Abstract
BackgroundChloroplasts and mitochondria evolved from the endosymbionts of once free-living eubacteria, and they transferred most of their genes to the host nuclear genome during evolution. The mechanisms used by plants to coordinate the expression of such transferred genes, as well as other genes in the host nuclear genome, are still poorly understood.ResultsIn this paper, we use nuclear-encoded chloroplast (cpRPGs), as well as mitochondrial (mtRPGs) and cytoplasmic (euRPGs) ribosomal protein genes to study the coordination of gene expression between organelles and the host. Results show that the mtRPGs, but not the cpRPGs, exhibit strongly synchronized expression with euRPGs in all investigated land plants and that this phenomenon is linked to the presence of a telo-box DNA motif in the promoter regions of mtRPGs and euRPGs. This motif is also enriched in the promoter regions of genes involved in DNA replication. Sequence analysis further indicates that mtRPGs, in contrast to cpRPGs, acquired telo-box from the host nuclear genome.ConclusionsBased on our results, we propose a model of plant nuclear genome evolution where coordination of activities in mitochondria and chloroplast and other cellular functions, including cell cycle, might have served as a strong selection pressure for the differential acquisition of telo-box between mtRPGs and cpRPGs. This research also highlights the significance of physiological needs in shaping transcriptional regulatory evolution.
Highlights
Chloroplasts and mitochondria evolved from the endosymbionts of once free-living eubacteria, and they transferred most of their genes to the host nuclear genome during evolution
Correlation analysis of the expression of cpRPGs, mtRPGs and euRPGs in Arabidopsis thaliana showed that the expression of mtRPGs was strongly positively correlated with the expression of euRPGs (Pearson’s Correlation Coefficient, PCC = 0.6260 ± 0.3220, p < 1.0E-10, t-test)
140 genes with “molecular function” annotation are mostly related to “RNA, nucleotide, nucleic acid or protein binding”, and “translation initiation factor activity” (Table 1). Since it has been shown in Drosophila [17] that euRPGs are regulated by a transcription factor, DREF, which participates in DNA replication, and since the expression of ribosomal protein genes is related to cell proliferation [18], we studied whether DNA replication genes in A. thaliana had coordinated expression with mtRPGs/euRPGs and showed enriched telo-boxes in their promoters
Summary
Chloroplasts and mitochondria evolved from the endosymbionts of once free-living eubacteria, and they transferred most of their genes to the host nuclear genome during evolution. Most of the genes in the endosymbionts were transferred to the nuclear genome during evolution, resulting in much smaller current organelle genomes than their ancient cousins [2,3,4]. In addition to the cytoplasmic ribosome of the host cell, mitochondria and chloroplasts each have their own respective ribosomes to translate proteins encoded in their genomes [9]. Since most organelle RPGs were transferred to the nuclear genome during evolution (Figure S1 in Additional File 1), specialized trans-factors and cis-elements may have evolved to ensure the expression of these transferred RPGs in a coordinated manner. We chose to examine the expression and regulatory patterns of these transferred RPGs
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