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1. Legacy effects of plant influences on abiotic and biotic soil properties can result in priority effects that influence the structure and composition of plant communities. To better understand the role of these plant-soil interactions, here we expand the concept of plant-soil feedbacks from a within-species approach (intraspecific plant-soil feedback) to a between-species approach (interspecific plant-soil interactions). 2. In a greenhouse experiment, we tested how the early successional Jacobaea vulgaris affects its own performance and the performance of 30 co-occurring plant species via changes in abiotic and biotic soil conditions. In addition, we examined the reciprocal effect of the co-occurring species on J. vulgaris. 3. Our study had three important results. First, J. vulgaris exhibits strong negative plant-soil feedback. Secondly, there were large differences among the co-occurring species in interspecific plant-soil effects on J. vulgaris growth. Approximately, half the species reduced J. vulgaris performance, whereas the other half had no effect. Thirdly, soil conditioned by J. vulgaris had a positive or neutral effect on the growth of the co-occurring species. 4. To test the soil effects of entire plant communities, in 10 old-fields that differed in time since abandonment we recorded the identity of all plants surrounding J. vulgaris individuals. We calculated the weighted soil effect of this community on J. vulgaris and the reciprocal effect of J. vulgaris on the community. There was a positive linear relationship between time since abandonment and the weighted feedback effect of J. vulgaris on the plant community. 5. We suggest three mechanisms how the legacy of plant-soil interactions may enhance the rate of succession through priority effects: early successional plant species exert negative plant-soil feedback; co-occurring plant species cause negative interspecific plant-soil effects to the early successional species; and the early successional species have overall positive interspecific plant-soil effects on the co-occurring plant species. 6. Synthesis. The performance of an early successional species can be reduced directly by the legacy effects of intraspecific plant-soil feedback, as well as indirectly by the legacy effects of both intra- and interspecific plant-soil interactions. These intra- and interspecific plant-soil interactions can prioritize transitions of plant species in plant communities.

1. Feeding by insect herbivores can affect plant growth and the concentration of defense compounds in plant tissues. Since plants provide resources for soil organisms, herbivory can also influence the composition of the soil community via its effects on the plant. Soil organisms, in turn, are important for plant growth. We tested whether insect herbivores, via their effects on the soil microbial community, can influence plant-soil feedbacks. 2. We first examined the effects of above-ground (AG) and below-ground (B) insect herbivory on the composition of pyrrolizidine alkaloids (PAs) in roots and on soil fungi in roots and rhizosphere soil of ragwort (Jacobaea vulgaris). The composition of fungal communities in roots and rhizosphere soil was affected by both AG and BG herbivory, but fungal composition also differed considerably between roots and rhizosphere soil. The composition of PAs in roots was affected only by BG herbivory. 3. Thirteen different fungal species were detected in roots and rhizosphere soil. The presence of the potentially pathogenic fungus Fusarium oxysporum decreased and that of Phoma exigua increased in presence of BG herbivory, but only in soil samples. 4. We then grew new plants in the soils conditioned by plants exposed to the herbivore treatments and in unconditioned soil. A subset of the new plants was exposed to foliar insect herbivory. Plantsoil feedback was strongly negative, but the feedback effect was least negative in soil conditioned by plants that had been exposed to BG herbivory. There was a negative direct effect of foliar herbivory on plant biomass during the feedback phase, but this effect was far less strong when the soil was conditioned by plants exposed to AG herbivory. AG herbivory during the conditioning phase also caused a soil feedback effect on the PA concentration in the foliage of ragwort. 5. Synthesis. Our results illustrate how insect herbivory can affect interactions between plants and soil organisms, and via these effects how herbivory can alter the performance of late-growing plants. Plant-soil feedback is emerging as an important theme in ecology and these results highlight that plant-soil feedback should be considered from a multitrophic AG and BG perspective.

