Cost of Having the Largest Mitochondrial Genome: Evolutionary Mechanism of Plant Mitochondrial Genome

Abstract

The angiosperm mitochondrial genome is the largest and least gene-dense among the eukaryotes, because its intergenic regions are expanded. There seems to be no functional constraint on the size of the intergenic regions; angiosperms maintain the large mitochondrial genome size by a currently unknown mechanism. After a brief description of the angiosperm mitochondrial genome, this review focuses on our current knowledge of the mechanisms that control the maintenance and alteration of the genome. In both processes, the control of homologous recombination is crucial in terms of site and frequency. The copy numbers of various types of mitochondrial DNA molecules may also be controlled, especially during transmission of the mitochondrial genome from one generation to the next. An important characteristic of angiosperm mitochondria is that they contain polypeptides that are translated from open reading frames created as byproducts of genome alteration and that are generally nonfunctional. Such polypeptides have potential to evolve into functional ones responsible for mitochondrially encoded traits such as cytoplasmic male sterility or may be remnants of the former functional polypeptides.

Plant Mitochondrial Genome Evolution and Cytoplasmic Male Sterility

“…By contrast, vertebrate animal mitogenomes are rather small (»14-20 kb) and highly conserved in both size and structure (Boore, 1999;Lavrov et al, 2016), and plant mitochondrial genomes exhibit substantial variation in both these features (Kitazaki and Kubo, 2010;Galtier, 2011;Mower et al, 2012b), although exceptions exist in nonflowering plants Guo et al, 2016). Plant mitochondrial genomes may vary enormously in size even within single plant families; in the Cucurbitaceae, for example, mitochondrial genomes vary over 7-fold in size, from 379 kb in Citrullus lanatus to 2,740 kb in Cucumis melo (Rodriguez-Moreno et al, 2011).…”

“…Flowering plant mitogenomes exemplify the former, with substantial variation in genome size and structure even among close relatives (Francis and Fernand, 1977;Alverson et al, 2010;Tang et al, 2015;Chen et al, 2017). They have highly variable intergenetic regions containing diverse repeated sequences (Kitazaki and Kubo, 2010), frequent structural rearrangements (Galtier, 2011), massive genes loss, frequent endogenous and foreign DNA transfer (Bergthorsson et al, 2003;Kubo and Newton, 2008;Hao and Palmer, 2009;Bock, 2010;Liu et al, 2011), and a highly variable RNA editing process (Takenaka et al, 2008). Conversely, plant mitochondrial genes display exceptionally low rates of nucleotide substitution (Wolfe et al, 1987;Palmer et al, 2000;Mower et al, 2007;Galtier, 2011).…”

“…In addition to variability in size, the structure of mitogenomes is remarkably variable (Mower et al, 2012b). While mitogenomes typically are depicted as single circular rings (Kitazaki and Kubo, 2010), many other configurations for plant mitochondrial chromosomes have been reported (Figure 1), including diverse linear and circular forms, highly branched and sigma-like morphologies, as well as multichromosomal structures that are capable of substoichiometric co-occurrence. The mitochondrial genomes of some CMS lines in maize (Allen et al, 2007) and rice, for example, have linear configurations (Notsu et al, 2002).…”

“…The accumulated evidence, therefore, is that plant mitochondrial genomes frequently have a multipartite organization (Kitazaki and Kubo, 2010) associated with complex recombination among repeated sequences (Oldenburg and Bendich, 1996;Backert and Borner, 2000). In general, mitogenomes are arranged in a main ring (i.e., a "master chromosome") that contains a complete set of genes and a number of sub-rings (Alverson et al, 2011a, b).…”

“…From the >60 sequenced mitogenomes (Mower et al, 2012b;Gualberto et al, 2014;Liu et al, 2014), it is clear that plant mitogenomes vary widely in repeat content and composition, which, in conjunction with the phylogenetically widespread occurrence of large mitogenomes, lend support to the idea that multiple divergent repeated sequences are acquired independently during evolution (Andre et al, 1992). Consequently, as the presence of repeated sequences is associated with recombination in the mitogenome (Manchekar et al, 2006;Kitazaki and Kubo, 2010;Chen et al, 2017), the high structural variability (Ogihara et al, 2005), complexity, and multipartite organization of plant mtDNA (Abdelnoor et al, 2003) should come as little surprise.…”