Rapid evolutionary divergence of diploid and allotetraploid Gossypium mitochondrial genomes

Abstract

Background: Cotton (Gossypium spp.) is commonly grouped into eight diploid genomic groups and an allotetraploid genomic group, AD. The mitochondrial genomes supply new information to understand both the evolution process and the mechanism of cytoplasmic male sterility. Based on previously released mitochondrial genomes of G. hirsutum (AD₁), G. barbadense (AD₂), G. raimondii (D₅) and G. arboreum (A₂), together with data of six other mitochondrial genomes, to elucidate the evolution and diversity of mitochondrial genomes within Gossypium.

Results: Six Gossypium mitochondrial genomes, including three diploid species from D and three allotetraploid species from AD genome groups (G. thurberi D₁, G. davidsonii D_3-d and G. trilobum D₈; G. tomentosum AD₃, G. mustelinum AD₄ and G. darwinii AD₅), were assembled as the single circular molecules of lengths about 644 kb in diploid species and 677 kb in allotetraploid species, respectively. The genomic structures of mitochondrial in D group species were identical but differed from the mitogenome of G. arboreum (A₂), as well as from the mitogenomes of five species of the AD group. There mainly existed four or six large repeats in the mitogenomes of the A + AD or D group species, respectively. These variations in repeat sequences caused the major inversions and translocations within the mitochondrial genome. The mitochondrial genome complexity in Gossypium presented eight unique segments in D group species, three specific fragments in A + AD group species and a large segment (more than 11 kb) in diploid species. These insertions or deletions were most probably generated from crossovers between repetitive or homologous regions. Unlike the highly variable genome structure, evolutionary distance of mitochondrial genes was 1/6th the frequency of that in chloroplast genes of Gossypium. RNA editing events were conserved in cotton mitochondrial genes. We confirmed two near full length of the integration of the mitochondrial genome into chromosome 1 of G. raimondii and chromosome A03 of G. hirsutum, respectively, with insertion time less than 1.03 MYA.

Conclusion: Ten Gossypium mitochondrial sequences highlight the insights to the evolution of cotton mitogenomes.

Keywords: Comparative genomics; Gossypium; Mitochondrial genomes; Multiple DNA rearrangement; Repeat sequences; Unique segments.

Fig. 1

Genome maps of three diploid Gossypium mitogenomes. The map shows both the gene map (outer circle) and repeat map (inner map). Genes exhibited on the inside of outer circles are transcribed in a clockwise direction, while genes on the outside of outer circles are transcribed in a reverse direction. The inner circle reveals the distribution of repeats in two mitogenomes with curved lines and ribbons connecting pairs of repeats and width proportional to repeat size. The red ribbons represent > = 1 Kb repeats, the very deep green lines represent repeats between 100 bp to 1 Kb and the very light grey lines represent repeats <100 bp. The numbers give genome coordinates in kilobase

Fig. 2

Genome maps of three allotetraploid Gossypium mitogenomes. The map explanations were the same to Fig. 1

Fig. 3

Progressive Mauve show the genome size variation and the global rearrangement structure of 10 mitochondrial chromosomes among Gossypium. The mitogenome of G. arboreum (A₂) is the largest with a circular DNA molecule of 687,482 base pairs (bp) while the smallest mitogenome (from G. hirsutum AD₁) is only 621,884 bp. Each genome is laid out horizontally and homologous segments are shown as colored blocks connected across genomes. Blocks that are shifted downward in any genome represented segments that are inverted relative to the reference genome (G. thurberi D₁)

Fig. 4

Observed coverage of mapped paired-end reads supporting the existence of a large insertion or deletion in Gossypium species. IGV screenshot of the variability and coverage observed in ten Gossypium sequence samples. Upper panel represent the unique sequences coordinates. There are ten panels corresponding to the different Gossypium sequences. The track in each of these panels describes the density of read mapping or coverage depth. a: unique segment in D group. b: unique segment in A + AD group. c: unique segment in diploid groups

Fig. 5

Maximum likelihood (ML) phylogenetic tree of ten Gossypium species was constructed based on nucleotide sequences of 36 mitochondrial genes. Bootstrap values for all major divergences were high (>70%) on the corresponding nodes. The hollow or black bars represent unique present or absent segments in ten Gossypium mitogenomes

Fig. 6

Distribution of p-distances from 78 chloroplast and 36 mitochondrial protein-coding exons among 10 Gossypium species

Fig. 7

Mitochondrial DNAs insertions into four Gossypium nuclear genomes detected by whole-genome alignment. The results were filtered to select only those alignments which comprise the one-to-one mapping between reference and query, and then display a dotplot of the selected alignments. The red and blue lines refer positive and reverse matches, respectively. a: Dot matrix analysis of numts in Gossypium raimondii (D₅) nuclear genome performed using MUMmer (Delcher et al., 2002). b: Dot matrix analysis of numts in G. arboreum (A₂) nuclear genome. c: Dot matrix analysis of numts in G. hirsutum (AD₁) nuclear genome. d: Dot matrix analysis of numts in G. barbadense (AD₂) nuclear genome

Fig. 8

p-distances (a) and estimated divergence time (b) of two recent nearly full length insertion in G. raimondii (Chr01, Fig. 7a) and G. hirsutum (Chr A03, Fig. 7c)