Arbuscular mycorrhizal fungal (AMF) colonisation of plant roots is one of the most ancient and widespread interactions in ecology, yet the systemic consequences for plant secondary chemistry remain unclear. We performed the first metabolomic investigation into the impact of AMF colonisation by Rhizophagus irregularis on the chemical defences, spanning above- and below-ground tissues, in its host-plant ragwort (Senecio jacobaea). We used a non-targeted metabolomics approach to profile, and where possible identify, compounds induced by AMF colonisation in both roots and shoots. Metabolomics analyses revealed that 33 compounds were significantly increased in the root tissue of AMF colonised plants, including seven blumenols, plant-derived compounds known to be associated with AMF colonisation. One of these was a novel structure conjugated with a malonyl-sugar and uronic acid moiety, hitherto an unreported combination. Such structural modifications of blumenols could be significant for their previously reported functional roles associated with the establishment and maintenance of AM colonisation. Pyrrolizidine alkaloids (PAs), key anti-herbivore defence compounds in ragwort, dominated the metabolomic profiles of root and shoot extracts. Analyses of the metabolomic profiles revealed an increase in four PAs in roots (but not shoots) of AMF colonised plants, with the potential to protect colonised plants from below-ground organisms.

1. Plant–soil feedback (PSF) effects on plant performance strongly depend on the plant species that conditioned the soil. Recent studies have shown that PSF can change above-ground plant–insect interactions via soil-mediated changes in plant quality, but whether these effects depend on species-specific soil conditioning is unknown. We examined how PSF effects of several plant species influence above-ground plant–aphid interactions. 2. We grew ragwort (Jacobaea vulgaris) in field soil conditioned specifically by 10 plant species, belonging to three functional groups (grasses, forbs and legumes), in a multispecies mixture of the conditioned soils and in control (unconditioned) field soil. We measured plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids) metabolites in phloem exudates, and performance of the generalist aphid Brachycaudus cardui and the specialist Aphis jacobaeae. 3. We observed that plant species, via species-specific effects on soil fungal communities, exerted unique plant–soil effects on J. vulgaris biomass, amino acid concentrations in phloem exudates and aphid performance. The direction and magnitude of the species-specific PSF effects on aphid performance differed between both aphid species. PSF effects on soil fungal communities, plant biomass and A. jacobaeae performance also differed between grasses, forbs and legumes, with soil conditioning by forbs resulting in lowest plant biomass and aphid performance. 4. Synthesis. Our study provides novel evidence that PSF effects on above-ground plant–insect interactions are highly species specific. Our results add a new dimension to the rapidly developing research fields of PSF and above-below-ground interactions, and highlights that these fields are tightly linked.

Western flower thrips (Frankliniella occidentalis) has become a key insect pest of agricultural and horticultural crops worldwide. Little is known about host plant resistance to thrips. In this study, we investigated thrips resistance in F ₂ hybrids of Senecio jacobaea and Senecio aquaticus. We identified thrips-resistant hybrids applying three different bioassays. Subsequently, we compared the metabolomic profiles of these hybrids applying nuclear magnetic resonance spectroscopy (NMR). The new developments of NMR facilitate a wide range coverage of the metabolome. This makes NMR especially suitable if there is no a priori knowledge of the compounds related to herbivore resistance and allows a holistic approach analyzing different chemical compounds simultaneously. We show that the metabolomes of thrips-resistant and -susceptible hybrids differed considerably. Thrips-resistant hybrids contained higher amounts of the pyrrolizidine alkaloids (PA), jacobine, and jaconine, especially in younger leaves. Also, a flavanoid, kaempferol glucoside, accumulated in the resistant plants. Both PAs and kaempferol are known for their inhibitory effect on herbivores. In resistant and susceptible F ₂ hybrids, young leaves showed less thrips damage than old leaves. Consistent with the optimal plant defense theory, young leaves contained increased levels of primary metabolites such as sucrose, raffinose, and stachyose, but also accumulated jacaranone as a secondary plant defense compound. Our results prove NMR as a promising tool to identify different metabolites involved in herbivore resistance. It constitutes a significant advance in the study of plant-insect relationships, providing key information on the implementation of herbivore resistance breeding strategies in plants.

