Abstract

BackgroundMitochondrial 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.ResultsAssembly 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.ConclusionsThe 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.

Highlights

  • Mitochondrial genomes of flowering plants are highly dynamic in genome structure

  • The relatively large size of Nymphaea Mitochondrial DNA (mtDNA) is primarily due to its abundant repetitive sequences, which add up to 301,676 bp and account for nearly half (49%) of the mitogenome, in contrast to most of other vascular plant mitogenomes with repeat ratio generally below 30% (Additional file 1: Table S1)

  • Nymphaea mt gene set differs from Amborella only by its presence of the functional protein-coding gene rps10 that is pseudogenized in Amborella, whereas differs from Liriodendron by its presence of plastid derived Transfer RNAs (tRNAs) gene trnL(CAA)-pt and absence of trnV(TAC)

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Summary

Introduction

Mitochondrial genomes of flowering plants (angiosperms) are highly dynamic in genome structure. We report the complete mitochondrial genome of water lily Nymphaea colorata from Nymphaeales, one of the three orders of the earliest angiosperms. Most (~ 80%, 176 out of 214) of the plant mitogenomes deposited in the GenBank database (https://www.ncbi.nlm.nih.gov/genome/organelle/) were generated in the past several years (since 2011). To date (as of July 2018), 53 bryophyte and 108 vascular plant complete mitogenomes have been reported (https://www.ncbi.nlm.nih.gov/genome/organelle/ ). Angiosperm mitogenomes exhibit highly dynamic characters: ranging from 66 Kb [10] to 11.3 Mb [7] with 19 to 64 [10] known genes (not including duplicate genes and ORFs), 5 [10] to 25 [1] introns, and highly variable intergenic regions [11]. The ca. 200-fold range of mitogenome size divergence is primarily due to the variation in non-coding regions, including repeated sequences [12], introns [13], intracellular transferred sequences from plastid [14] and nucleus [13], and horizontal gene transfers from foreign donors [15, 16]

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