Summary1. Plant roots selectively forage for soil nutrients when these are heterogeneously distributed. In turn, effects of plant roots on biotic and abiotic conditions in the soil, which result in socalled plant-soil feedback can be heterogeneously distributed as well, but it is unknown how this heterogeneity affects root distribution, nutrient uptake and plant biomass production. Here, we investigate plant root distribution patterns as influenced by spatial heterogeneity of plant-soil feedback in soil and quantify consequences for plant nitrogen uptake and biomass production. 2. We conditioned soils by four grassland plant species to obtain 'own' and 'foreign' soils that differed in biotic conditions similar as is done by the first phase of plant-soil feedback experiments. We used these conditioned soils to create heterogeneous (one patch of own and three patches of foreign soils) or homogeneous substrates where own and foreign soils were mixed. We also included sterilized soil to study the effect of excluding soil biota, such as pathogens, symbionts and decomposers. We supplied 15 N as tracer to measure nutrient uptake.3. In nonsterile conditions, most plant species produced more biomass in heterogeneous than in homogeneous soil. Root biomass and 15 N uptake rates were higher in foreign than own soil patches. These differences between heterogeneous and homogeneous soil disappeared when soil was sterilized, suggesting that the effects in nonsterilized soils were due to species-specific soil biota that had responded to soil conditioning. 4. We conclude that plants produce more biomass when own and foreign soils are patchily distributed than when mixed. We show that this enhanced productivity is due to nutrient uptake being overall most efficient when own and foreign soils are spatially separated. We propose that spatial heterogeneity of negative plant-soil feedback in species diverse plant communities may provide a better explanation of overyielding than assuming that plant-soil feedback effects are diluted.
The development of pesticide resistance in insects and recent bans on pesticides call for the identification of natural sources of resistance in crops. Here, we used natural variation in pepper ( Capsicum spp.) resistance combined with an untargeted metabolomics approach to detect secondary metabolites related to thrips ( Frankliniella occidentalis ) resistance. Using leaf disc choice assays, we tested 11 Capsicum accessions of C. annuum and C. chinense in both vegetative and flowering stages for thrips resistance. Metabolites in the leaves of these 11 accessions were analyzed using LC-MS based untargeted metabolomics. The choice assays showed significant differences among the accessions in thrips feeding damage. The level of resistance depended on plant developmental stage. Metabolomics analyses showed differences in metabolomes among the Capsicum species and plant developmental stages. Moreover, metabolomic profiles of resistant and susceptible accessions differed. Monomer and dimer acyclic diterpene glycosides (capsianosides) were pinpointed as metabolites that were related to thrips resistance. Sucrose and malonylated flavone glycosides were related to susceptibility. To our knowledge, this is the first time that dimer capsianosides of pepper have been linked to insect resistance. Our results show the potential of untargeted metabolomics as a tool for discovering metabolites that are important in plant – insect interactions. Electronic supplementary material The online version of this article (10.1007/s10886-019-01074-4) contains supplementary material, which is available to authorized users.
Capsicum is a genus containing important crop species, many of which severely suffer from thrips infestation. Thrips feeding damages leaves and fruits, and often results in virus infections. Only a few insecticides are still effective against thrips, underlining the importance of finding natural resistance in crops. Capsicum is a perennial plant which is usually cultivated for several months, during which time the fruits are harvested. From the young vegetative stage to the mature fruit bearing stage, the plants are at risk to thrips infestation. Constitutive resistance to thrips over the entire ontogenetic development is therefore a key trait for a more sustainable and successful cultivation of the hot and sweet pepper. In addition to ontogeny, leaf position can affect the level of thrips resistance. Pest resistance levels are known to differ between young and old leaves. To our knowledge, no studies have explicitly considered ontogeny and leaf position when screening for constitutive resistance to thrips in Capsicum . In this study we analyze whether ontogeny and leaf position affect leaf-based resistance to Frankliniella occidentalis and Thrips tabaci , in 40 Capsicum accessions, comprising five different species. Our results show that resistance to both thrips species in Capsicum varies with ontogenetic stage. This variation in resistance among ontogenetic stages was not consistent among the accessions. However, accessions with constitutive resistance in both the flowering and fruit ripening stage could be identified. In addition, we found that thrips resistance is overall similar at different leaf positions within the ontogenetic stage. This implies that resistance mechanisms, such as defense compounds, are constitutively present at sufficient levels on all leaf positions. Finally, we found that resistance to F. occidentalis and resistance to T. tabaci were not correlated. This indicates that leaf-based resistance in Capsicum is thrips species-specific. Because of the variation in resistance over ontogeny, identifying Capsicum accessions with resistance over their entire lifespan is challenging. For resistance screening, accounting for leaf position may be less of a concern. To identify the defense mechanisms responsible for thrips resistance, it is important to further analyze and compare resistant and susceptible accessions.
Quantifying thrips damage is challenging. We present an automated protocol for the screening of thrips (Thysanoptera: Thripidae) damage on Capsicum (pepper) leaves. We show that standardizing the exposed leaf side is important for resistance ranking of accessions. Our results indicate that thrips resistance is dependent on the plant's developmental stage and its genetic background. Ultimately, our method provides an efficient tool for screening for resistance to insects in applied research and commercial breeding.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. AbstractCapsicum species are commercially grown for pepper production. This crop suffers severely from thrips damage and the identification of natural sources of thrips resistance is essential for the development of resistant cultivars. It is unclear whether resistance to Frankliniella occidentalis as assessed in a specific environment holds under different conditions. Additionally, other thrips species may respond differently to the plant genotypes. Screening for robust and general resistance to thrips encompasses testing different Capsicum accessions under various conditions and with different thrips species. We screened 11 Capsicum accessions (C. annuum and C. chinense) for resistance to F. occidentalis at three different locations in the Netherlands. Next, the same 11 accessions were screened for resistance to Thrips palmi and Scirtothrips dorsalis at two locations in Asia. This resulted in a unique analysis of thrips resistance in Capsicum at five different locations around the world. Finally, all accessions were also screened for resistance to F. occidentalis in the Netherlands using a leaf disc choice assay, allowing direct comparison of whole plant and leaf disc assays. Resistance to F. occidentalis was only partially consistent among the three sites in the Netherlands.The most susceptible accessions were consistently susceptible, but which accession was the most resistant differed among sites. In Asia, one C. chinense accession was particularly resistant to S. dorsalis and T. palmi, but this was not the most resistant accession to F. occidentalis. Overall, resistance to F. occidentalis correlated with S. dorsalis but not with T. palmi resistance in the C. annuum accessions. Damage inflicted on leaf discs reflected damage on the whole plant level. Our study showed that identifying broad spectrum resistance to thrips in Capsicum may prove to be challenging.Breeding programmes should focus on developing cultivars suitable for growing in defined geographic regions with specific thrips species and abiotic conditions.
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