The Soil-Borne Legacy.

Plants greatly rely on their root microbiome for uptake of nutrients and protection against stresses. Recent studies have uncovered the involvement of plant stress responses in the assembly of plant-beneficial microbiomes. To facilitate durable crop production, deciphering the driving forces that shape the microbiome is crucial.

Environmental drivers of increased ecosystem respiration in a warming tundra.

Arctic and alpine tundra ecosystems are large reservoirs of organic carbon1,2. Climate warming may stimulate ecosystem respiration and release carbon into the atmosphere3,4. The magnitude and persistency of this stimulation and the environmental mechanisms that drive its variation remain uncertain5-7. This hampers the accuracy of global land carbon-climate feedback projections7,8. Here we synthesize 136 datasets from 56 open-top chamber in situ warming experiments located at 28 arctic and alpine tundra sites which have been running for less than 1 year up to 25 years. We show that a mean rise of 1.4 °C [confidence interval (CI) 0.9-2.0 °C] in air and 0.4 °C [CI 0.2-0.7 °C] in soil temperature results in an increase in growing season ecosystem respiration by 30% [CI 22-38%] (n = 136). Our findings indicate that the stimulation of ecosystem respiration was due to increases in both plant-related and microbial respiration (n = 9) and continued for at least 25 years (n = 136). The magnitude of the warming effects on respiration was driven by variation in warming-induced changes in local soil conditions, that is, changes in total nitrogen concentration and pH and by context-dependent spatial variation in these conditions, in particular total nitrogen concentration and the carbon:nitrogen ratio. Tundra sites with stronger nitrogen limitations and sites in which warming had stimulated plant and microbial nutrient turnover seemed particularly sensitive in their respiration response to warming. The results highlight the importance of local soil conditions and warming-induced changes therein for future climatic impacts on respiration.

Microbial competition for phosphorus limits the CO2 response of a mature forest.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3-6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.

Amazon forest biogeography predicts resilience and vulnerability to drought.

Amazonia contains the most extensive tropical forests on Earth, but Amazon carbon sinks of atmospheric CO2 are declining, as deforestation and climate-change-associated droughts1-4 threaten to push these forests past a tipping point towards collapse5-8. Forests exhibit complex drought responses, indicating both resilience (photosynthetic greening) and vulnerability (browning and tree mortality), that are difficult to explain by climate variation alone9-17. Here we combine remotely sensed photosynthetic indices with ground-measured tree demography to identify mechanisms underlying drought resilience/vulnerability in different intact forest ecotopes18,19 (defined by water-table depth, soil fertility and texture, and vegetation characteristics). In higher-fertility southern Amazonia, drought response was structured by water-table depth, with resilient greening in shallow-water-table forests (where greater water availability heightened response to excess sunlight), contrasting with vulnerability (browning and excess tree mortality) over deeper water tables. Notably, the resilience of shallow-water-table forest weakened as drought lengthened. By contrast, lower-fertility northern Amazonia, with slower-growing but hardier trees (or, alternatively, tall forests, with deep-rooted water access), supported more-drought-resilient forests independent of water-table depth. This functional biogeography of drought response provides a framework for conservation decisions and improved predictions of heterogeneous forest responses to future climate changes, warning that Amazonia's most productive forests are also at greatest risk, and that longer/more frequent droughts are undermining multiple ecohydrological strategies and capacities for Amazon forest resilience.

Rainforest transformation reallocates energy from green to brown food webs.

Terrestrial animal biodiversity is increasingly being lost because of land-use change1,2. However, functional and energetic consequences aboveground and belowground and across trophic levels in megadiverse tropical ecosystems remain largely unknown. To fill this gap, we assessed changes in energy fluxes across 'green' aboveground (canopy arthropods and birds) and 'brown' belowground (soil arthropods and earthworms) animal food webs in tropical rainforests and plantations in Sumatra, Indonesia. Our results showed that most of the energy in rainforests is channelled to the belowground animal food web. Oil palm and rubber plantations had similar or, in the case of rubber agroforest, higher total animal energy fluxes compared to rainforest but the key energetic nodes were distinctly different: in rainforest more than 90% of the total animal energy flux was channelled by arthropods in soil and canopy, whereas in plantations more than 50% of the energy was allocated to annelids (earthworms). Land-use change led to a consistent decline in multitrophic energy flux aboveground, whereas belowground food webs responded with reduced energy flux to higher trophic levels, down to -90%, and with shifts from slow (fungal) to fast (bacterial) energy channels and from faeces production towards consumption of soil organic matter. This coincides with previously reported soil carbon stock depletion3. Here we show that well-documented animal biodiversity declines with tropical land-use change4-6 are associated with vast energetic and functional restructuring in food webs across aboveground and belowground ecosystem compartments.

