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.
Abstract1. Plant neighbours can strongly influence the interactions between herbivores and focal plants, for instance by providing food of different quality (consumptive effects) or by changing the behaviour and metabolism of the herbivore and the focal plant without being consumed (non-consumptive effects). Determining the species-specific contributions of consumptive and non-consumptive effects is important to understand the ecophysiological mechanisms which underlie neighbourhood effects. 4. Diet-mixing experiments showed that P. pratensis increased M. melolontha growth when offered together with T. officinale, while C. stoebe suppressed it. When feeding was restricted to artificial diet, larval growth was not changed by the presence of P. pratensis or C. stoebe. However, when feeding was restricted to T. officinale, larval growth was increased by both heterospecific neighbours. Biomass and primary metabolism of T. officinale under attack by M. melolontha was also altered by the presence of C. stoebe and P. pratensis. Together, these results show that consumptive and non-consumptive effects can explain the positive effect of P. pratensis. In contrast, the negative effect of C. stoebe is likely driven exclusively by intoxication. 5.Synthesis. The performed experiments suggest that different combinations of consumptive and non-consumptive effects are likely to contribute to the diversity of neighbourhood effects in nature. Furthermore, they show that neighbourhood effects are important factors in below-ground plant-insect interactions. K E Y W O R D Sassociational effect, diet mixing, Melolontha melolontha, neighbouring plant, physiological response, plant-herbivore interactions, plant-plant interactions, root insects, species-specificity, Taraxacum officinalePaper previously published as Standard Paper
Understanding the molecular basis of morphological shifts is a fundamental question of evolutionary biology. New morphologies may arise through the birth/death of genes (gene gain/loss) or by reutilizing existing gene sets. Yet, the relative contribution of these two processes to radical morphological shifts is still poorly understood. Here, we use the model system of two mosses, Funaria hygrometrica and Physcomitrium (Physcomitrella) patens, to investigate the molecular mechanisms underlying contrasting sporophyte architectures. We used comparative analysis of time-series expression data for four stages of sporophyte development in both species to address this question in detail. We found that large-scale differences in sporophytic architecture are mainly governed by orthologous (i.e., shared) genes frequently experiencing temporal gene expression shifts between the two species. While the absolute number of species-specific genes expressed during sporophyte development is somewhat smaller, we observed a significant increase of their proportion in preferentially sporophyte expressed genes, suggesting a fundamental role in the sporophyte phase. However, further functional studies are necessary to determine their contribution to diverging sporophyte morphologies. Our results add to the growing set of studies suggesting that radical changes in morphology may rely on the heterochronic expression of conserved regulators.
Plants experience seasonal fluctuations in abiotic and biotic factors such as herbivore attack rates. If and how root defense expression co-varies with seasonal fluctuations in abiotic factors and root herbivore attack rates is not well understood. Here, we evaluated seasonal changes in defensive root latex chemistry of Taraxacum officinale plants in the field and correlated the changes with seasonal fluctuations in abiotic factors and damage potential by Melolontha melolontha, a major natural enemy of T. officinale. We then explored the causality and consequences of these relationships under controlled conditions. The concentration of the defensive sesquiterpene lactone taraxinic acid β-D glucopyranosyl ester (TA-G) varied substantially over the year and was most strongly correlated to mean monthly temperature. Both temperature and TAG levels were correlated with annual fluctuations in potential M. melolontha damage. Under controlled conditions, plants grown under high temperature produced more TAG and were less attractive for M. melolontha. However, temperature-dependent M. melolontha feeding preferences were not significantly altered in TAG deficient transgenic lines. Our results suggest that fluctuations in temperature leads to variation in the production of a root defensive metabolites that co-varies with expected attack of a major root herbivore. Temperature-dependent herbivore preference, however, is likely to be modulated by other phenotypic alterations.
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