Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

Abstract

Despite the enormous diversity among parasitic angiosperms in form and structure, life-history strategies, and plastid genomes, little is known about the diversity of their mitogenomes. We report the sequence of the wonderfully bizarre mitogenome of the hemiparasitic aerial mistletoe Viscum scurruloideum. This genome is only 66 kb in size, making it the smallest known angiosperm mitogenome by a factor of more than three and the smallest land plant mitogenome. Accompanying this size reduction is exceptional reduction of gene content. Much of this reduction arises from the unexpected loss of respiratory complex I (NADH dehydrogenase), universally present in all 300+ other angiosperms examined, where it is encoded by nine mitochondrial and many nuclear nad genes. Loss of complex I in a multicellular organism is unprecedented. We explore the potential relationship between this loss in Viscum and its parasitic lifestyle. Despite its small size, the Viscum mitogenome is unusually rich in recombinationally active repeats, possessing unparalleled levels of predicted sublimons resulting from recombination across short repeats. Many mitochondrial gene products exhibit extraordinary levels of divergence in Viscum, indicative of highly relaxed if not positive selection. In addition, all Viscum mitochondrial protein genes have experienced a dramatic acceleration in synonymous substitution rates, consistent with the hypothesis of genomic streamlining in response to a high mutation rate but completely opposite to the pattern seen for the high-rate but enormous mitogenomes of Silene. In sum, the Viscum mitogenome possesses a unique constellation of extremely unusual features, a subset of which may be related to its parasitic lifestyle.

Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

“…A second apparent concentration of horizontally acquired sequences in plant genomes is associated with parasitic plants, where both mitochondrial (14,(17)(18)(19)(20)(21)(22)(23) and nuclear horizontal transfers (24)(25)(26)(27)(28)(29) have been identified. Repeated horizontal acquisitions of mitochondrial atpI by parasitic flowering plants occurred in four extreme parasite lineages where the parasite lives inside the host for much of its lifespan (14).…”

The Roles of Mutation, Selection, and Expression in Determining Relative Rates of Evolution in Mitochondrial versus Nuclear Genomes

“…We focused on three genes (sdh3, sdh4, and cox2) to specifically investigate the effects of intracellular gene transfer on expression. The sdh3 and sdh4 genes are encoded by the mt genome in Vitis and Nicotiana, and the nuclear genome in Arabidopsis, Silene, and Vigna (Alverson et al 2011;Skippington et al 2015). Mt genomes have not been sequenced from Humulus and Lupinus, so we investigated whether these genes are likely mt-or nuclear-encoded in these species.…”

“…Nearly all angiosperm mt genomes contain a core gene set comprising 18 OXPHOS genes (including all 13 of the mtencoded proteins found in most bilaterian animals), four genes involved in cytochrome C biogenesis, and two genes (matR and mttB) that may play a role in intron splicing and membrane transport, respectively (cf. Skippington et al 2015). …”

Plant Mitochondrial Genome Evolution and Cytoplasmic Male Sterility

“…These include protein-encoding, rRNA, and tRNA genes, in addition to pseudogenes and ORFs of unknown function, the latter having been implicated in CMS (Satoh et al, 2004;Luo et al, 2013). Conservation and loss of these genes in different plant groups have been extensively studied (Rice et al, 2013;Skippington et al, 2015;Skippington et al, 2017). Plant mitochondrial protein-encoding genes are commonly divided into five categories (participating in five complexes or subunits associated with mitochondrial respiratory metabolism; Figure 2 [ Lei et al, 2013]), which typically are conserved among plants, albeit to varying degrees.…”

“…Plant mitochondrial protein-encoding genes are commonly divided into five categories (participating in five complexes or subunits associated with mitochondrial respiratory metabolism; Figure 2 [ Lei et al, 2013]), which typically are conserved among plants, albeit to varying degrees. Genes classified in complex II, for example, have been lost in most higher plants, particularly in monocots, whereas complexes I, III, IV, and V show much greater conservation across land plant species with occasionally loss of nad genes (Viscum scurruloideum) and cox2 (legumes) Fujii et al, 2007;Bentolila and Stefanov, 2012;Rice et al, 2013;Skippington et al, 2015;Skippington et al, 2017). Conversely, both the ribosomal subunit and tRNA-encoding genes have experienced a more dynamic pattern of evolution (Figure 2), often displaying progressive loss, and collectively representing the majority of cases of genic variation among plant mitogenomes (Clifton et al, 2004;Lei et al, 2013).…”