Mitochondrial Fostering: The Mitochondrial Genome May Play a Role in Plant Orphan Gene Evolution

Abstract

Plant mitochondrial genomes exhibit unique evolutionary patterns. They have a high rearrangement but low mutation rate, and a large size. Based on massive mitochondrial DNA transfers to the nucleus as well as the mitochondrial unique evolutionary traits, we propose a "Mitochondrial Fostering" theory where the organelle genome plays an integral role in the arrival and development of orphan genes (genes with no homologs in other lineages). Two approaches were used to test this theory: (1) bioinformatic analysis of nuclear mitochondrial DNA (Numts: mitochondrial originating DNA that migrated to the nucleus) at the genome level, and (2) bioinformatic analysis of particular orphan sequences present in both the mitochondrial genome and the nuclear genome of Arabidopsis thaliana. One study example is given about one orphan sequence that codes for two unique orphan genes: one in the mitochondrial genome and another one in the nuclear genome. DNA alignments show regions of this A. thaliana orphan sequence exist scattered throughout other land plant mitochondrial genomes. This is consistent with the high recombination rates of mitochondrial genomes in land plants. This may also enable the creation of novel coding sequences within the orphan loci, which can then be transferred to the nuclear genome and become exposed to new evolutionary pressures. Our study also reveals a high correlation between the amount of mitochondrial DNA transferred to the nuclear genome and the number of orphan genes in land plants. All the data suggests the mitochondrial genome may play a role in nuclear orphan gene evolution in land plants.

Keywords: evolution; mitochondrial genome; numt; orphan gene; plant.

FIGURE 1

Orphan gene content in three well characterized land plants. Three plant genomes show higher orphan gene content in mitochondrial genome compared to whole genome and chloroplast genome.

FIGURE 2

Predicted subcellular localization for A. thaliana orphan genes. (A) Subcellular localization prediction from TAIR for all A. thaliana 1,169 orphan genes. (B) Cellular component GO term analysis of A. thaliana orphan genes (including 852 orphan genes that have predictions). (C) Target peptide analysis of 100 protein sequences generated from A. thaliana intergenic and Numt sequences. Numt DNA is more likely to produce a mitochondrial targeting peptide than intergenic DNA (Chi-squared analysis, X-squared = 29.088, df = 1, P = 6.918e-08). (D) Target peptide analysis on A. thaliana Numt DNA and completely randomized DNA shows similar proclivities for mitochondrial targeting peptides (Chi-squared analysis, X-squared = 0.5002, df = 1, P = 0.4794). (E) The percentage of orphan genes with a putative mitochondrial targeting peptide shows a positive correlation with the percentage of orphan genes in the genome. The correlation coefficient for mitochondria, chloroplast and secreted targeting peptides is 0.488, –0.184, and –0.358 with P of 0.004, 0.305, and 0.041, respectively, n = 33.

FIGURE 3

Positive correlation between Numts and orphan genes. (A) A significantly positive correlation between Numt turnover % (total Numt length/mitochondrial genome size) and orphan gene percentage (Correlation coefficient = 0.91; P = 0.01). (B) No significant correlation is found between % of TEs in the genome and orphan gene percentage (Correlation coefficient = 0.56; P = 0.25). Species used in this analysis: A. thaliana, G. max, Z. mays, O. sativa, S. bicolor, and V. vinifera. TE data was retrieved from Oliver et al. (2013). Orphan gene data for O. sativa, Z. mays and S. bicolor was obtained from Yao et al. (2017); A. thaliana was obtained from Arendsee et al. (2014); G. max, and V. vinifera were obtained from http://www.greenphyl.org/cgi-bin/index.cgi (version 4).

FIGURE 4

Orphan gene content in six aquatic mammals. (A) Whole genome sizes of the six mammalian species and the six plant species (data from NCBI). (B) Orphan gene content (as a percentage of total genes) for aquatic mammals and land plants. (C) The correlation of orphan gene content as percentage of total genes and Numt turnover %. Correlation coefficient = –0.48; P = 0.31. The amount of orphan genes in mammal species is not significantly correlated with their Numt content.

FIGURE 5

KNIT sequence origin and location. (A) Model of KNIT loci in both chromosome 2 and the mitochondrial genome. The gene model indicates that the full genomic sequence of KNIT exists in both chromosome 2 near the centromere and in the mitochondrial genome of A. thaliana, but the predicted protein sequences differ. (B) The gap sequence that separates genic sequences is not present in A. thaliana. G, gap sequence; S1, first segment of KNIT gene; S2, second segment of KNIT gene.

FIGURE 6

A model for orphan gene evolution through the mitochondrial genome. Novel sequences are created due to the high rearrangement rate in the mitochondrial genome, and then inserted into a nuclear chromosome. The transferred DNA may already contain gene coding information like KNIT (left side of model: Route 1) or may obtain an open reading frame via other genome mechanisms such as transposon transposition (right side: Route 2).