The complete mitochondrial genome of okra (Abelmoschus esculentus): using nanopore long reads to investigate gene transfer from chloroplast genomes and rearrangements of mitochondrial DNA molecules

Abstract

Background: Okra (Abelmoschus esculentus L. Moench) is an economically important crop and is known for its slimy juice, which has significant scientific research value. The A. esculentus chloroplast genome has been reported; however, the sequence of its mitochondrial genome is still lacking.

Results: We sequenced the plastid and mitochondrial genomes of okra based on Illumina short reads and Nanopore long reads and conducted a comparative study between the two organelle genomes. The plastid genome of okra is highly structurally conserved, but the mitochondrial genome of okra has been confirmed to have abundant subgenomic configurations. The assembly results showed that okra's mitochondrial genome existed mainly in the form of two independent molecules, which could be divided into four independent molecules through two pairs of long repeats. In addition, we found that four pairs of short repeats could mediate the integration of the two independent molecules into one complete molecule at a low frequency. Subsequently, we also found extensive sequence transfer between the two organelles of okra, where three plastid-derived genes (psaA, rps7 and psbJ) remained intact in the mitochondrial genome. Furthermore, psbJ, psbF, psbE and psbL were integrated into the mitochondrial genome as a conserved gene cluster and underwent pseudogenization as nonfunctional genes. Only psbJ retained a relatively complete sequence, but its expression was not detected in the transcriptome data, and we speculate that it is still nonfunctional. Finally, we characterized the RNA editing events of protein-coding genes located in the organelle genomes of okra.

Conclusions: In the current study, our results not only provide high-quality organelle genomes for okra but also advance our understanding of the gene dialogue between organelle genomes and provide information to breed okra cultivars efficiently.

Keywords: Abelmoschus esculentus; Mitochondrial genome; Okra; Organelle genome; RNA editing.

Fig. 1

The assembly graph of the A. esculentus mitogenome. Each colored segment is labeled with its size and named contig/R 1–12 by rank of size. Only segment 9, 11 and 12 representations are inferred as repeats. All segment adjacencies are supported by the long reads, indicating a complex branching genomic structure. The possible structures formed by high frequency rearrangements mediated by three long repeats were drew

Fig. 2

Schematic mitochondrial genome diagram of A. esculentus. Genes belonging to different functional groups are color-coded

Fig. 3

The location of repeats in the mtDNA of A. esculentus

Fig. 4

Schematic of homologous sequences identified among the two organelle genomes. A The blue arcs represent the mtpts with 100% similarity, the green arcs represent the mtpts has similarity be-tween 90 to 100%, the red arcs represent the mtpts has similarity between 80 to 90%, and the orange arcs represent the mtpts has similarity between less than 80%. B Phylogenetic tree base on the partial of mtpt14 sequences identified in cp DNA and mt DNA. The purple branches represent origin from mt DNA and green branches represent origin from cp DNA. The mt DNA mtpt14 and cp DNA mtpt14 are extracted from okra organelle genomes. The other sequences are downloaded from NCBI, the accession number and position are shown in the label

Fig. 5

Characteristics of the RNA editing sites identified in PCGs of A. esculentus organelle genomes. A The number of RNA editing sites identified in each PCGs of plastid genome; B The number of RNA editing sites identified in each PCGs of mitochondrial genome; C RNA editing type and their number identified in all PCGs. D RNA editing efficiency