The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Abstract

Across eukaryotes, mitochondria exhibit staggering diversity in genomic architecture, including the repeated evolution of multichromosomal structures. Unlike in the nucleus, where mitosis and meiosis ensure faithful transmission of chromosomes, the mechanisms of inheritance in fragmented mitochondrial genomes remain mysterious. Multichromosomal mitochondrial genomes have recently been found in multiple species of flowering plants, including Silene noctiflora, which harbors an unusually large and complex mitochondrial genome with more than 50 circular-mapping chromosomes totaling ∼7 Mb in size. To determine the extent to which such genomes are stably maintained, we analyzed intraspecific variation in the mitochondrial genome of S. noctiflora. Complete genomes from two populations revealed a high degree of similarity in the sequence, structure, and relative abundance of mitochondrial chromosomes. For example, there are no inversions between the genomes, and there are only nine SNPs in 25 kb of protein-coding sequence. Remarkably, however, these genomes differ in the presence or absence of 19 entire chromosomes, all of which lack any identifiable genes or contain only duplicate gene copies. Thus, these mitochondrial genomes retain a full gene complement but carry a highly variable set of chromosomes that are filled with presumably dispensable sequence. In S. noctiflora, conventional mechanisms of mitochondrial sequence divergence are being outstripped by an apparently nonadaptive process of whole-chromosome gain/loss, highlighting the inherent challenge in maintaining a fragmented genome. We discuss the implications of these findings in relation to the question of why mitochondria, more so than plastids and bacterial endosymbionts, are prone to the repeated evolution of multichromosomal genomes. meiosis | mitochondrial DNA | mitosis | multichromosomal | multipartite

Unparalleled replacement of native mitochondrial genes by foreign homologs in a holoparasitic plant

“…Likewise, 20 of the 59 chromosomes in Silene noctiflora, 86 of the 128 chromosomes in S. conica (Sloan et al, 2012), and the two smaller chromosomes of cucumber (Alverson et al, 2011) bear no intact genes. The existence of possibly noncoding chromosomes raises questions about their origin and perpetuation, for which both neutral and adaptive explanations have been advanced, but the questions remain unanswered (Alverson et al, 2011;Sloan et al, 2012;Rice et al, 2013;Wu et al, 2015). Adaptive hypotheses for the existence of noncoding chromosomes suggest the presence of unidentified genes or regulatory regions that are functionally relevant and are maintained by natural selection.…”

“…Adaptive hypotheses for the existence of noncoding chromosomes suggest the presence of unidentified genes or regulatory regions that are functionally relevant and are maintained by natural selection. Alternatively, gene-lacking chromosomes may replicate and be perpetuated by genetic drift (or even selfishly) as a result of an insignificant fitness cost on the organism (Sloan et al, 2012;Wu et al, 2015). A population study of S. noctiflora revealed some differences in the presence/absence of chromosomes that lack any identifiable genes (Wu et al, 2015).…”

“…Alternatively, gene-lacking chromosomes may replicate and be perpetuated by genetic drift (or even selfishly) as a result of an insignificant fitness cost on the organism (Sloan et al, 2012;Wu et al, 2015). A population study of S. noctiflora revealed some differences in the presence/absence of chromosomes that lack any identifiable genes (Wu et al, 2015). These findings suggest that at least some chromosomes are evolving under genetic drift (suffering stochastic loss), while others (those carrying essential genes) may be subjected to natural selection (Wu et al, 2015).…”

Monogonont Rotifer, Brachionus calyciflorus, Possesses Exceptionally Large, Fragmented Mitogenome

“…Metazoan mtDNA is usually very compact: there are generally no introns, little or no intergenic DNA, and most genes show clear signatures of selection for small size [1,2]. Nevertheless, fragmentation of the “standard” single-circle mtDNA into multichromosomal genomes, which is common in higher plants [3,4], has occurred independently in some metazoans as well: nematodes [5], mesozoans [6], cnidaria [7], insects [8], and some monogonont rotifers [9,10]. …”

Symbiosis becoming permanent: Survival of the luckiest

“…The colloquium was a collaboration between the US National Academy of Sciences and the Canadian Institute for Advanced Research, and spanned a wide range of overlapping themes in symbiosis: major evolutionary transitions and the nature of individuality (10-13); the mosaic phylogenetic nature of organelle proteomes (14)(15)(16)(17); the risks and costs associated with long-term endosymbiosis (18,19); the structure and dynamics of symbiont and organelle genomes (20)(21)(22); the metabolic complexities that develop during the establishment and integration of endosymbionts (23-31); and how endosymbiosis has been understood in the history of biology and how it might be thought of in the future (32,33).…”