The European mistletoe (Viscum album) is a plant steeped in ancient associations with druids and Northern European folklore and since the 18th century, has been synonymous with kissing at Christmas time. This plant is a hemiparasite (a parasitic plant that is capable of some photosynthesis), latching onto trees and extracting water and nutrients from them. Now, two new studies, published in the journal Current Biology, show that mistletoe’s parasitic lifestyle has led the species to a rather surprising evolutionary loss.
The European mistletoe (Viscum album). Image credit: Etienne Meyer.
Two research teams — one of which was led by Dr. Etienne Meyer from the Max Planck Institute of Molecular Plant Physiology and the other by Dr. Hans-Peter Braun of the Leibniz Universität Hannover — discovered that the European mistletoe has evolved in a manner that makes it unique among multicellular organisms.
The plant lacks key components of the cellular machinery other organisms depend upon to convert glucose into the energy-carrying molecule ATP.
“A loss of respiratory capacity has previously been observed only in unicellular eukaryotes, leading to a parasitic or symbiotic life style. We are reporting the first case of a multicellular eukaryote that lost most of its respiratory capacity,” Dr. Meyer said.
“There was no known example that life without mitochondrial complex I is possible in multicellular eukaryotes. So, we were definitely surprised to realize that Viscum album lives without this complex,” Dr. Braun added.
Earlier studies suggested that the genomes within cellular powerhouses known as mitochondria of Viscum species had lost genes encoding complex I subunits. It was a first among multicellular eukaryotes. But it wasn’t proof that mistletoe lacked the complex altogether.
There was a possibility that the genes encoding complex I had been transferred from mitochondria into the nuclear genome.
Nevertheless, the findings drew the attention of the researchers. Without knowing about one another, they decided to take a closer look.
Dr. Braun and co-authors found biochemical evidence that the mitochondria of European mistletoe completely lack complex I. They also have greatly reduced amounts of complexes II and V.
At the same time, complexes III and IV form what they described as ‘remarkably stable respiratory supercomplexes.’
The team’s results offer biochemical proof that the genes encoding subunits of complex I have not been transferred to the nuclear genome and that this respiratory complex indeed is not assembled. As a consequence, the plant’s entire respiratory chain is remodeled.
Dr. Meyer and co-authors found that they could not detect any activity from complex I or its protein subunits.
They found that levels of complex IV and the enzyme that synthesizes ATP were present at 5-fold lower concentration than another commonly studied laboratory plant. Other essential metabolic enzymes were detected at higher levels.
The findings add to evidence that mitochondrial functions within parasitic mistletoe have undergone ‘extreme adjustments’ over evolutionary time.
“Over millions of years of evolution, mistletoe has remodeled the way it generates energy at the molecular level,” said Andrew Maclean, from the John Innes Centre and the University of East Anglia.
“We were following up earlier studies that had shown genes responsible for producing complex I were missing, but we thought they may have relocated to other parts of the genome.”
“We were stunned to discover that mistletoe has managed to dispense with this piece of metabolic machinery that was thought to be essential for all multicellular organisms. But maybe because mistletoe is a parasite and it gets lots of nutrition from its host then it doesn’t need a high capacity for respiration.”
“The discovery of mistletoe’s remarkable metabolism provides a unique window into the life cycle of a high-profile parasite in evolutionary time.”
“These adaptations to a parasitic lifestyle may save the plant the energy required to assemble these mitochondrial complexes. However, this comes at a price, as the capacity for ATP generation by mitochondria is reduced,” Dr. Braun said.
The two studies indicated loss of ATP generation by mitochondria might be compensated for by ATP-producing processes in other cellular components.
“That’s a possibility that deserves further investigation,” Dr. Braun said.
“The mitochondria of other parasitic plant species should be investigated to determine whether the reduction of respiratory capacity is specific to mistletoe,” Dr. Meyer added.
_____
Jennifer Senkler et al. Absence of Complex I Implicates Rearrangement of the Respiratory Chain in European Mistletoe. Current Biology, published online May 3, 2018; doi: 10.1016/j.cub.2018.03.050
Andrew E. Maclean et al. Absence of Complex I Is Associated with Diminished Respiratory Chain Function in European Mistletoe. Current Biology, published online May 3, 2018; doi: 10.1016/j.cub.2018.03.036
