Coevolution between Nuclear-Encoded DNA Replication, Recombination, and Repair Genes and Plastid Genome Complexity

Abstract

Disruption of DNA replication, recombination, and repair (DNA-RRR) systems has been hypothesized to cause highly elevated nucleotide substitution rates and genome rearrangements in the plastids of angiosperms, but this theory remains untested. To investigate nuclear-plastid genome (plastome) coevolution in Geraniaceae, four different measures of plastome complexity (rearrangements, repeats, nucleotide insertions/deletions, and substitution rates) were evaluated along with substitution rates of 12 nuclear-encoded, plastid-targeted DNA-RRR genes from 27 Geraniales species. Significant correlations were detected for nonsynonymous (dN) but not synonymous (dS) substitution rates for three DNA-RRR genes (uvrB/C, why1, and gyrA) supporting a role for these genes in accelerated plastid genome evolution in Geraniaceae. Furthermore, correlation between dN of uvrB/C and plastome complexity suggests the presence of nucleotide excision repair system in plastids. Significant correlations were also detected between plastome complexity and 13 of the 90 nuclear-encoded organelle-targeted genes investigated. Comparisons revealed significant acceleration of dN in plastid-targeted genes of Geraniales relative to Brassicales suggesting this correlation may be an artifact of elevated rates in this gene set in Geraniaceae. Correlation between dN of plastid-targeted DNA-RRR genes and plastome complexity supports the hypothesis that the aberrant patterns in angiosperm plastome evolution could be caused by dysfunction in DNA-RRR systems.

Keywords: nuclear–plastid genome coevolution; nucleotide insertions/deletions; plastid genome rearrangement; substitution rates.

Fig. 1.—

Evolutionary rates of DNA-RRR, nuclear control, and plastid-encoded genes. (A) Nonsynonymous (dN) and (B) synonymous (dS) substitution rates of different gene groups are shown. NUCP, nuclear encoded plastid targeted control genes; NUMT, nuclear encoded mitochondrial targeted control genes; NUOT, other nuclear encoded control genes; RRR, plastid-targeted DNA replication, recombination and repair genes; plastid, plastid-encoded genes. Boxes represent sorted rates ranging from 25% to 75%, dashed lines extend to maximal and minimal rates, red lines represent the median rate for each gene group.

Fig. 2.—

Pearson correlation coefficient between gene evolutionary rates and genome complexity. Correlations of (A) nonsynonymous (dN) and (B) synonymous (dS) substitution rates of genes and genome complexity are shown. NUCP, nuclear encoded plastid targeted control genes; NUMT, nuclear encoded mitochondrial targeted control genes; NUOT, other nuclear encoded control genes; RRR, plastid-targeted DNA replication, recombination and repair genes; LCBs-p, inversion distance estimated from local collinear blocks; Gene order, inversion distance estimated from gene order; SDR, small dispersal repeats; Tandem, repeats estimated from Tandem Repeat Finder (Benson 1999); CDR, indels in coding and rRNA regions; Intron, indels in intron regions; IG, indels in intergenic regions; dN CP, nonsynonymous substitution rates of the plastid genome; dS CP, synonymous substitution rates of the plastid genome.

Fig. 3.—

Significant correlation of evolutionary rates (dN) and genome complexity in different gene groups. Significant correlations were identified in NUCP, NUMT, and RRR but not NUOT genes. NUCP, nuclear encoded plastid targeted control genes; NUMT, nuclear encoded mitochondrial targeted control genes; NUOT, other nuclear encoded control genes; RRR, plastid-targeted DNA replication, recombination and repair genes.

Fig. 4.—

Comparison of dN of genes with and without significant correlation to genome complexity. dN of genes from (A) NUCP or (B) RRR gene groups were compared. NUCP, nuclear encoded plastid targeted control genes; RRR, plastid-targeted DNA replication, recombination and repair genes. Boxes represent sorted rates ranging from 25% to 75%, dashed lines extend to maximal and minimal rates, red lines represent the median rate for each gene group, and outliers are shown as “+.” Horizontal lines represent average rate of gene groups with correlation (green) or without correlation (cyan).

Fig. 5.—

Comparison of evolutionary rates between gene groups in Geraniales and Brassicales. Ger, gene groups are from Geraniales; Bra, gene groups are from Brassicales; NUCP, nuclear encoded plastid targeted control genes; NUMT, nuclear encoded mitochondrial targeted control genes; NUOT, other nuclear encoded control genes; RRR, plastid-targeted DNA replication, recombination and repair genes; plastid, plastid-encoded genes. Boxes represent sorted rates ranging from 25% to 75%, dashed lines extend to maximal and minimal rates, red lines represent the median rate of each gene group. *P < 0.05 and **P < 0.001.