Unlocking bacterial potential to reduce farmland N2O emissions.

Farmed soils contribute substantially to global warming by emitting N2O (ref. 1), and mitigation has proved difficult2. Several microbial nitrogen transformations produce N2O, but the only biological sink for N2O is the enzyme NosZ, catalysing the reduction of N2O to N2 (ref. 3). Although strengthening the NosZ activity in soils would reduce N2O emissions, such bioengineering of the soil microbiota is considered challenging4,5. However, we have developed a technology to achieve this, using organic waste as a substrate and vector for N2O-respiring bacteria selected for their capacity to thrive in soil6-8. Here we have analysed the biokinetics of N2O reduction by our most promising N2O-respiring bacterium, Cloacibacterium sp. CB-01, its survival in soil and its effect on N2O emissions in field experiments. Fertilization with waste from biogas production, in which CB-01 had grown aerobically to about 6 × 109 cells per millilitre, reduced N2O emissions by 50-95%, depending on soil type. The strong and long-lasting effect of CB-01 is ascribed to its tenacity in soil, rather than its biokinetic parameters, which were inferior to those of other strains of N2O-respiring bacteria. Scaling our data up to the European level, we find that national anthropogenic N2O emissions could be reduced by 5-20%, and more if including other organic wastes. This opens an avenue for cost-effective reduction of N2O emissions for which other mitigation options are lacking at present.

Fertilizer management for global ammonia emission reduction.

Crop production is a large source of atmospheric ammonia (NH3), which poses risks to air quality, human health and ecosystems1-5. However, estimating global NH3 emissions from croplands is subject to uncertainties because of data limitations, thereby limiting the accurate identification of mitigation options and efficacy4,5. Here we develop a machine learning model for generating crop-specific and spatially explicit NH3 emission factors globally (5-arcmin resolution) based on a compiled dataset of field observations. We show that global NH3 emissions from rice, wheat and maize fields in 2018 were 4.3 ± 1.0 Tg N yr-1, lower than previous estimates that did not fully consider fertilizer management practices6-9. Furthermore, spatially optimizing fertilizer management, as guided by the machine learning model, has the potential to reduce the NH3 emissions by about 38% (1.6 ± 0.4 Tg N yr-1) without altering total fertilizer nitrogen inputs. Specifically, we estimate potential NH3 emissions reductions of 47% (44-56%) for rice, 27% (24-28%) for maize and 26% (20-28%) for wheat cultivation, respectively. Under future climate change scenarios, we estimate that NH3 emissions could increase by 4.0 ± 2.7% under SSP1-2.6 and 5.5 ± 5.7% under SSP5-8.5 by 2030-2060. However, targeted fertilizer management has the potential to mitigate these increases.

Microbial carbon use efficiency promotes global soil carbon storage.

Soils store more carbon than other terrestrial ecosystems1,2. How soil organic carbon (SOC) forms and persists remains uncertain1,3, which makes it challenging to understand how it will respond to climatic change3,4. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss5-7. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways4,6,8-11, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes12,13. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved7,14,15. Here we examine the relationship between CUE and the preservation of SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis. We find that CUE is at least four times as important as other evaluated factors, such as carbon input, decomposition or vertical transport, in determining SOC storage and its spatial variation across the globe. In addition, CUE shows a positive correlation with SOC content. Our findings point to microbial CUE as a major determinant of global SOC storage. Understanding the microbial processes underlying CUE and their environmental dependence may help the prediction of SOC feedback to a changing climate.

Tree diversity increases decadal forest soil carbon and nitrogen accrual.

