Plants display extensive intraspecific variation in secondary metabolites. However, the selective forces shaping this diversity remain often unknown, especially below ground. Using Taraxacum officinale and its major native insect root herbivore Melolontha melolontha, we tested whether below-ground herbivores drive intraspecific variation in root secondary metabolites. We found that high M. melolontha infestation levels over recent decades are associated with high concentrations of major root latex secondary metabolites across 21 central European T. officinale field populations. By cultivating offspring of these populations, we show that both heritable variation and phenotypic plasticity contribute to the observed differences. Furthermore, we demonstrate that the production of the sesquiterpene lactone taraxinic acid b-D-glucopyranosyl ester (TA-G) is costly in the absence, but beneficial in the presence of M. melolontha, resulting in divergent selection of TA-G. Our results highlight the role of soil-dwelling insects for the evolution of plant defences in nature. BackgroundHeritable intraspecific variation is a common feature of many biological traits. Genetic variation results from heterogeneous selection pressures in relation to genetic architecture, population substructures and gene flow [1 -4]. In plants, local differences in both abiotic and biotic factors may drive trait evolution [5]. Insect herbivores, the most abundant and diverse plant consumers, have long been suspected to play an important role in this context [6]. Recent studies demonstrate that herbivore abundance can covary with the expression of plant defence metabolites [7], that the exclusion of phytophagous insects can lead to a relaxation of defences within a few generations [8] and that defence genes are under differential selection across environments [9,10]. Together, these studies show that the temporal and spatial variation in above-ground herbivore communities can shape plant defensive chemistry.In contrast with the ecological and evolutionary dynamics of above-ground plant-herbivore interactions, below-ground interactions have received little attention, despite the importance of roots for plant fitness and the high concentrations of secondary metabolites in below-ground organs [11][12][13][14]. The rhizosphere differs from the phyllosphere in both biotic and abiotic conditions [15], and the selective forces shaping variation in secondary metabolites may therefore differ between the two environments. The evolution of root secondary metabolites may for instance be driven by herbivores [11,12,16], pathogens [17] and symbionts [18], as well as nutrient availability [19], salt, drought and cold stress [20]. By comparing one mainland and two island populations, Watts et al. [21] showed that geographical isolation, including the escape from pocket gophers (Geomyidae), resulted in the evolutionary decline of root alkaloid concentrations of the host plant Eschscholzia californica (Papaveraceae). The specific potential of root herbivores to shap...

Summary Herbivore communities are shaped by indirect plant‐mediated interactions whose outcomes are strongly dependent on the sequence of herbivore arrival. However, the mechanisms underlying sequence specificity are poorly understood.We examined the mechanisms that govern sequence‐specific effects of the interaction between two specialist maize herbivores, the leaf feeder Spodoptera frugiperda and the root feeder Diabrotica virgifera virgifera. In the field, S. frugiperda reduces D. v. virgifera abundance, but only when it arrives on the plant first.In behavioral experiments, D. v. virgifera larvae continued feeding on plants that they had infested before leaf infestation, but refused to initiate feeding on plants that were infested by S. frugiperda before their arrival. Changes in root‐emitted volatiles were sufficient to elicit this sequence‐specific behavior. Root volatile and headspace mixing experiments showed that early‐arriving D. v. virgifera larvae suppressed S. frugiperda‐induced volatile repellents, which led to the maintenance of host attractiveness to D. v. virgifera.Our study provides a physiological and behavioral mechanism for sequence specificity in plant‐mediated interactions and suggests that physiological canalization of behaviorally active metabolites can drive sequence specificity and result in strongly diverging herbivore distribution patterns.

Foraging behavior of root feeding organisms strongly affects plant-environment-interactions and ecosystem processes. However, the impact of plant chemistry on root herbivore movement in the soil is poorly understood. Here, we apply a simple technique to trace the movement of soil-dwelling insects in their habitats without disturbing or restricting their interactions with host plants. We tagged the root feeding larvae of Melolontha melolontha with a copper ring and repeatedly located their position in relation to their preferred host plant, Taraxacum officinale, using a commercial metal detector. This method was validated and used to study the influence of the sesquiterpene lactone taraxinic acid β-D-glucopyranosyl ester (TA-G) on the foraging of M. melolontha. TA-G is stored in the latex of T. officinale and protects the roots from herbivory. Using behavioral arenas with TA-G deficient and control plants, we tested the impact of physical root access and plant distance on the effect of TA-G on M. melolontha. The larvae preferred TA-G deficient plants to control plants, but only when physical root contact was possible and the plants were separated by 5 cm. Melolontha melolontha showed no preference for TA-G deficient plants when the plants were grown 15 cm apart, which may indicate a trade-off between the cost of movement and the benefit of consuming less toxic food. We demonstrate that M. melolontha integrates host plant quality and distance into its foraging patterns and suggest that plant chemistry affects root herbivore behavior in a plant-density dependent manner.

Plants produce a tremendous variety of structurally diverse organic compounds, so-called secondary or specialized metabolites. These metabolites defend plants against herbivores and pathogens

Summary Marchantia polymorpha has recently become a prime model for cellular, evo‐devo, synthetic biological, and evolutionary investigations. We present a pseudomolecule‐scale assembly of the M. polymorpha genome, making comparative genome structure analysis and classical genetic mapping approaches feasible. We anchored 88% of the M. polymorpha draft genome to a high‐density linkage map resulting in eight pseudomolecules. We found that the overall genome structure of M. polymorpha is in some respects different from that of the model moss Physcomitrella patens. Specifically, genome collinearity between the two bryophyte genomes and vascular plants is limited, suggesting extensive rearrangements since divergence. Furthermore, recombination rates are greatest in the middle of the chromosome arms in M. polymorpha like in most vascular plant genomes, which is in contrast with P. patens where recombination rates are evenly distributed along the chromosomes. Nevertheless, some other properties of the genome are shared with P. patens. As in P. patens, DNA methylation in M. polymorpha is spread evenly along the chromosomes, which is in stark contrast with the angiosperm model Arabidopsis thaliana, where DNA methylation is strongly enriched at the centromeres. Nevertheless, DNA methylation and recombination rate are anticorrelated in all three species. Finally, M. polymorpha and P. patens centromeres are of similar structure and marked by high abundance of retroelements unlike in vascular plants. Taken together, the highly contiguous genome assembly we present opens unexplored avenues for M. polymorpha research by linking the physical and genetic maps, making novel genomic and genetic analyses, including map‐based cloning, feasible.