PLANT-SOIL FEEDBACKS IN A CHANGING WORLD Plant-soil feedbacks: the past, the present and future challenges
01 Jan 2013-
TL;DR: In this article, a plant-soil feedback model has been proposed to explain succession, invasion, response to climate warming and diversity-productivity relationships in terrestrial ecosystems, and to predict consequences of these interactions under a variety of conditions.
Abstract: Summary 1. Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. 2. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. 3. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. 4. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. 5. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.
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TL;DR: It is suggested that other topics also need addressing, including better assessment of the wider benefits of intercropping in terms of multiple ecosystem services, collaboration with agricultural engineering, and more effective interdisciplinary research.
Abstract: Intercropping is a farming practice involving two or more crop species, or genotypes, growing together and coexisting for a time. On the fringes of modern intensive agriculture, intercropping is important in many subsistence or low-input/resource-limited agricultural systems. By allowing genuine yield gains without increased inputs, or greater stability of yield with decreased inputs, intercropping could be one route to delivering ‘sustainable intensification’. We discuss how recent knowledge from agronomy, plant physiology and ecology can be combined with the aim of improving intercropping systems. Recent advances in agronomy and plant physiology include better understanding of the mechanisms of interactions between crop genotypes and species – for example, enhanced resource availability through niche complementarity. Ecological advances include better understanding of the context-dependency of interactions, the mechanisms behind disease and pest avoidance, the links between above- and below-ground systems, and the role of microtopographic variation in coexistence. This improved understanding can guide approaches for improving intercropping systems, including breeding crops for intercropping. Although such advances can help to improve intercropping systems, we suggest that other topics also need addressing. These include better assessment of the wider benefits of intercropping in terms of multiple ecosystem services, collaboration with agricultural engineering, and more effective interdisciplinary research.
738 citations
Cites background from "PLANT-SOIL FEEDBACKS IN A CHANGING ..."
...Increasing plant diversity helps tomaintain soil organismdiversity (Van der Putten et al., 2013), and increasing soil organism diversity leads to increased plant productivity with, for example, a > 50% increase in shoot biomass observed with increasing mycrorrhizal species number (Van der Heijden…...
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TL;DR: It is demonstrated that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition and the causes of variation in root microbiomes are emphasized.
Abstract: Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host–microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere Streptomyces are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors.
598 citations
TL;DR: It is demonstrated that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome, and this is the first study to report mycorrhizal keystoneTaxa for agroecosystems.
Abstract: Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till, and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harbored a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R2 = 0.366; P < 0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH, and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.
573 citations
TL;DR: A large-scale study of North American trees reveals how different soil-associated fungi can either help or hinder tree growth, and suggests mycorrhizal type could be an important contributor to population regulation and community structure in temperate forests.
Abstract: Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.
436 citations
TL;DR: How climatic change affects soil microbes and soil microbe-plant interactions directly and indirectly is explored, and what ramifications changes in these interactions may have on the composition and function of ecosystems are discussed.
Abstract: Global change is altering species distributions and thus interactions among organisms. Organisms live in concert with thousands of other species, some beneficial, some pathogenic, some which have little to no effect in complex communities. Since natural communities are composed of organisms with very different life history traits and dispersal ability it is unlikely they will all respond to climatic change in a similar way. Disjuncts in plant-pollinator and plant-herbivore interactions under global change have been relatively well described, but plant-soil microorganism and soil microbe-microbe relationships have received less attention. Since soil microorganisms regulate nutrient transformations, provide plants with nutrients, allow co-existence among neighbors, and control plant populations, changes in soil microorganism-plant interactions could have significant ramifications for plant community composition and ecosystem function. In this paper we explore how climatic change affects soil microbes and soil microbe-plant interactions directly and indirectly, discuss what we see as emerging and exciting questions and areas for future research, and discuss what ramifications changes in these interactions may have on the composition and function of ecosystems.
429 citations
References
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TL;DR: A review of the ecological impacts of recent climate change exposes a coherent pattern of ecological change across systems, from polar terrestrial to tropical marine environments.
Abstract: There is now ample evidence of the ecological impacts of recent climate change, from polar terrestrial to tropical marine environments. The responses of both flora and fauna span an array of ecosystems and organizational hierarchies, from the species to the community levels. Despite continued uncertainty as to community and ecosystem trajectories under global change, our review exposes a coherent pattern of ecological change across systems. Although we are only at an early stage in the projected trends of global warming, ecological responses to recent climate change are already clearly visible.
9,369 citations
"PLANT-SOIL FEEDBACKS IN A CHANGING ..." refers background in this paper
...cies (Walther et al. 2002) is expected to disrupt current com-...
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...The current climate-mediated range expansion of many species (Walther et al. 2002) is expected to disrupt current communities when species differ in dispersal capacity: plants disperse faster than many soil organisms (Berg et al. 2010)....
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TL;DR: Rooting patterns for terrestrial biomes are analyzed and distributions for various plant functional groups are compared and the merits and possible shortcomings of the analysis are discussed in the context of root biomass and root functioning.
