Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

Abstract

In parasitic plants, the reduction in plastid genome (plastome) size and content is driven predominantly by the loss of photosynthetic genes. The first completed mitochondrial genomes (mitogenomes) from parasitic mistletoes also exhibit significant degradation, but the generality of this observation for other parasitic plants is unclear. We sequenced the complete mitogenome and plastome of the hemiparasite Castilleja paramensis (Orobanchaceae) and compared them with additional holoparasitic, hemiparasitic and nonparasitic species from Orobanchaceae. Comparative mitogenomic analysis revealed minimal gene loss among the seven Orobanchaceae species, indicating the retention of typical mitochondrial function among Orobanchaceae species. Phylogenetic analysis demonstrated that the mobile cox1 intron was acquired vertically from a nonparasitic ancestor, arguing against a role for Orobanchaceae parasites in the horizontal acquisition or distribution of this intron. The C. paramensis plastome has retained nearly all genes except for the recent pseudogenization of four subunits of the NAD(P)H dehydrogenase complex, indicating a very early stage of plastome degradation. These results lend support to the notion that loss of ndh gene function is the first step of plastome degradation in the transition to a parasitic lifestyle.

Mitochondrial genome of non-photosynthetic mycoheterotrophic plant Hypopitys monotropa,its structure, gene expression and RNA editing

“…The gene content of the H. monotropa mitogenome is typical of flowering plants, with most genes encoding components of electron transfer chain and translation apparatus. Unlike parasitic plants, which show a certain degree of reduction, from limited to high (Fan et al, 2016; Skippington et al, 2015), the gene content in H. monotropa is not reduced. Surprisingly it is even larger than in V. macrocarpon , a close photosynthetic relative: nad4L and atp6 are pseudogenized and sdh3 and rps3 are absent in V. macrocarpon .…”

“…In many angiosperm lineages, the cox1 gene contains a group I intron, acquired by horizontal transfer events ((Cho et al, 1998; Sanchez-Puerta et al, 2011) but see (Cusimano et al, 2008). The cox1 intron is highly overrepresented in the parasitic plants that have been examined to date, though the hypothesis that parasitism may serve as a mediator of horizontal intron transfer is not supported by phylogenetic analysis (Fan et al, 2016). V. macrocarpon lacks an intron in cox1 , while in H. monotropa it is present.…”

“…Mitochondrial genome is in this case a “refugium” of plastid genes. The Castilleja paramensis mitogenome contains 55 full-length or nearly full-length plastid genes and only about half of them are obvious pseudogenes (Fan et al, 2016). By now the only example of functionality of mitochondrial genes transferred from plastids are tRNA genes of plastid origin recruited in the protein synthesis in mitochondria (Joyce and Gray, 1989).…”

“…By now only few complete mitochondrial genomes of non-photosynthetic plants are characterized, and all but one of them are parasitic. A comparative analysis of mitogenomes of several parasitic, hemiparasitic and autotrophic Orobanchaceae (Fan et al, 2016) showed that the gene content does not depend on trophic specialization in family range. Mitogenomes of two non-related lineages of parasitic plants: Rafflesiaceae and Cynomoriaceae also do not show reduction in gene content; besides that, they are the example of massive HGT from other plants (including, but not only, their hosts).…”

Assessing mitochondrial function in angiosperms with highly divergent mitochondrial genomes

“…We speculate that this may be due to the parasitic vs. free-living lifestyles of Viscum v S. Silene . Although not all parasitic plants have reduced mt gene content (Fan et al ., 2016), they do tend to show elevated rates of mt genomic evolution compared to free-living relatives (Bromham et al ., 2013), possibly reflecting increased mutation rates or relaxed selection.…”