Increasing soil carbon and nitrogen storage can help mitigate climate change and sustain soil fertility1,2. A large number of biodiversity-manipulation experiments collectively suggest that high plant diversity increases soil carbon and nitrogen stocks3,4. It remains debated, however, whether such conclusions hold in natural ecosystems5-12. Here we analyse Canada's National Forest Inventory (NFI) database with the help of structural equation modelling (SEM) to explore the relationship between tree diversity and soil carbon and nitrogen accumulation in natural forests. We find that greater tree diversity is associated with higher soil carbon and nitrogen accumulation, validating inferences from biodiversity-manipulation experiments. Specifically, on a decadal scale, increasing species evenness from its minimum to maximum value increases soil carbon and nitrogen in the organic horizon by 30% and 42%, whereas increasing functional diversity enhances soil carbon and nitrogen in the mineral horizon by 32% and 50%, respectively. Our results highlight that conserving and promoting functionally diverse forests could promote soil carbon and nitrogen storage, enhancing both carbon sink capacity and soil nitrogen fertility.

Landscape dynamics and the Phanerozoic diversification of the biosphere.

The long-term diversification of the biosphere responds to changes in the physical environment. Yet, over the continents, the nearly monotonic expansion of life started later in the early part of the Phanerozoic eon1 than the expansion in the marine realm, where instead the number of genera waxed and waned over time2. A comprehensive evaluation of the changes in the geodynamic and climatic forcing fails to provide a unified theory for the long-term pattern of evolution of life on Earth. Here we couple climate and plate tectonics models to numerically reconstruct the evolution of the Earth's landscape over the entire Phanerozoic eon, which we then compare to palaeo-diversity datasets from marine animal and land plant genera. Our results indicate that biodiversity is strongly reliant on landscape dynamics, which at all times determine the carrying capacity of both the continental domain and the oceanic domain. In the oceans, diversity closely adjusted to the riverine sedimentary flux that provides nutrients for primary production. On land, plant expansion was hampered by poor edaphic conditions until widespread endorheic basins resurfaced continents with a sedimentary cover that facilitated the development of soil-dependent rooted flora, and the increasing variety of the landscape additionally promoted their development.

Cost-effective mitigation of nitrogen pollution from global croplands.

Cropland is a main source of global nitrogen pollution1,2. Mitigating nitrogen pollution from global croplands is a grand challenge because of the nature of non-point-source pollution from millions of farms and the constraints to implementing pollution-reduction measures, such as lack of financial resources and limited nitrogen-management knowledge of farmers3. Here we synthesize 1,521 field observations worldwide and identify 11 key measures that can reduce nitrogen losses from croplands to air and water by 30-70%, while increasing crop yield and nitrogen use efficiency (NUE) by 10-30% and 10-80%, respectively. Overall, adoption of this package of measures on global croplands would allow the production of 17 ± 3 Tg (1012 g) more crop nitrogen (20% increase) with 22 ± 4 Tg less nitrogen fertilizer used (21% reduction) and 26 ± 5 Tg less nitrogen pollution (32% reduction) to the environment for the considered base year of 2015. These changes could gain a global societal benefit of 476 ± 123 billion US dollars (USD) for food supply, human health, ecosystems and climate, with net mitigation costs of only 19 ± 5 billion USD, of which 15 ± 4 billion USD fertilizer saving offsets 44% of the gross mitigation cost. To mitigate nitrogen pollution from croplands in the future, innovative policies such as a nitrogen credit system (NCS) could be implemented to select, incentivize and, where necessary, subsidize the adoption of these measures.

Optimal nitrogen rate strategy for sustainable rice production in China.

Avoiding excessive agricultural nitrogen (N) use without compromising yields has long been a priority for both research and government policy in China1,2. Although numerous rice-related strategies have been proposed3-5, few studies have assessed their impacts on national food self-sufficiency and environmental sustainability and fewer still have considered economic risks faced by millions of smallholders. Here we established an optimal N rate strategy based on maximizing either economic (ON) or ecological (EON) performance using new subregion-specific models. Using an extensive on-farm dataset, we then assessed the risk of yield losses among smallholder farmers and the challenges of implementing the optimal N rate strategy. We find that meeting national rice production targets in 2030 is possible while concurrently reducing nationwide N consumption by 10% (6-16%) and 27% (22-32%), mitigating reactive N (Nr) losses by 7% (3-13%) and 24% (19-28%) and increasing N-use efficiency by 30% (3-57%) and 36% (8-64%) for ON and EON, respectively. This study identifies and targets subregions with disproportionate environmental impacts and proposes N rate strategies to limit national Nr pollution below proposed environmental thresholds, without compromising soil N stocks or economic benefits for smallholders. Thereafter, the preferable N strategy is allocated to each region based on the trade-off between economic risk and environmental benefit. To facilitate the adoption of the annually revised subregional N rate strategy, several recommendations were provided, including a monitoring network, fertilization quotas and smallholder subsidies.

