Plant-Soil Feedback Effects on Growth, Defense and Susceptibility to a Soil-Borne Disease in a Cut Flower Crop: Species and Functional Group Effects.

Plants can influence the soil they grow in, and via these changes in the soil they can positively or negatively influence other plants that grow later in this soil, a phenomenon called plant-soil feedback. A fascinating possibility is then to apply positive plant-soil feedback effects in sustainable agriculture to promote plant growth and resistance to pathogens. We grew the cut flower chrysanthemum (Dendranthema X grandiflora) in sterile soil inoculated with soil collected from a grassland that was subsequently conditioned by 37 plant species of three functional groups (grass, forb, legume), and compared it to growth in 100% sterile soil (control). We tested the performance of chrysanthemum by measuring plant growth, and defense (leaf chlorogenic acid concentration) and susceptibility to the oomycete pathogen Pythium ultimum. In presence of Pythium, belowground biomass of chrysanthemum declined but aboveground biomass was not affected compared to non-Pythium inoculated plants. We observed strong differences among species and among functional groups in their plant-soil feedback effects on chrysanthemum. Soil inocula that were conditioned by grasses produced higher chrysanthemum above- and belowground biomass and less leaf yellowness than inocula conditioned by legumes or forbs. Chrysanthemum had lower root/shoot ratios in response to Pythium in soil conditioned by forbs than by grasses. Leaf chlorogenic acid concentrations increased in presence of Pythium and correlated positively with chrysanthemum aboveground biomass. Although chlorogenic acid differed between soil inocula, it did not differ between functional groups. There was no relationship between the phylogenetic distance of the conditioning plant species to chrysanthemum and their plant-soil feedback effects on chrysanthemum. Our study provides novel evidence that plant-soil feedback effects can influence crop health, and shows that plant-soil feedbacks, plant disease susceptibility, and plant aboveground defense compounds are tightly linked. Moreover, we highlight the relevance of considering plant-soil feedbacks in sustainable horticulture, and the larger role of grasses compared to legumes or forbs in this.

Divergent composition but similar function of soil food webs of individual plants: plant species and community effects.

Soils are extremely rich in biodiversity, and soil organisms play pivotal roles in supporting terrestrial life, but the role that individual plants and plant communities play in influencing the diversity and functioning of soil food webs remains highly debated. Plants, as primary producers and providers of resources to the soil food web, are of vital importance for the composition, structure, and functioning of soil communities. However, whether natural soil food webs that are completely open to immigration and emigration differ underneath individual plants remains unknown. In a biodiversity restoration experiment we first compared the soil nematode communities of 228 individual plants belonging to eight herbaceous species. We included grass, leguminous, and non-leguminous species. Each individual plant grew intermingled with other species, but all plant species had a different nematode community. Moreover, nematode communities were more similar when plant individuals were growing in the same as compared to different plant communities, and these effects were most apparent for the groups of bacterivorous, carnivorous, and omnivorous nematodes. Subsequently, we analyzed the composition, structure, and functioning of the complete soil food webs of 58 individual plants, belonging to two of the plant species, Lotus corniculatus (Fabaceae) and Plantago lanceolata (Plantaginaceae). We isolated and identified more than 150 taxa/groups of soil organisms. The soil community composition and structure of the entire food webs were influenced both by the species identity of the plant individual and the surrounding plant community. Unexpectedly, plant identity had the strongest effects on decomposing soil organisms, widely believed to be generalist feeders. In contrast, quantitative food web modeling showed that the composition of the plant community influenced nitrogen mineralization under individual plants, but that plant species identity did not affect nitrogen or carbon mineralization or food web stability. Hence, the composition and structure of entire soil food webs vary at the scale of individual plants and are strongly influenced by the species identity of the plant. However, the ecosystem functions these food webs provide are determined by the identity of the entire plant community.

Empirical and theoretical challenges in aboveground-belowground ecology.

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground-belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground-belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury.

Studies on induced defenses have predominantly focused on foliar induction by above-ground herbivores and pathogens. However, roots are attacked by as many if not more phytophages than shoots, so in reality plants are exposed to above- and below-ground attack. Here, we report effects of foliar and/or root damage on terpenoid aldehyde accumulation in cotton (Gossypium herbaceum). Using HPLC, we analyzed concentrations of individual terpenoid aldehydes in foliage and root tissue. In undamaged plants, terpenoid aldehydes were concentrated in young immature main leaves. Concentrations in side leaves, branching from the main leaves, did not differ among leaf position. Above-ground feeding by Spodopterta exigua larvae on a mature leaf enhanced terpenoid concentrations in immature leaves but not in the damaged leaf. In particular, concentrations of hemigossypolone and the heliocides 1 and 4 were enhanced following herbivory. Root herbivory by wireworms (Agriotes lineatus) also resulted in an increase in terpenoid levels in the foliage. In contrast with foliar herbivory, both immature and mature leaves were induced. However, the level of induction after root herbivory was much lower compared to foliar herbivory. Plants exposed to root herbivory also had significantly higher levels of terpenoid aldehydes in root tissue, while no such effect was found following foliar herbivory. Plants exposed to both root and foliar herbivory appeared to induce primarily above-ground at the cost of below-ground defense. The implications for above- and below-ground Mutitrophic interactions are discussed.

Above- and below ground trophic interactions on creeping thistle (Cirsium arvense) in high- and low-diversity plant communities: potential for biotic resistance?

The capacity of local communities to control introduced plants is called biotic resistance. Biotic resistance has been almost exclusively tested for plant competition and above ground herbivores and pathogens, while neglecting root herbivores and soil pathogens. Here, we present biotic resistance by above- and below ground herbivores in concert, and relate the abundance of the plant enemies to the species diversity of the local plant communities. The study was carried out in a 7-year-old biodiversity field experiment. We used creeping thistle (Cirsium arvense) as a model, and quantified sap-sucking herbivores: above ground aphids, their antagonists, and root-feeding nematodes. As plant diversity treatments, we used field plots sown with high (15 plant species, HSD) or low (4 plant species, LSD) diverse seed mixtures in 1996 and that were not weeded. Creeping thistle became established spontaneously at the start of the experiment. In 2002, in HSD plots, 90 % of the plant community was made up by 11 species, compared to seven species in LSD plots. No differences were found for C. arvense abundance or biomass. Above ground, three aphid species were found on C. arvense-Uroleucon cirsii, Aphis fabae, and Macrosiphum euphorbiae, but the latter was found only in low densities. Significantly more aphid species were found on individual plants in HSD plots. Moreover, in HSD plots, on average 10 % of aphids were parasitized, while no parasitism was observed in LSD plots. In the root zone of C. arvense, significantly more nematodes were found in HSD than in LSD plots, and a significantly higher proportion of those nematodes were plant parasites. The dominant plant parasitic nematode in both treatments was Paratylenchus. We conclude that biotic resistance by natural enemies may be enhanced by plant species diversity, but that above- and below ground sap-sucking herbivores do not necessarily have to respond similarly to the diversity of the surrounding plant community.