Untargeted metabolic profiling reveals geography as the strongest predictor of metabolic phenotypes of a cosmopolitan weed

Abstract

Plants produce a multitude of metabolites that contribute to their fitness and survival and play a role in local adaptation to environmental conditions. The effects of environmental variation are particularly well studied within the genus Plantago; however, previous studies have largely focused on targeting specific metabolites. Studies exploring metabolome‐wide changes are lacking, and the effects of natural environmental variation and herbivory on the metabolomes of plants growing in situ remain unknown. An untargeted metabolomic approach using ultra‐high‐performance liquid chromatography–mass spectrometry, coupled with variation partitioning, general linear mixed modeling, and network analysis was used to detect differences in metabolic phenotypes of Plantago major in fifteen natural populations across Denmark. Geographic region, distance, habitat type, phenological stage, soil parameters, light levels, and leaf area were investigated for their relative contributions to explaining differences in foliar metabolomes. Herbivory effects were further investigated by comparing metabolomes from damaged and undamaged leaves from each plant. Geographic region explained the greatest number of significant metabolic differences. Soil pH had the second largest effect, followed by habitat and leaf area, while phenological stage had no effect. No evidence of the induction of metabolic features was found between leaves damaged by herbivores compared to undamaged leaves on the same plant. Differences in metabolic phenotypes explained by geographic factors are attributed to genotypic variation and/or unmeasured environmental factors that differ at the regional level in Denmark. A small number of specialized features in the metabolome may be involved in facilitating the success of a widespread species such as Plantago major into such wide range of environmental conditions, although overall resilience in the metabolome was found in response to environmental parameters tested. Untargeted metabolomic approaches have great potential to improve our understanding of how specialized plant metabolites respond to environmental change and assist in adaptation to local conditions.

Valuable Fatty Acids in Bryophytes—Production, Biosynthesis, Analysis and Applications

“…Screening of biomarkers by untargeted lipid analysis using liquid chromatography-mass spectrometry (LC-MS), allows for the separation and identification of possible lipophilic compounds and derivatives in biological samples. It is a powerful tool to evaluate the phylogenetic diversity among different species [45] and examine the change of related lipid species due to environmental variability [46]. The lipid extract can also be injected directly to electrospray ionization triple quadrupole mass spectrometry (ESI-MS/MS), which has a great advantage on analyzing the formation of PLs in plants [46].…”

Travel tales of a worldwide weed: genomic signatures reveal colonial trade routes and prior adaptation are key to the success of Plantago major

“…Asexual plants have been found to change just as often and as fast as do sexual plants when introduced to a new range (Dalrymple et al, 2015). The extraordinary phenotypic plasticity known in P. major is likely important for ecotypes coping with a high level of environmental and climate heterogeneity (Warwick & Briggs, 1980;Samuelsen, 2000).Plantago major can vary extensively in morphology even within populations, and therefore high phenotypic variation for the species is not related to genetic diversity at least within a population level, though further studies are needed (Mølgaard, 1976;Lotz and Blom, 1986;Wolff, 1991;Iwanycki Ahlstrand et al, 2018). Wide environmental tolerance and an ability to grow in a multitude of climatic and edaphic conditions as a result of well-developed phenotypic plasticity, makesPlantago major a classic example of a weed that possesses the "general purpose genotype strategy" as coined by Baker (1965) -in this case, it appears that as few as three general-purpose genotypes or ecotypes may have been involved in the global success of the common plantain.…”

“…Plantago major has been extensively studied in its native range and a wealth of ecological, physiological and genetic information is available for the species (Mølgaard, 1976;Kuiper & Bos, 1992;Morgan-Richards & Wolff, 1999). It possesses many of the traits that are common amongst the most successful introduced plants (Pysek et al, 2009;Hejda et al, 2014;Pysek et al, 2015), including high phenotypic plasticity, large ecological amplitudes, a high tolerance to human disturbance, rapid growth rates, and the production of propagules with specialized adaptations for long-distance dispersal such as mucilaginous seeds and wind pollination (Young & Evans, 1973;Hawthorn, 1974;van Dijk, 1984;Rahn, 1996;Samuelsen, 2000;Kreitschitz, Kovalev, & Gorb, 2016;Iwanycki Ahlstrand et al, 2018;Iwanycki Ahlstrand et al, 2019). Furthermore, the species is capable of self-fertilizing, meaning that a single propagule can putatively establish sexually reproducing populations in new ranges (Baker, 1974;Wolff, 1991).…”

Variations of Secondary Metabolites among Natural Populations of Sub-Antarctic Ranunculus Species Suggest Functional Redundancy and Versatility

“…Larger-scale variation such as among regions or latitudes was also investigated, sometimes with the aim to enrich biochemical resources. Thus, studies also show variability in plant metabolite composition across latitudinal gradients or regions [23,24]. Yet, environments may be more different among populations or regions as within, and differences in metabolite composition among populations or regions might hence be dependent or independent of environments.…”

“…Yet, environments may be more different among populations or regions as within, and differences in metabolite composition among populations or regions might hence be dependent or independent of environments. However, relatively few studies have examined differences in metabolite composition among populations or regions, trying to dissociate metabolite variations that are dependent on environments and such that are independent [23,24,25,26,27]. This latter part of variation in metabolite composition that would be independent of environmental factors would likely reflect either selection by unknown past environments or neutral microevolutionary differentiation among populations or regions [13,14] and remains largely to be described [9,28].…”