The complete chloroplast and mitochondrial genome sequences of Boea hygrometrica: insights into the evolution of plant organellar genomes

Abstract

The complete nucleotide sequences of the chloroplast (cp) and mitochondrial (mt) genomes of resurrection plant Boea hygrometrica (Bh, Gesneriaceae) have been determined with the lengths of 153,493 bp and 510,519 bp, respectively. The smaller chloroplast genome contains more genes (147) with a 72% coding sequence, and the larger mitochondrial genome have less genes (65) with a coding faction of 12%. Similar to other seed plants, the Bh cp genome has a typical quadripartite organization with a conserved gene in each region. The Bh mt genome has three recombinant sequence repeats of 222 bp, 843 bp, and 1474 bp in length, which divide the genome into a single master circle (MC) and four isomeric molecules. Compared to other angiosperms, one remarkable feature of the Bh mt genome is the frequent transfer of genetic material from the cp genome during recent Bh evolution. We also analyzed organellar genome evolution in general regarding genome features as well as compositional dynamics of sequence and gene structure/organization, providing clues for the understanding of the evolution of organellar genomes in plants. The cp-derived sequences including tRNAs found in angiosperm mt genomes support the conclusion that frequent gene transfer events may have begun early in the land plant lineage.

Figure 1. The circular-mapping chloroplast genome of B. hygrometrica.

Features on transcriptionally clockwise and counter-clockwise strands are drawn on the inside and outside of the outer circle, respectively. Genes belonging to different groups are color-coded (Ψ, pseudogene). The genome coordinate and GC content are shown in the inner circle. The thick lines indicate inverted repeats (IRA and IRB), which separate the genome into small (SSC) and large (LSC) single copy regions. The map was drawn by using OGDRAW .

Figure 2. The circular-mapping mitochondrial genome of B. hygrometrica.

Features on transcriptionally clockwise and counter-clockwise strands are drawn on the inside and outside of the outer circle, respectively. The genome coordinate and GC content are shown in the inner circle. Genes belonging to different groups are color-coded. The map was drawn by using OGDRAW .

Figure 3. Production of various molecular structures from the MC molecule by intra-molecular recombination between 3 different repeat pairs.

A, B, C, D, E, and F are 6 segments separated by repeat pairs. Underlined segments are the negative strand as compared to the MC molecule. Three repeat pairs are shown in different colors. The keys show repeat name, length, and matching direction. F and P stand for forward and palindromic matches, respectively.

Figure 4. Distribution of tRNA genes in 15 plant mt genomes.

Figure 5. Phylogenetic distribution of gene gain and loss from chloroplast and mitochondrial genomes in plant lineages.

The genes that are gained independently in different lineages are underlined. Genes of chloroplast and mitochondrial origins are indicated with green and red, respectively. Phylogenetic relationships of the plants are determined based on the conserved genes of chloroplast genomes described in Figure S2.