Spatially explicit data on heterogeneously distributed plant populations are difficult to quantify using either traditional field-based methods or remote sensing techniques alone. Unmanned Aerial Vehicles (UAVs) offer new means and tools for baseline monitoring of such populations. We tested the use of vegetation classification of UAV-acquired photographs as a method to capture heterogeneously distributed plant populations, using Jacobaea vulgaris as a model species. Five sites, each containing 1–4 pastures with varying J. vulgaris abundance, were selected across Schleswig–Holstein, Germany. Surveys were conducted in July 2017 when J. vulgaris was at its flowering peak. We took aerial photographs at a 50 m altitude using three digital cameras (RGB, red-edge and near-infrared). Orthomosaics were created before a pixel-based supervised classification. Classification results were evaluated for accuracy; reliability was assessed with field data collected for ground verification. An ANOVA tested the relationship between field-based abundance estimations and the supervised classifications. Overall accuracy of the classification was very high (90.6%, ± 1.76 s.e.). Kappa coefficients indicated substantial agreement between field data and image classification (≥ 0.65). Field-based estimations were a good predictor of the supervised classifications (F = 7.91, df = 4, P = 0.007), resulting in similar rankings of J. vulgaris abundance. UAV-acquired images demonstrated the potential as an objective method for data collection and species monitoring. However, our method was more time consuming than field-based estimations due to challenges in image processing. Nonetheless, the increasing availability of low-cost consumer-grade UAVs is likely to increase the use of UAVs in plant ecological studies.

The diversity of secondary metabolites (SMs) has been poorly understood from both a mechanistic and a functional perspective. Hybridization is suggested to contribute to the evolution of diversity of SMs. In this paper we discuss the effects of hybridization on SMs and herbivore resistance by evaluating the literature and with special reference to our own research results from the hybrids between Jacobaea vulgaris (syn. Senecio jacobaea) and Jacobaea aquatica (syn. Senecio aquaticus). We also review the possible genetic mechanism which causes the variation of SMs and herbivore resistance in hybrids. Most SMs in hybrids are present in the parents as well. But hybrids may miss some parental SMs or have novel SMs. The concentration of parental SMs in hybrids generally is constrained by that in parental plants, but transgressive expression was present in some hybrids. Hybrids may be as susceptible (resistant) as the parents or more susceptible than the parents, but rarely more resistant than the parents. However, different hybrid classes (F1, F2, backcrossing and mixed genotypes) show different patterns in relation to herbivore resistance. The variation in SMs and herbivore resistance occurring in hybrids could be explained by complicated genetic mechanisms rather than a simple one-gene model. Most previous work in this field only reported mean trait values for hybrid classes and few studies focused on genotype differences within hybrid classes. Our study in Jacobaea hybrids showed transgressive segregation in most SMs and herbivore resistance. To summarize, our article shows that hybridization may increase the variation of SMs and affect herbivore resistance, which may partially explain the evolution of chemical diversity in plants.