Abstract: Understanding and predicting ecosystem functioning (e.g., carbon and water fluxes) and the role of soils in carbon storage requires an accurate assessment of plant rooting distributions. Here, in a comprehensive literature synthesis, we analyze rooting patterns for terrestrial biomes and compare distributions for various plant functional groups. We compiled a database of 250 root studies, subdividing suitable results into 11 biomes, and fitted the depth coefficient β to the data for each biome (Gale and Grigal 1987). β is a simple numerical index of rooting distribution based on the asymptotic equation Y=1-βd, where d = depth and Y = the proportion of roots from the surface to depth d. High values of β correspond to a greater proportion of roots with depth. Tundra, boreal forest, and temperate grasslands showed the shallowest rooting profiles (β=0.913, 0.943, and 0.943, respectively), with 80-90% of roots in the top 30 cm of soil; deserts and temperate coniferous forests showed the deepest profiles (β=0.975 and 0.976, respectively) and had only 50% of their roots in the upper 30 cm. Standing root biomass varied by over an order of magnitude across biomes, from approximately 0.2 to 5 kg m-2. Tropical evergreen forests had the highest root biomass (5 kg m-2), but other forest biomes and sclerophyllous shrublands were of similar magnitude. Root biomass for croplands, deserts, tundra and grasslands was below 1.5 kg m-2. Root/shoot (R/S) ratios were highest for tundra, grasslands, and cold deserts (ranging from 4 to 7); forest ecosystems and croplands had the lowest R/S ratios (approximately 0.1 to 0.5). Comparing data across biomes for plant functional groups, grasses had 44% of their roots in the top 10 cm of soil. (β=0.952), while shrubs had only 21% in the same depth increment (β=0.978). The rooting distribution of all temperate and tropical trees was β=0.970 with 26% of roots in the top 10 cm and 60% in the top 30 cm. Overall, the globally averaged root distribution for all ecosystems was β=0.966 (r 2=0.89) with approximately 30%, 50%, and 75% of roots in the top 10 cm, 20 cm, and 40 cm, respectively. We discuss the merits and possible shortcomings of our analysis in the context of root biomass and root functioning.
2,554 citations
"PLANT-SOIL FEEDBACKS IN A CHANGING ..." refers background in this paper
...and biological environment by changing root architecture and rooting depth (Jackson et al. 1996)....
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...Moreover, such shifts can modify the soil physical, chemical and biological environment by changing root architecture and rooting depth (Jackson et al. 1996)....
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TL;DR: It is suggested that more effectively integrating microbial ecology into ecosystem ecology will require a more complete integration of microbial physiological ecology, population biology, and process ecology.
Abstract: Microorganisms have a variety of evolutionary adaptations and physiological acclimation mechanisms that allow them to survive and remain active in the face of environmental stress. Physiological responses to stress have costs at the organismal level that can result in altered ecosystem-level C, energy, and nutrient flows. These large-scale impacts result from direct effects on active microbes' physiology and by controlling the composition of the active microbial community. We first consider some general aspects of how microbes experience environmental stresses and how they respond to them. We then discuss the impacts of two important ecosystem-level stressors, drought and freezing, on microbial physiology and community composition. Even when microbial community response to stress is limited, the physiological costs imposed on soil microbes are large enough that they may cause large shifts in the allocation and fate of C and N. For example, for microbes to synthesize the osmolytes they need to survive a single drought episode they may consume up to 5% of total annual net primary production in grassland ecosystems, while acclimating to freezing conditions switches Arctic tundra soils from immobilizing N during the growing season to mineralizing it during the winter. We suggest that more effectively integrating microbial ecology into ecosystem ecology will require a more complete integration of microbial physiological ecology, population biology, and process ecology.
1,828 citations
TL;DR: A greater understanding of how mycorrhizas function in complex natural systems is a prerequisite to managing them in agriculture, forestry, and restoration.
Abstract: A great diversity of plants and fungi engage in mycorrhizal associations. In natural habitats, and in an ecologically meaningful time span, these associations have evolved to improve the fitness of both plant and fungal symbionts. In systems managed by humans, mycorrhizal associations often improve plant productivity, but this is not always the case. Mycorrhizal fungi might be considered to be parasitic on plants when net cost of the symbiosis exceeds net benefits. Parasitism can be developmentally induced, environmentally induced, or possibly genotypically induced. Morphological, phenological, and physiological characteristics of the symbionts influence the functioning of mycorrhizas at an individual scale. Biotic and abiotic factors at the rhizosphere, community, and ecosystem scales further mediate mycorrhizal functioning. Despite the complexity of mycorrhizal associations, it might be possible to construct predictive models of mycorrhizal functioning. These models will need to incorporate variables and parameters that account for differences in plant responses to, and control of, mycorrhizal fungi, and differences in fungal effects on, and responses to, the plant. Developing and testing quantitative models of mycorrhizal functioning in the real world requires creative experimental manipulations and measurements. This work will be facilitated by recent advances in molecular and biochemical techniques. A greater understanding of how mycorrhizas function in complex natural systems is a prerequisite to managing them in agriculture, forestry, and restoration.
1,776 citations