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Non-functional plastid ndh gene fragments are present in the nuclear genome of Norway spruce (Picea abies L. Karsch): insights from in silico analysis of nuclear and organellar genomes

Abstract

Many genes have been lost from the prokaryote plastidial genome during the early events of endosymbiosis in eukaryotes. Some of them were definitively lost, but others were relocated and functionally integrated to the host nuclear genomes through serial events of gene transfer during plant evolution. In gymnosperms, plastid genome sequencing has revealed the loss of ndh genes from several species of Gnetales and Pinaceae, including Norway spruce (Picea abies). This study aims to trace the ndh genes in the nuclear and organellar Norway spruce genomes. The plastid genomes of higher plants contain 11 ndh genes which are homologues of mitochondrial genes encoding subunits of the proton-pumping NADH-dehydrogenase (nicotinamide adenine dinucleotide dehydrogenase) or complex I (electron transport chain). Ndh genes encode 11 NDH polypeptides forming the Ndh complex (analogous to complex I) which seems to be primarily involved in chloro-respiration processes. We considered ndh genes from the plastidial genome of four gymnosperms (Cryptomeria japonica, Cycas revoluta, Ginkgo biloba, Podocarpus totara) and a single angiosperm species (Arabidopsis thaliana) to trace putative homologs in the nuclear and organellar Norway spruce genomes using tBLASTn to assess the evolutionary fate of ndh genes in Norway spruce and to address their genomic location(s), structure, integrity and functionality. The results obtained from tBLASTn were subsequently analyzed by performing homology search for finding ndh specific conserved domains using conserved domain search. We report the presence of non-functional plastid ndh gene fragments, excepting ndhE and ndhG genes, in the nuclear genome of Norway spruce. Regulatory transcriptional elements like promoters, TATA boxes and enhancers were detected in the upstream regions of some ndh fragments. We also found transposable elements in the flanking regions of few ndh fragments suggesting nuclear rearrangements in those regions. These evidences support the hypothesis that, at least in Picea, ndh translocations from the plastid to the nuclear genome have occurred, and that there might have been a functional machinery at some time during evolution to accommodate them within a nuclear-encoded environment, or attempts to form it.

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Acknowledgments

We acknowledge Andrea Zuccolo for support in the transposable elements (TEs) analysis. We also acknowledge the Swedish research Council (VR) and the Swedish Governmental Agency for Innovation Systems (VINNOVA) for supporting the infrastructure to maintain P. abies genome assembly as publically available at Umeå Plant Science Centre (UPSC), Umeå, Sweden. S.S.R. postdoc position was granted by the Kempe foundation. This research was partly supported by funds from the Spanish Ministry of Education and Science (Project CGL2010-22347-C02-01).

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Correspondence to Sonali Sachin Ranade.

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This study was funded by Swedish research Council (VR), the Swedish Governmental Agency for Innovation Systems (VINNOVA), Kempe foundation and the Spanish Ministry of Education and Science (Project CGL2010-22347-C02-01).

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Communicated by B. F. Lang.

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Ranade, S.S., García-Gil, M.R. & Rosselló, J.A. Non-functional plastid ndh gene fragments are present in the nuclear genome of Norway spruce (Picea abies L. Karsch): insights from in silico analysis of nuclear and organellar genomes. Mol Genet Genomics 291, 935–941 (2016). https://doi.org/10.1007/s00438-015-1159-7

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  • DOI: https://doi.org/10.1007/s00438-015-1159-7

Keywords

  • ndh genes
  • Picea abies
  • Norway spruce gene transfer
  • Organellar genomes