Plant–soil feedback (PSF) effects on plant performance can be influenced by the availability of nutrients in the soil. Recent studies have shown that PSF effects can also change aboveground plant–insect interactions via soil-mediated changes in plant quality, but whether this is influenced by soil nutrient availability is unknown. We examined how fertilisation influences PSF effects on aboveground plant-aphid interactions in ragwort Jacobaea vulgaris. We grew J. vulgaris in soil conditioned by conspecific plants and in unconditioned soil at two levels of fertilisation and measured soil fungal communities, plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids; PAs) metabolites in phloem exudates, performance of the specialist aphid Aphis jacobaeae and sequestration of PAs by the aphid. We observed a strong interaction between soil conditioning and fertilisation on amino acid and PA concentrations in phloem exudates of J. vulgaris and on aphid performance, with opposite effects of soil conditioning at the two fertilisation levels. Plant biomass was reduced by soil conditioning and increased by fertilisation. Aphids contained high PA concentrations, converted N-oxides into tertiary amines and preferentially sequestered certain PA compounds, but PA sequestration was not affected by any of the treatments. We conclude that effects of PSF and fertilisation on plant chemistry and aphid performance are interdependent. Our study highlights the need to consider the importance of abiotic soil conditions on the outcome of PSF effects on aboveground plant–insect interactions.

Background Collectively, plants produce a huge variety of secondary metabolites (SMs) which are involved in the adaptation of plants to biotic and abiotic stresses. The most characteristic feature of SMs is their striking inter- and intraspecific chemical diversity. Cytochrome P450 monooxygenases (CYPs) often play an important role in the biosynthesis of SMs and thus in the evolution of chemical diversity. Here we studied the diversity and evolution of CYPs of two Jacobaea species which contain a characteristic group of SMs namely the pyrrolizidine alkaloids (PAs). Results We retrieved CYPs from RNA-seq data of J. vulgaris and J. aquatica , resulting in 221 and 157 full-length CYP genes, respectively. The analyses of conserved motifs confirmed that Jacobaea CYP proteins share conserved motifs including the heme-binding signature, the PERF motif, the K-helix and the I-helix. KEGG annotation revealed that the CYPs assigned as being SM metabolic pathway genes were all from the CYP71 clan but no CYPs were assigned as being involved in alkaloid pathways. Phylogenetic analyses of full-length CYPs were conducted for the six largest CYP families of Jacobaea (CYP71, CYP76, CYP706, CYP82, CYP93 and CYP72) and were compared with CYPs of two other members of the Asteraceae, Helianthus annuus and Lactuca sativa , and with Arabidopsis thaliana . The phylogenetic trees showed strong lineage specific diversification of CYPs, implying that the evolution of CYPs has been very fast even within the Asteraceae family. Only in the closely related species J. vulgaris and J. aquatica , CYPs were found often in pairs, confirming a close relationship in the evolutionary history. Conclusions This study discovered 378 full-length CYPs in Jacobaea species, which can be used for future exploration of their functions, including possible involvement in PA biosynthesis and PA diversity.

Background Senecio jacobaea contains pyrrolizidine alkaloids that can induce severe hepatic intoxication in horses, either acute when ingested in high amounts or chronic when consumed over a long period. The aim of this study was to determine horses’ rejection behaviour towards the presence of Senecio jacobaea in hay when fed ad libitum. We hypothesized that adult horses can sort Senecio jacobaea out of the contaminated hay when hay is fed ad libitum. Six warmblood geldings with a mean (±SD) age of 15 ± 2 years were included. In a randomized study, Senecio jacobaea contaminated hay (5% or 10% contamination level) was provided at several timepoints over the day for 1 hour to six. Hay was provided ad libitum for the rest of the day. The horses’ rejection behaviour towards Senecio jacobaea was observed. If a horse ingested two Senecio jacobaea plants twice at different timepoints, then the horse was excluded from the experiment. Results Two out of six horses had to be excluded from the study after three out of 12 observation periods due to repeated Senecio jacobaea intake. Two other horses had to be excluded after nine and 11 out of 12 observation periods. Only two horses were able to sort out the various amounts (5 and 10% contamination level) of Senecio jacobaea during the whole experiment. Conclusions Horses’ intake of Senecio jacobaea cannot be avoided despite being fed with hay ad libitum. Due to the risk of chronic intoxication by pyrrolizidine alkaloids intake, feeding Senecio jacobaea contaminated hay must be avoided, and pastures with Senecio jacobaea growth are considered inappropriate for feed production.