Implications of mistletoe parasitism for the host metabolome: A new plant identity in the forest canopy

Abstract

Mistletoe–host systems exemplify an intimate and chronic relationship where mistletoes represent protracted stress for hosts, causing long‐lasting impact. Although host changes in morphological and reproductive traits due to parasitism are well known, shifts in their physiological system, altering metabolite concentrations, are less known due to the difficulty of quantification. Here, we use ecometabolomic techniques in the plant–plant interaction, comparing the complete metabolome of the leaves from mistletoe (Viscum album) and needles from their host (Pinus nigra), both parasitized and unparasitized, to elucidate host responses to plant parasitism. Our results show that mistletoe acquires metabolites basically from the primary metabolism of its host and synthesizes its own defence compounds. In response to mistletoe parasitism, pines modify a quarter of their metabolome over the year, making the pine canopy metabolome more homogeneous by reducing the seasonal shifts in top‐down stratification. Overall, host pines increase antioxidant metabolites, suggesting oxidative stress, and also increase part of the metabolites required by mistletoe, which act as a permanent sink of host resources. In conclusion, by exerting biotic stress and thereby causing permanent systemic change, mistletoe parasitism generates a new host‐plant metabolic identity available in forest canopy, which could have notable ecological consequences in the forest ecosystem.

Seasonal variations of triterpene acid contents in Viscum album L. on typical host trees of Hyrcanian forests

“…Carbohydrate accumulation as a precursor primary metabolite for TTAs biosynthesis may cause an increase in mistletoe TTAs content in spring and summer. In correspondence with our assumption, Lázaro-González et al 41 demonstrated that Viscum album subsp. austriacum obtains metabolites mostly through the primary metabolism of the host tree and produces its defensive chemicals.…”

“…Besides, in agreement with our findings, they reported a higher concentration of a few amino acids, carbohydrates, and defense compounds of V. album subsp. austriacum in the summer 41 .…”

Mitigating the Mistletoe Menace: Biotechnological and Smart Management Approaches

“…Moreover, mistletoe can interfere with flowering and fruiting and make the hosts more vulnerable to insect and fungal damage [ 128 , 129 ]. They also compete with host chemical profiles to remain healthy [ 130 , 131 ]. Lázaro-González and coworkers showed that Viscum album may load-dependently reduce the nitrogen concentrations in its pine hosts and may effectuate defense signals resembling drought, burning, and defoliation [ 130 ].…”

Consuming and consumed: Biotic interactions of African mistletoes across different trophic levels

“…Studies in the northern temperate regions have empirically demonstrated mistletoes promoting the diversities of endophytic fungi (Peršoh, 2013; Peršoh et al, 2010), arthropods (Lázaro‐González et al, 2017, 2020; Zamora et al, 2020), and frugivorous birds (Mellado & Zamora, 2016) in the host‐tree canopies. In addition to the direct mistletoes' input to biodiversity, modifications in the host plant metabolome in response to permanent mistletoe parasitism impose selective pressure on associated communities (Lázaro‐González et al, 2021), triggering cascading responses in ecosystems. Mistletoes can therefore exert an ambivalent effect on host plants by facilitating their reproduction through the attraction and permanent support of shared generalist pollinators and vectors (Těšitel et al, 2021), but at the same time reducing the physiological fitness of the hosts by depletion of their water and nutrient supplies and increasing susceptibility to pathogens and herbivores (Griebel et al, 2017).…”