PhD Fellow, University of Copenhagen
Introduction: Parasitic plants rely on their host to cover their nutritional requirements either for their entire life or a smaller part of it. Correlated with the level of parasitism, a reduction in the plastome has been found. However, knowledge on gene loss and evolution of the mitogenome of parasitic plants is only available for four hemiparasitic Viscum species (Viscaceae), which lack most of the mitochondrial genes, while the remaining exhibit increased evolutionary rates. In this study, we include another genus, Phoradendron, from the Viscaceae, and 10 other parasitic plants from other clades across the angiosperm phylogeny to investigate how fast molecular evolution works on the mitogenomes, and the extent of gene loss.
Methods: Total DNA from 11 parasitic plants was extracted and sequenced on the Illumina HiSeq platform. The mitochondrial gene sequences for each taxon were recovered and aligned. Phylogenetic trees were constructed using sets of the mitochondrial genes and up to 418 taxa of autotrophic and parasitic plants. The molecular evolution rates of all genes were analysed and tested for statistical significance between hemiparasitic, holoparasitic, and autrotrophic plants.
Results: The Viscaceae are alone in missing many mitochondrial genes, while those remaining evolve significantly faster than in any other taxa in this study. The evolutionary rates of the remaining hemiparasitic and holoparasitic plants do not differ significantly from the included autotrophic plants. The Balanophoraceae and Cynomoriaceae are strongly supported as members of Santalales.
Discussion: We confirm the uniqueness of previous observations in Viscaceae and show that the remaining parasitic plants do not have significantly higher substitution rates than autotrophic plants. We provide strong evidence for the inclusion of Balanophoraceae and Cynomoriaceae in Santalales. Thus, parasitism has evolved only 11 times in the angiosperms.
Abstract: Cynomoriaceae, one of the last unplaced families of flowering plants, comprises one or two species or subspecies of root parasites that occur from the Mediterranean to the Gobi Desert. Using Illumina sequencing, we assembled the mitochondrial and plastid genomes as well as some nuclear genes of a Cynomorium specimen from Italy. Selected genes were also obtained by Sanger sequencing from individuals collected in China and Iran, resulting in matrices of 33 mitochondrial, 6 nuclear, and 14 plastid genes and rDNAs enlarged to include a representative angiosperm taxon sampling based on data available in GenBank. We also compiled a new geographic map to discern possible discontinuities in the parasites' occurrence. Cynomorium has large genomes of 13.70-13.61 (Italy) to 13.95-13.76 pg (China). Its mitochondrial genome consists of up to 49 circular subgenomes and has an overall gene content similar to that of photosynthetic angiosperms, while its plastome retains only 27 of the normally 116 genes. Nuclear plastid and mitochondrial phylogenies place Cynomoriaceae in Saxifragales, and we found evidence for several horizontal gene transfers from different hosts, as well as intracellular gene transfers.
Pub.: 01 Jul '16, Pinned: 09 Jun '17
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.
Pub.: 24 Jun '15, Pinned: 09 Jun '17
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.
Pub.: 03 Dec '15, Pinned: 09 Jun '17