Dynamic changes in the plastid and mitochondrial genomes of the angiosperm Corydalis pauciovulata (Papaveraceae)

Abstract

Background: Corydalis DC., the largest genus in the family Papaveraceae, comprises > 465 species. Complete plastid genomes (plastomes) of Corydalis show evolutionary changes, including syntenic arrangements, gene losses and duplications, and IR boundary shifts. However, little is known about the evolution of the mitochondrial genome (mitogenome) in Corydalis. Both the organelle genomes and transcriptomes are needed to better understand the relationships between the patterns of evolution in mitochondrial and plastid genomes.

Results: We obtained complete plastid and mitochondrial genomes from Corydalis pauciovulata using a hybrid assembly of Illumina and Oxford Nanopore Technologies reads to assess the evolutionary parallels between the organelle genomes. The mitogenome and plastome of C. pauciovulata had sizes of 675,483 bp and 185,814 bp, respectively. Three ancestral gene clusters were missing from the mitogenome, and expanded IR (46,060 bp) and miniaturized SSC (202 bp) regions were identified in the plastome. The mitogenome and plastome of C. pauciovulata contained 41 and 67 protein-coding genes, respectively; the loss of genes was a plastid-specific event. We also generated a draft genome and transcriptome for C. pauciovulata. A combination of genomic and transcriptomic data supported the functional replacement of acetyl-CoA carboxylase subunit β (accD) by intracellular transfer to the nucleus in C. pauciovulata. In contrast, our analyses suggested a concurrent loss of the NADH-plastoquinone oxidoreductase (ndh) complex in both the nuclear and plastid genomes. Finally, we performed genomic and transcriptomic analyses to characterize DNA replication, recombination, and repair (DNA-RRR) genes in C. pauciovulata as well as the transcriptomes of Liriodendron tulipifera and Nelumbo nuicifera. We obtained 25 DNA-RRR genes and identified their structure in C. pauciovulata. Pairwise comparisons of nonsynonymous (d_N) and synonymous (d_S) substitution rates revealed that several DNA-RRR genes in C. pauciovulata have higher d_N and d_S values than those in N. nuicifera.

Conclusions: The C. pauciovulata genomic data generated here provide a valuable resource for understanding the evolution of Corydalis organelle genomes. The first mitogenome of Papaveraceae provides an example that can be explored by other researchers sequencing the mitogenomes of related plants. Our results also provide fundamental information about DNA-RRR genes in Corydalis and their related rate variation, which elucidates the relationships between DNA-RRR genes and organelle genome stability.

Keywords: Concomitant loss; DNA-RRR; Genome rearrangement; NDH complex; Organelle genomes.

Fig. 1

The Corydalis pauciovulata plastome. Thick lines on the genome map indicate the inverted repeats (IRa and IRb: 46,060 bp), which separate the genome into small (SSC: 202 bp) and large (LSC: 92,155) single-copy regions. Genes on the inside and outside of the map are transcribed in clockwise and counterclockwise directions, respectively. Asterisks indicate genes transferred from single-copy regions to the IR, and ψ denotes a pseudogene. The red lines on the inner circle indicate tandem repeats. The black and red arrows on the outside of the map indicate contraction and expansion events, respectively. The colored boxes on the map correspond to the locally collinear blocks inferred by Mauve (see Fig. 3). The green lines within the inner circle indicate the positions of the pairs of repeats, with crossed connecting lines denoting reverse repeats

Fig. 2

The Corydalis pauciovulata mitogenome. Genes on the inside and outside of the map are transcribed in clockwise and counterclockwise directions, respectively. The red lines on the inner circle indicate tandem repeats, and ψ denotes a pseudogene. The blue lines within the inner circle indicate the positions of the pairs of repeats, with crossed connecting lines denoting reverse repeats

Fig. 3

Structural alignments of the organelle genome arrangements in Corydalis pauciovulata. Blocks drawn below the horizontal line indicate sequences found in an inverted orientation. A The colored blocks represent collinear sequence blocks shared by all plastomes. Individual genes and strandedness are represented below the Liriodendron genome block. Only one copy of the inverted repeat (IR) is shown for each plastome, and the pink box below each plastome block indicates its IR. B The colored blocks represent collinear sequence blocks shared by all mitogenomes. The red boxes indicate the conserved gene clusters

Fig. 4

Mitogenome rearrangements in Corydalis pauciovulata. Alternative genomic conformations based on five repeat pairs (R1, R2, R4, R5, and R6). MC: master circle corresponding to the mitogenome in Fig. 2

Fig. 5

Schematic diagram of the organelle gene transfer to the nucleus and the NDH-PSI supercomplex. The colored blocks represent collinear sequence blocks shared by all plastomes. Blocks drawn below the horizontal line indicate sequences found in an inverted orientation. Individual genes and strandedness are represented below the Euptelea genome block. Only one copy of the inverted repeat (IR) is shown for each plastome, and the pink box below each plastome block indicates its IR

Fig. 6

Structure of 25 DNA replication, recombination, and repair system genes in Corydalis pauciovulata. Exons and introns are represented by boxes and lines, respectively

Fig. 7

Boxplots of d_N and d_S values for plastid and mitochondrial genes in Corydalis pauciovulata and Nelumbo nucifera. The box represents values between quartiles, the solid lines extend to the minimum and maximum values, and the horizontal lines in the boxes show the median values. The numbers below the boxes represent the mean values

Fig. 8

Sequence divergence of 25 DNA replication, recombination, and repair system genes. A Nonsynonymous (d_N) and synonymous (d_S) divergence values for 25 individual genes are plotted for C. pauciovulata and N. nucifera. Dual-targeted, plastid-targeted, and mitochondrial-targeted genes are indicated in red, green, and blue, respectively. The DNA-RRR genes are grouped into nine categories by gray parallelograms. B Boxplots of d_N and d_S values for the target groups. The box represents values between quartiles, the solid lines extend to the minimum and maximum values, and the horizontal lines in the boxes show the median values. The numbers below the boxes represent the mean values. The colors corresponding to the target groups (red, dual-targeted; green, plastid-targeted; and blue, mitochondrial-targeted genes)