Genomic variation and evolutionary patterns in organelle genomes between annual and perennial Glycine species

Abstract

Background: The complexity of structural variations and long stretches of repetitive DNA make the analysis of plant mitochondrial genomes (mitogenomes) exceptionally challenging. A thorough investigation of plant mitogenomes is essential for uncovering the evolutionary processes of plant organelles and optimizing traits related to plant cellular metabolism. The genus Glycine includes groups with both perennial and annual life strategies, making it an ideal subject for studying the complexity and variations of plant mitogenomes during evolution across different life strategies.

Results: Here, we assembled 20 complete mitochondrial and plastid genomes of Glycine accessions, including both annual and perennial species using the latest organelle genome assembly tool. Significant structural variations and differences in tRNA content were observed in the mitogenomes between the two life-history strategy subgenera, while protein-coding genes and rRNAs content were highly conserved. Distinct patterns of nuclear plastid DNAs and nuclear mitochondrial DNAs (NUPTs/NUMTs) were uncovered among annual and perennial species. Genes residing in NUMTs (NUMGs) showed a substantial presence in Glycine accessions, with annual soybeans exhibiting a higher proportion of protein-coding genes fully integrated into the nuclear genome. Phylogenetic analysis indicated a closely related evolutionary trajectory between mitochondrial and nuclear genomes in Glycine, providing supplementary evidence relevant to the evolutionary history of Glycine.

Conclusions: This study showed the structural variations and evolutionary patterns of mitochondrial genomes between annual and perennial Glycine species. These findings contribute to our understanding of plant organelle complexity, variation and history of intracellular genomic integration.

Keywords: Glycine; Intracellular transfer; Mitochondrion; Plastid.

Fig. 1

Mitogenome structure of 20 Glycine accessions. A, The mitogenome structure of 6 perennial Glycine species: Gcy, Glycine cyrtoloba; Gdo, Glycine dolichocarpa; Gfa, Glycine falcata; Gst, Glycine stenophita; Gsy, Glycine syndetika; GtoD3, Glycine tomentella D3 (marked with a red box). B, The mitogenome structure of 3 annual wild soybeans (Glycine soja): SoyW01, SoyW02, SoyW03 (marked with a yellow box). C, The mitogenome structure of 6 annual cultivar soybeans (Glycine max): SoyC01, SoyC05, SoyC06, SoyC07, SoyC08, SoyC10 (marked with a blue box). D, The mitogenome structure of 5 annual landrace soybeans (Glycine max): SoyL01, SoyL03, SoyL04, SoyL07, SoyL08 (marked with a blue box). The mitogenomes were visualized using Bandage, with the distinct colors being randomly assigned by the software

Fig. 2

Gene content of 20 Glycine organelle genomes. A, Gene content of 20 Glycine mitogenomes. B and C, Gene content of 20 Glycine plastomes. Different colors represent the copy number of genes present in each genome

Fig. 3

Codon preference of 20 Glycine mitogenomes. A, The total count of each amino acid residue in all mitochondrial proteins is shown on the y-axis. B, The relative percentage of each amino acid residue in all mitochondrial proteins is shown on the y-axis. C, Relative synonymous codon usage (RSCU) in 20 Glycine mitogenomes (Glycine max in red frame, Glycine soja in yellow frame, perennial Glycine species in blue frame)

Fig. 4

Distribution of inserts by size and type of Glycine organelle sequences transferred to the nucleus. A, Total number and total length of NUMTs (left two panels) and NUPTs (right two panels) are demonstrated by accession. B, Number and length of NUMTs are demonstrated by accession, with panels separated by percent similarity to origin. C, Number and length of NUPTs are demonstrated by accession, with panels separated by percent similarity to origin

Fig. 5

Gene transfer events in Glycine mitogenomes. A, Overview of NUMGs among 20 Glycine accessions. B, Proportion of genes that are fully, partially, and not integrated into nuclear genome for each gene. C, Heatmap of genes that are fully, partially, and not integrated into nuclear genome in PCGs, tRNAs, and rRNAs across 20 Glycine accessions. In (A) and (B), dark blue, light blue, and gray represent fully, partially, and not integrated into nuclear genome, respectively. In (C), the scale represents the log-transformed number of genes with fully, partially, and not integrated into nuclear genome

Fig. 6

Phylogenetic relationships of 20 Glycine accessions based on organelle genomes. A, Maximum likelihood phylogenetic tree based on PCGs of mitogenomes. B, Maximum likelihood phylogenetic tree based on PCGs of plastomes