Repetitive Elements, Sequence Turnover and Cyto-Nuclear Gene Transfer in Gymnosperm Mitogenomes

Abstract

Among the three genomes in plant cells, the mitochondrial genome (mitogenome) is the least studied due to complex recombination and intergenomic transfer. In gymnosperms only ∼20 mitogenomes have been released thus far, which hinders a systematic investigation into the tempo and mode of mitochondrial DNA evolution in seed plants. Here, we report the complete mitogenome sequence of Platycladus orientalis (Cupressaceae). This mitogenome is assembled as two circular-mapping chromosomes with a size of ∼2.6 Mb and which contains 32 protein-coding genes, three rRNA and seven tRNA genes, and 1,068 RNA editing sites. Repetitive sequences, including dispersed repeats, transposable elements (TEs), and tandem repeats, made up 23% of the genome. Comparative analyses with 17 other mitogenomes representing the five gymnosperm lineages revealed a 30-fold difference in genome size, 80-fold in repetitive content, and 230-fold in substitution rate. We found dispersed repeats are highly associated with mitogenome expansion (r = 0.99), and most of them were accumulated during recent duplication events. Syntenic blocks and shared sequences between mitogenomes decay rapidly with divergence time (r = 0.53), with the exceptions of Ginkgo and Cycads which retained conserved genome structure over long evolutionary time. Our phylogenetic analysis supports a sister group relationship of Cupressophytes and Gnetophytes; both groups are unique in that they lost 8–12 protein-coding genes, of which 4–7 intact genes are likely transferred to nucleus. These two clades also show accelerated and highly variable substitution rates relative to other gymnosperms. Our study highlights the dynamic and enigmatic evolution of gymnosperm mitogenomes.

Complete mitochondrial genome of Thuja sutchuenensis and its implications on evolutionary analysis of complex mitogenome architecture in Cupressaceae

“…orientalis , Larix sibirica and Picea sitchensis (Bong.) Carrière, which were composed of 2, 9 and 13 segments, respectively [ 4 , 12 , 13 ].…”

“…However, gymnosperms only make up a small portion of the published plant mitogenomes; the majority come from angiosperms. Only 33 gymnosperm mitogenomes (including draft mitogenomes) have been reported to date [ 4 , 8 – 13 ]. Previous research has demonstrated that the gymnosperm mitogenome has undergone substantial changes in genomic size, physical structure, and gene composition [ 4 , 8 – 13 ].…”

“…Only 33 gymnosperm mitogenomes (including draft mitogenomes) have been reported to date [ 4 , 8 – 13 ]. Previous research has demonstrated that the gymnosperm mitogenome has undergone substantial changes in genomic size, physical structure, and gene composition [ 4 , 8 – 13 ]. For example, the genome size of Larix sibirica Ledeb.…”

“…Cupressaceae, as the most widely distributed and the second largest family among gymnosperms (the number of species is only second to Pinaceae), is an essential component of Conifer II. However, Cupressaceae has only reported six assembled mitogenomes to date, including five draft mitogenomes and one complete mitogenome [ 9 , 10 , 13 ]. This may greatly hinder a deep understanding of the evolution of mitogenomes in this large family, even gymnosperms.…”

Integration of large and diverse angiosperm DNA fragments into Asian Gnetum mitogenomes

“…Two alternative hypotheses can explain their origins: (1) they were originally ancient angiosperm mitochondrial DNA fragments independently inserted into the common ancestor’s mitogenomes of the two Asia Gnetum clades or (2) they were initially seed plant descendants but had been lost from all gymnosperms except Gnetum . The second hypothesis is unlikely because Gnetum mitogenomes have drastically elevated rates of nucleotide substitutions with frequent gene loss [ 34 , 35 ].…”