Abstract

The genus Trifolium is the largest of the tribe Trifolieae in the subfamily Papilionoideae (Fabaceae). The paucity of mitochondrial genome (mitogenome) sequences has hindered comparative analyses among the three genomic compartments of the plant cell (nucleus, mitochondrion and plastid). We assembled four mitogenomes from the two subgenera (Chronosemium and Trifolium) of the genus. The four Trifolium mitogenomes were compact (294,911–348,724 bp in length) and contained limited repetitive (6.6–8.6%) DNA. Comparison of organelle repeat content highlighted the distinct evolutionary trajectory of plastid genomes in a subset of Trifolium species. Intracellular gene transfer (IGT) was analyzed among the three genomic compartments revealing functional transfer of mitochondrial rps1 to nuclear genome along with other IGT events. Phylogenetic analysis based on mitochondrial and nuclear rps1 sequences revealed that the functional transfer in Trifolieae was independent from the event that occurred in robinioid clade that includes genus Lotus. A novel, independent fission event of ccmFn in Trifolium was identified, caused by a 59 bp deletion. Fissions of this gene reported previously in land plants were reassessed and compared with Trifolium.

Highlights

  • Transfer of mitochondrial DNA to the nuclear genome is an ongoing process in both of plants and animals but functional transfer of mitochondrial genes has almost ceased in animals [14]

  • Mitochondrial intracellular gene transfer (IGT) events may be successful or unsuccessful in terms of functionality and the phylogenetic distribution of pseudogenization and deletion of mitochondrial genes can be assessed in descendant lineages [17]

  • Mitochondrial contigs were selected by BLAST searches against reference Fabaceae mitogenome sequences at National Center for Biotechnology Information (NCBI) using BLASTN 2.8.0+ [63] with default options

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Summary

Introduction

Plant cells comprise three genomic compartments (i.e., nucleus, mitochondrion and plastid). Substitution rates of mitochondrial protein coding genes, are the most conservative among the three genomic compartments [9]. The relative rate of synonymous substitutions of mitogenome, plastome and nuclear genome is 1:3:16 [10]. Nuclear genome sequences that originate from the mitogenome and plastome are referred to as nuclear mitochondrial DNA sequences (NUMTs) and nuclear plastid DNA sequences (NUPTs), respectively [12,13]. Transfer of mitochondrial DNA to the nuclear genome is an ongoing process in both of plants and animals but functional transfer of mitochondrial genes has almost ceased in animals [14]. Transfer of mitochondrial genes to the nuclear genome cannot substitute function of the original mitochondrial copy unless the nuclear copy acquires the appropriate expression and targeting signals [15]. Mitochondrial IGT events may be successful or unsuccessful in terms of functionality and the phylogenetic distribution of pseudogenization and deletion of mitochondrial genes can be assessed in descendant lineages [17]

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