The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination

Abstract

Background: Mitochondrial genomes of flowering plants (angiosperms) are highly dynamic in genome structure. The mitogenome of the earliest angiosperm Amborella is remarkable in carrying rampant foreign DNAs, in contrast to Liriodendron, the other only known early angiosperm mitogenome that is described as 'fossilized'. The distinctive features observed in the two early flowering plant mitogenomes add to the current confusions of what early flowering plants look like. Expanded sampling would provide more details in understanding the mitogenomic evolution of early angiosperms. Here we report the complete mitochondrial genome of water lily Nymphaea colorata from Nymphaeales, one of the three orders of the earliest angiosperms.

Results: Assembly of data from Pac-Bio long-read sequencing yielded a circular mitochondria chromosome of 617,195 bp with an average depth of 601×. The genome encoded 41 protein coding genes, 20 tRNA and three rRNA genes with 25 group II introns disrupting 10 protein coding genes. Nearly half of the genome is composed of repeated sequences, which contributed substantially to the intron size expansion, making the gross intron length of the Nymphaea mitochondrial genome one of the longest among angiosperms, including an 11.4-Kb intron in cox2, which is the longest organellar intron reported to date in plants. Nevertheless, repeat mediated homologous recombination is unexpectedly low in Nymphaea evidenced by 74 recombined reads detected from ten recombinationally active repeat pairs among 886,982 repeat pairs examined. Extensive gene order changes were detected in the three early angiosperm mitogenomes, i.e. 38 or 44 events of inversions and translocations are needed to reconcile the mitogenome of Nymphaea with Amborella or Liriodendron, respectively. In contrast to Amborella with six genome equivalents of foreign mitochondrial DNA, not a single horizontal gene transfer event was observed in the Nymphaea mitogenome.

Conclusions: The Nymphaea mitogenome resembles the other available early angiosperm mitogenomes by a similarly rich 64-coding gene set, and many conserved gene clusters, whereas stands out by its highly repetitive nature and resultant remarkable intron expansions. The low recombination level in Nymphaea provides evidence for the predominant master conformation in vivo with a highly substoichiometric set of rearranged molecules.

Keywords: Mitochondrial genome; Nymphaea; PacBio sequencing; Recombination; Repeats.

Fig. 1

Mitochondrial genome map of Nymphaea colorata. The total length of the Nymphaea mitogenome is 617,195 bp. Genes (exons are shown as closed boxes) shown on the outside of the circle are transcribed clockwise, whereas those on the inside are transcribed counter-clockwise. Genes from the same protein complex are colored the same, introns are indicated in white boxes, and tRNAs of plastid origin are noted with a ‘-pt’ suffix. The inner circle shows the locations of direct (blue) and inverted (red) repeats (R1 to R10) with evidence for recombination activity (see Methods and Table 2). Numbers on the inner circle represent genome coordinates (Kb)

Fig. 2

Comparison of the length of 11 introns (see Additional file 4: Table S2) of the Nymphaea mitogenome with repeated sequence inserted with that of some selected seed plant mitogenomes

Fig. 3

Mitochondrial genome rearrangements and alternative genomic conformations observed from Nymphaea colorata based on repeat-mediated intra-molecular recombination products of three repeat pairs (R1, R2 and R3) that induced recombination with the highest frequencies as listed in Table 2