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.

Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

“…As in the Orobanchaceae parasites described here, the Cynomoriaceae and Rafflesiaceae holoparasites contain a nearly complete set of the expected mitochondrial genes, although a substantial fraction were reported to have been acquired horizontally1337. By contrast, in the hemiparasitic V. scurruloideum , the mitogenome has been greatly reduced in size, and in all four mistletoes the coding content has undergone extreme reduction, including the pseudogenization or loss of all nine nad genes encoding subunits of mitochondrial complex I, a NADH dehydrogenase1617. The coordinated loss of functional copies of all nine nad genes, which has not been reported for any other multicellular eukaryote, argues against a nuclear transfer scenario and instead suggests that the entire complex I was lost16, with nuclear-encoded alternative dehydrogenases38 compensating for the loss of complex I activity.…”

“…In addition to the Orobanchaceae data reported here, large-scale mitogenomic data from a parasitic plant is available from four hemiparasitic mistletoes1617, four holoparasitic members of Rafflesiaceae1537, and a holoparasite in Cynomoriaceae13. As in the Orobanchaceae parasites described here, the Cynomoriaceae and Rafflesiaceae holoparasites contain a nearly complete set of the expected mitochondrial genes, although a substantial fraction were reported to have been acquired horizontally1337.…”

“…In fact, only a single genus of parasitic plants has a completely sequenced mitogenome, from the hemiparasitic mistletoes Viscum scurruloideum and Viscum album , along with draft genomes from two additional Viscum species1617. Compared with other land plants, V. scurruloideum has the smallest mitogenome (66 kb) and all four Viscum sequences have lost functional copies of all nine nad genes encoding subunits of the mitochondrial NADH dehydrogenase complex I, the first reported loss of this complex from any multicellular eukaryote16.…”

Loss of aTrans-Splicingnad1Intron from Geraniaceae and Transfer of the Maturase GenematRto the Nucleus inPelargonium

“…In addition, embedded within the final nad1 intron [named nad1i728 based on Dombrovska and Qiu (2004) intron notation] of nearly all angiosperms is another gene ( matR ) that encodes a putative intron splicing factor termed a maturase, although recent survey sequencing has identified a few plant lineages in which matR is no longer in this position. In Viscum album , matR was established as a freestanding gene due to loss of the host gene nad1 (Petersen et al 2015). The matR gene is also freestanding in several species of Geranium , presumably by translocation prior to the loss of the host intron (Park et al 2015).…”

“…In the gnetophyte Welwitschia mirabilis , matR is no longer adjacent to any nad1 exons, but it is flanked by segments of the nad1i728 intron and may still be associated with the intron through a double trans -splicing event (Guo et al 2016). In some other species of Viscum (Petersen et al 2015; Skippington et al 2015) and two species within Malpighiales (Wurdack and Davis 2009), the matR gene appears to be missing completely from the mitochondrial genome. Using the extensive genomic and transcriptomic data available for many species within Geraniaceae (Weng et al 2014; Park et al 2015; Zhang et al 2015; Blazier et al 2016), we assessed the status of matR and nad1 in this family and present an evolutionary scenario to explain the unusual structural and functional diversity among species.…”