Agricultural pesticide land budget and river discharge to oceans.

Pesticides are ubiquitous environmental pollutants negatively affecting ecosystem and human health1,2. About 3 Tg of pesticides are used annually in agriculture to protect crops3. How much of these pesticides remain on land and reach the aquifer or the ocean is uncertain. Monitoring their environmental fate is challenging, and a detailed picture of their mobility in time and space is largely missing4. Here, we develop a process-based model accounting for the hydrology and biogeochemistry of the 92 most used agricultural pesticide active substances to assess their pathways through the principal catchments of the world and draw a near-present picture of the global land and river budgets, including discharge to oceans. Of the 0.94 Tg net annual pesticide input in 2015 used in this study, 82% is biologically degraded, 10% remains as residue in soil and 7.2% leaches below the root zone. Rivers receive 0.73 Gg of pesticides from their drainage at a rate of 10 to more than 100 kg yr-1 km-1. By contrast to their fate in soil, only 1.1% of pesticides entering rivers are degraded along streams, exceeding safety levels (concentrations >1 µg l-1) in more than 13,000 km of river length, with 0.71 Gg of pesticide active ingredients released to oceans every year. Herbicides represent the prevalent pesticide residue on both land (72%) and river outlets (62%).

The Arabidopsis SGN3/GSO1 receptor kinase integrates soil nitrogen status into shoot development.

The Casparian strip is a barrier in the endodermal cell walls of plants that allows the selective uptake of nutrients and water. In the model plant Arabidopsis thaliana, its development and establishment are under the control of a receptor-ligand mechanism termed the Schengen pathway. This pathway facilitates barrier formation and activates downstream compensatory responses in case of dysfunction. However, due to a very tight functional association with the Casparian strip, other potential signaling functions of the Schengen pathway remain obscure. In this work, we created a MYB36-dependent synthetic positive feedback loop that drives Casparian strip formation independently of Schengen-induced signaling. We evaluated this by subjecting plants in which the Schengen pathway has been uncoupled from barrier formation, as well as a number of established barrier-mutant plants, to agar-based and soil conditions that mimic agricultural settings. Under the latter conditions, the Schengen pathway is necessary for the establishment of nitrogen-deficiency responses in shoots. These data highlight Schengen signaling as an essential hub for the adaptive integration of signaling from the rhizosphere to aboveground tissues.

The Microbiology of Biological Soil Crusts.

Biological soil crusts are thin, inconspicuous communities along the soil atmosphere ecotone that, until recently, were unrecognized by ecologists and even more so by microbiologists. In its broadest meaning, the term biological soil crust (or biocrust) encompasses a variety of communities that develop on soil surfaces and are powered by photosynthetic primary producers other than higher plants: cyanobacteria, microalgae, and cryptogams like lichens and mosses. Arid land biocrusts are the most studied, but biocrusts also exist in other settings where plant development is constrained. The minimal requirement is that light impinge directly on the soil; this is impeded by the accumulation of plant litter where plants abound. Since scientists started paying attention, much has been learned about their microbial communities, their composition, ecological extent, and biogeochemical roles, about how they alter the physical behavior of soils, and even how they inform an understanding of early life on land. This has opened new avenues for ecological restoration and agriculture.

Abiotic stress responses in plants.

Plants cannot move, so they must endure abiotic stresses such as drought, salinity and extreme temperatures. These stressors greatly limit the distribution of plants, alter their growth and development, and reduce crop productivity. Recent progress in our understanding of the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications. This improved knowledge can be used to boost crop productivity and agricultural sustainability through genetic, chemical and microbial approaches.

Sufficient conditions for rapid range expansion of a boreal conifer.

Unprecedented modern rates of warming are expected to advance boreal forest into Arctic tundra1, thereby reducing albedo2-4, altering carbon cycling4 and further changing climate1-4, yet the patterns and processes of this biome shift remain unclear5. Climate warming, required for previous boreal advances6-17, is not sufficient by itself for modern range expansion of conifers forming forest-tundra ecotones5,12-15,17-20. No high-latitude population of conifers, the dominant North American Arctic treeline taxon, has previously been documented5 advancing at rates following the last glacial maximum (LGM)6-8. Here we describe a population of white spruce (Picea glauca) advancing at post-LGM rates7 across an Arctic basin distant from established treelines and provide evidence of mechanisms sustaining the advance. The population doubles each decade, with exponential radial growth in the main stems of individual trees correlating positively with July air temperature. Lateral branches in adults and terminal leaders in large juveniles grow almost twice as fast as those at established treelines. We conclude that surpassing temperature thresholds1,6-17, together with winter winds facilitating long-distance dispersal, deeper snowpack and increased soil nutrient availability promoting recruitment and growth, provides sufficient conditions for boreal forest advance. These observations enable forecast modelling with important insights into the environmental conditions converting tundra into forest.

