuola d’ Arda, (PC), Italy

3 Departamento de Mejora Genética, IAS-CSIC, Apdo. 4084, Cordoba 14980, Spain

4 Center for Genome Research, Biomedical Sciences Department, Biological Chemistry Section, University of Modena and Reggio Emilia, Via G. Campi 287, 41125 Modena, Italy

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BMC Genomics 2013, 14:868  doi:10.1186/1471-2164-14-868

Published: 10 December 2013

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.

Keywords:
Wheat; Alloplasmic line; Nuclear-cytoplasmic interaction; ROS signaling; Cytoplasmic male sterility