Massive gene loss in mistletoe (Viscum, Viscaceae) mitochondria

Abstract

Parasitism is a successful survival strategy across all kingdoms and has evolved repeatedly in angiosperms. Parasitic plants obtain nutrients from other plants and some are agricultural pests. Obligate parasites, which cannot complete their lifecycle without a host, may lack functional photosystems (holoparasites), or have retained photosynthesis (hemiparasites). Plastid genomes are often reduced in parasites, but complete mitochondrial genomes have not been sequenced and their mitochondrial respiratory capacities are largely unknown. The hemiparasitic European mistletoe (Viscum album), known from folklore and postulated therapeutic properties, is a pest in plantations and forestry. We compare the mitochondrial genomes of three Viscum species based on the complete mitochondrial genome of V. album, the first from a parasitic plant. We show that mitochondrial genes encoding proteins of all respiratory complexes are lacking or pseudogenized raising several questions relevant to all parasitic plants: Are any mitochondrial gene functions essential? Do any genes need to be located in the mitochondrial genome or can they all be transferred to the nucleus? Can parasitic plants survive without oxidative phosphorylation by using alternative respiratory pathways? More generally, our study is a step towards understanding how host- and self-perception, host integration and nucleic acid transfer has modified ancestral mitochondrial genomes.

Figure 1. Viscum minimum parasitizing succulent Euphorbia.

(a) The Viscum seedling to the left has established contact with the host through a haustorium. Endophytic growth of the parasite is visible to the right just beneath the host, Euphorbia horrida, epidermis; (b) Mature, green shoots of Viscum minimum on Euphorbia mammillaris. (Photo: Gitte Petersen).

Figure 2. Overview of gene content in the mitochondrial genome of Viscum and 29 other seed plants.

Dark grey fields indicate presence of the gene. Light grey fields indicate pseudogenes or gene fragments. The rrn18 genes are scored as functional with doubt. See Extended Data Table 1 for details of the genes (including tRNAs) found in Viscum.

Figure 3. Phylogenetic tree based on sequence data from 10 mitochondrial genes.

The position of Viscum is in agreement with models of angiosperm phylogeny, but the long branch indicates that the Viscum gene sequences are extremely divergent compared to other plants. See Extended Data Figs 1–4 for individual gene trees. Scale bar, substitutions per site.