Absence of Complex I Is Associated with Diminished Respiratory Chain Function in European Mistletoe

Abstract

Parasitism is a life history strategy found across all domains of life whereby nutrition is obtained from a host. It is often associated with reductive evolution of the genome, including loss of genes from the organellar genomes [1, 2]. In some unicellular parasites, the mitochondrial genome (mitogenome) has been lost entirely, with far-reaching consequences for the physiology of the organism [3, 4]. Recently, mitogenome sequences of several species of the hemiparasitic plant mistletoe (Viscum sp.) have been reported [5, 6], revealing a striking loss of genes not seen in any other multicellular eukaryotes. In particular, the nad genes encoding subunits of respiratory complex I are all absent and other protein-coding genes are also lost or highly diverged in sequence, raising the question what remains of the respiratory complexes and mitochondrial functions. Here we show that oxidative phosphorylation (OXPHOS) in European mistletoe, Viscum album, is highly diminished. Complex I activity and protein subunits of complex I could not be detected. The levels of complex IV and ATP synthase were at least 5-fold lower than in the non-parasitic model plant Arabidopsis thaliana, whereas alternative dehydrogenases and oxidases were higher in abundance. Carbon flux analysis indicates that cytosolic reactions including glycolysis are greater contributors to ATP synthesis than the mitochondrial tricarboxylic acid (TCA) cycle. Our results describe the extreme adjustments in mitochondrial functions of the first reported multicellular eukaryote without complex I.

The PPR-related splicing cofactor MSP1/EMB1025 protein, encoded by At4g20090, encode an essential protein that is required for the splicing ofnad1intron 1 and for the biogenesis of complex I in Arabidopsis mitochondria

“…Previously, it has been noted that complex I defects in plants can result in a broad spectrum of phenotypes, ranging 20 from mild growth to severe developmental defects and arrested embryogenesis (Dahan, et al 2014, Kuhn, et al 2015, Ostersetzer-Biran 2016. In some rear cases plants may adapted to live in the absence of complex I, as the parasitic mistletoe (Viscum album) plant (Maclean et al 2018, Petersen et al 2015, Senkler et al 2018.…”

Topologies of N6‐adenosine methylation (m6A) in land plant mitochondria and their putative effects on organellar gene expression

“…These include genes encoding tRNAs, rRNAs, ribosomal proteins, various subunits of the respiratory complexes I (NADH dehydrogenase), III (cytochrome c reductase or bc1), and IV (cytochrome c oxidase), subunits of the ATP‐synthase (also denoted as CV), cytochrome c biogenesis (CCM) factors, and at least one component of the twin‐arginine protein translocation complex (for a recent review see Bonen, ). Recent studies indicate that the mistletoe mitochondrial genome had undergone massive gene losses including all CI subunits (Petersen et al , ; Maclean et al , ; Senkler et al , ).…”

Assessing mitochondrial function in angiosperms with highly divergent mitochondrial genomes

“…Accelerated evolutionary rates in Viscum are associated with the loss of many mt genes and a large reduction in genome size (Skippington et al ., 2015, 2017). Importantly, CI mt genes have been entirely lost in Viscum (i.e., not transferred to the nuclear genome), which explains why CI activity has been lost and activities of the AOX and alternative NADH dehydrogenases are elevated (Maclean et al ., 2018). In addition, the formation of OXPHOS “supercomplexes” and mt morphology are altered in Viscum, also likely due to loss of CI (Senkler et al ., 2018).…”

“…Recent evidence suggests that unusual angiosperm mt genomes can be associated with altered mt function. For example, the parasitic plant Viscum exhibits highly accelerated evolutionary rates, altered structure, and gene loss in its mt genome (Skippington et al ., 2015, 2017) and was recently shown to: 1) have lost CI, 2) rely heavily on AOX and alternative NADH dehydrogenases, 3) have reduced abundances of all OXPHOS complexes, and 4) have an altered ETS configuration (Maclean et al ., 2018; Senkler et al ., 2018).…”