Direct evidence for phosphorus limitation on Amazon forest productivity.

The productivity of rainforests growing on highly weathered tropical soils is expected to be limited by phosphorus availability1. Yet, controlled fertilization experiments have been unable to demonstrate a dominant role for phosphorus in controlling tropical forest net primary productivity. Recent syntheses have demonstrated that responses to nitrogen addition are as large as to phosphorus2, and adaptations to low phosphorus availability appear to enable net primary productivity to be maintained across major soil phosphorus gradients3. Thus, the extent to which phosphorus availability limits tropical forest productivity is highly uncertain. The majority of the Amazonia, however, is characterized by soils that are more depleted in phosphorus than those in which most tropical fertilization experiments have taken place2. Thus, we established a phosphorus, nitrogen and base cation addition experiment in an old growth Amazon rainforest, with a low soil phosphorus content that is representative of approximately 60% of the Amazon basin. Here we show that net primary productivity increased exclusively with phosphorus addition. After 2 years, strong responses were observed in fine root (+29%) and canopy productivity (+19%), but not stem growth. The direct evidence of phosphorus limitation of net primary productivity suggests that phosphorus availability may restrict Amazon forest responses to CO2 fertilization4, with major implications for future carbon sequestration and forest resilience to climate change.

The OsEIL1-OsWOX11 transcription factor module controls rice crown root development in response to soil compaction.

Optimizing the root architecture of crops is an effective strategy for improving crop yields. Soil compaction is a serious global problem that limits crop productivity by restricting root growth, but the underlying molecular mechanisms are largely unclear. Here, we show that ethylene stimulates rice (Oryza sativa) crown root development in response to soil compaction. First, we demonstrate that compacted soil promotes ethylene production and the accumulation of ETHYLENE INSENSITIVE 3-LIKE 1 (OsEIL1) in rice roots, stimulating crown root primordia initiation and development, thereby increasing crown root number in lower stem nodes. Through transcriptome profiling and molecular analyses, we reveal that OsEIL1 directly activates the expression of WUSCHEL-RELATED HOMEOBOX 11 (OsWOX11), an activator of crown root emergence and growth, and that OsWOX11 mutations delay crown root development, thus impairing the plant's response to ethylene and soil compaction. Genetic analysis demonstrates that OsWOX11 functions downstream of OsEIL1. In summary, our results demonstrate that the OsEIL1-OsWOX11 module regulates ethylene action during crown root development in response to soil compaction, providing a strategy for the genetic modification of crop root architecture and grain agronomic traits.

A trade-off between plant and soil carbon storage under elevated CO2.

Terrestrial ecosystems remove about 30 per cent of the carbon dioxide (CO2) emitted by human activities each year1, yet the persistence of this carbon sink depends partly on how plant biomass and soil organic carbon (SOC) stocks respond to future increases in atmospheric CO2 (refs. 2,3). Although plant biomass often increases in elevated CO2 (eCO2) experiments4-6, SOC has been observed to increase, remain unchanged or even decline7. The mechanisms that drive this variation across experiments remain poorly understood, creating uncertainty in climate projections8,9. Here we synthesized data from 108 eCO2 experiments and found that the effect of eCO2 on SOC stocks is best explained by a negative relationship with plant biomass: when plant biomass is strongly stimulated by eCO2, SOC storage declines; conversely, when biomass is weakly stimulated, SOC storage increases. This trade-off appears to be related to plant nutrient acquisition, in which plants increase their biomass by mining the soil for nutrients, which decreases SOC storage. We found that, overall, SOC stocks increase with eCO2 in grasslands (8 ± 2 per cent) but not in forests (0 ± 2 per cent), even though plant biomass in grasslands increase less (9 ± 3 per cent) than in forests (23 ± 2 per cent). Ecosystem models do not reproduce this trade-off, which implies that projections of SOC may need to be revised.