Plant Ecology: Getting the metabolites right

A study of almost 800 Arabidopsis thaliana plants from across Europe reveals how the environment and evolutionary pressures shape their metabolites.
  1. Arthur Korte  Is a corresponding author
  1. Center for Computational and Theoretical Biology, University of Würzburg, Germany

All living organisms look different. Even within a species, individuals can show differences in their shape, size and coloring. This is true both for outward appearances and for physiological traits, such as the concentration of various metabolites. These variations are determined by the underlying genetics of the organism and by the environment it lives in. This results in phenotypic differences that affect the entire organism, allowing it to rapidly respond to changes in its environment. A well-known example of this is the change in color and pattern of butterfly wings under different temperatures, which is regulated by specific hormones (Bhardwaj et al., 2020).

The relationship between genotype and phenotype has been of interest since Mendel postulated the existence of 'internal factors' that are passed on to the next generation (Mendel, 1865), and Bateson originated the term 'genetics' (Bateson, 1909). This link is of major interest in fields ranging from evolutionary biology to molecular biology, and also medicine or agriculture, where untangling genetic effects on phenotypes from environmental effects can lead to beneficial interventions.

The mechanisms by which genetic differences translate into phenotypic differences involve many intermediate steps (Figure 1A); this so-called ‘in-between-ome’ consists of the transcriptome, the proteome and the metabolome. The integration of data from these different levels is necessary to understand how complex phenotypes evolve, and how they are regulated (Subramanian et al., 2020). In plants, the metabolome – all of the small molecules required for an organism to live – is particularly important for adaptation. This is because plants, being immobile, rely on the substances they can absorb from their environment and the derivatives they can produce. However, it is unclear how the variety of metabolites found in plants from different environments arose during evolution. Now, in eLife, Daniel J Kliebenstein, from the University of California Davis, along with colleagues from Austria, the United States and Germany – including Ella Katz as first author – report the factors that drive phenotypic differences in the chemical composition of a specific type of metabolites found in the plant Arabidopsis thaliana (Katz et al., 2021).

The complex interplay between genotype, phenotype and the environment.

(A) The environment of an organism influences its phenotype through natural selection, and its genome, which adapts to distinct environments. The mechanisms by which genetic differences translate into phenotypic variation are mediated by the ‘in-between-ome’. This consists of the transcriptome and the proteome, which are indirectly affected by the environment (shown in grey), and the metabolome, which is directly influenced by the environment (shown in black). (B) Map of Europe showing dots in different colors representing lines of A. thaliana with different glucosinolate profiles (GSL), also known as chemotypes. These chemotypes change depending on the environment, with plants from similar environments exhibiting similar chemotypes.

Katz et al. measured the levels of specialized metabolites called glucosinolates in nearly 800 lines of A. thaliana from different ecosystems in Europe. Glucosinolates are biologically active compounds that protect plants from pests and diseases. They are usually found in the Brassicaceae family (Rask et al., 2000), which includes plants like broccoli, cauliflower or mustard, and provide these plants with their characteristic taste. Additionally, plants use glucosinolates to counteract both biotic stress, caused by other living organisms such as herbivores that try to eat the plants, and abiotic stress, such as drought stress (Del Carmen Martínez-Ballesta et al., 2013). The fact that glucosinolates can protect plants from predators, pests and other stressors make it likely that the mechanisms that regulate the abundance of these compounds in individual plants are under strong selection and evolutionary constraints.

The analysis performed by Katz et al. revealed that plants from different regions in Europe had glucosinolates with different chemical compositions or ‘chemotypes’. The spatial distribution of the different chemotypes throughout Europe exhibits distinctive patterns, both at a local and a global scale (Figure 1B). But how did this trait variation evolve? What is its genetic basis and what phenotypic consequences does it have?

To answer these questions, Katz et al. used a technique called genome-wide association mapping (GWAS), which scans the genome of each plant for genetic markers that may be associated with the different chemotypes detected. This analysis found only two major sites in the genome that are responsible for variation in glucosinolate content. However, these previously known loci cannot explain all the variation observed, suggesting that additional loci must also be involved. Additionally, Katz et al. discovered previously unknown alleles at these sites and showed that different combinations of these alleles could lead to similar chemotypes in similar environments.

Based on these observations, Katz et al. suggest that these different combinations of alleles emerged through a mixture of evolutionary events. Some arose through parallel evolution, which occurs when mutations in the same gene lead to similar traits. Others are the result of convergent evolution, where independent mutations in different genes give rise to similar features. Apart from the genetic factors, Katz et al. also show how environmental parameters like climate and geography directly affect the chemotype of A. thaliana in different regions. Specifically, they found that specific environmental conditions were associated with certain chemotypes across different geographic locations.

Katz et al. show that many factors, both environmental and genetic, shape the chemotype of glucosinolates in A. thaliana. The findings highlight the complexity of the interplay between genetics and the environment, and how both contribute to the evolution of traits in natural populations. They also underline how complex traits appear in a population that is adapted to distinct environments. Additionally, this work demonstrates the need to correctly design studies that aim to explain and dissect complex traits, given that results can be confounded by individuals from the same species being adapted to distinct environmental conditions. Future work will show whether the findings of Katz et al. findings hold for other traits, and if they shed light on general principles of trait evolution.


    1. Mendel G
    Experiments in plant hybridization
    Proceedings of the Natural History Society of Brünn.

Article and author information

Author details

  1. Arthur Korte

    Arthur Korte is in the Center for Computational and Theoretical Biology, University of Würzburg, Würzburg, Germany

    For correspondence
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0831-1463

Publication history

  1. Version of Record published: June 15, 2021 (version 1)


© 2021, Korte

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.


  • 1,066
    Page views
  • 73
  • 0

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Arthur Korte
Plant Ecology: Getting the metabolites right
eLife 10:e70149.

Further reading

    1. Ecology
    2. Evolutionary Biology
    Nicholas Grebe, Jean Paul Hirwa ... Stacy Rosenbaum
    Research Article

    Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development, and/or only with same-sex individuals. Besides humans, one notable exception are mountain gorillas, in which non-sex biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hours of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin, but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with high reproductive skew (i.e., high relatedness certainty), even though low reproductive skew (i.e., low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.

    1. Ecology
    Ines Braga Goncalves, Andrew N Radford
    Research Article

    Conflicts with conspecific outsiders are common in group-living species, from ants to primates, and are argued to be an important selective force in social evolution. However, whilst an extensive empirical literature exists on the behaviour exhibited during and immediately after interactions with rivals, only very few observational studies have considered the cumulative fitness consequences of outgroup conflict. Using a cooperatively breeding fish, the daffodil cichlid (Neolamprologus pulcher), we conducted the first experimental test of the effects of chronic outgroup conflict on reproductive investment and output. ‘Intruded’ groups received long-term simulated territorial intrusions by neighbours that generated consistent group-defence behaviour; matched ‘Control’ groups (each the same size and with the same neighbours as an Intruded group) received no intrusions in the same period. Intruded groups had longer inter-clutch intervals and produced eggs with increasingly less protein than Control groups. Despite the lower egg investment, Intruded groups provided more parental care and achieved similar hatching success to Control groups. Ultimately, however, Intruded groups had fewer and smaller surviving offspring than Control groups at 1-month post-hatching. We therefore provide experimental evidence that outgroup conflict can decrease fitness via cumulative effects on reproductive success, confirming the selective potential of this empirically neglected aspect of sociality.