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.
Highlights
Our depth of understanding organism genomes has progressed with the advancement of sequencing technology
We propose a “Mitochondrial Fostering” theory where the plant mitochondrial genome may play an integral role in the arrival and development of de novo orphan genes
To explain the possible impact of the mitochondrial genome on orphan gene evolution, we propose a model with two routes whereby orphan open reading frames may be either: (1) generated in the mitochondrial genome and transferred to the nuclear genome as a Numt or (2) mitochondrial DNA is transferred to the nuclear genome and further diversification generates novel open reading frames (Figure 6)
Summary
Our depth of understanding organism genomes has progressed with the advancement of sequencing technology. Around 5–15% of an organism’s genes are estimated to be orphans (Arendsee et al, 2014). The function of orphan genes can range from negligible to necessary; mutants of some orphan genes in Drosophila cause lethality (Reinhardt et al, 2013). In A. thaliana, Qua Quine Starch (QQS) – the species-specific orphan gene and its network have been shown to be involved in regulation of carbon and nitrogen allocation (Li et al, 2009, 2015; Li and Wurtele, 2015; Jones et al, 2016; O’Conner et al, 2018), and several orphans have been implicated in stress response
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