Publications by authors named "Marcel G A van der Heijden"

79 Publications

Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field.

Microbiome 2021 May 7;9(1):103. Epub 2021 May 7.

Division of Agroecology and Environment, Agroscope, Zurich, Switzerland.

Background: Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties.

Results: Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments.

Conclusions: These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions. Video Abstract.
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http://dx.doi.org/10.1186/s40168-021-01049-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8106187PMC
May 2021

A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana.

Plant Mol Biol 2021 Apr 6. Epub 2021 Apr 6.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.

Key Message: Overexpression of genes involved in coumarin production and secretion can mitigate mycorrhizal incompatibility in nonhost Arabidopsis plants. The coumarin scopoletin, in particular, stimulates pre-penetration development and metabolism in mycorrhizal fungi. Although most plants can benefit from mutualistic associations with arbuscular mycorrhizal (AM) fungi, nonhost plant species such as the model Arabidopsis thaliana have acquired incompatibility. The transcriptional response of Arabidopsis to colonization by host-supported AM fungi switches from initial AM recognition to defense activation and plant growth antagonism. However, detailed functional information on incompatibility in nonhost-AM fungus interactions is largely missing. We studied interactions between host-sustained AM fungal networks of Rhizophagus irregularis and 18 Arabidopsis genotypes affected in nonhost penetration resistance, coumarin production and secretion, and defense (salicylic acid, jasmonic acid, and ethylene) and growth hormones (auxin, brassinosteroid, cytokinin, and gibberellin). We demonstrated that root-secreted coumarins can mitigate incompatibility by stimulating fungal metabolism and promoting initial steps of AM colonization. Moreover, we provide evidence that major molecular defenses in Arabidopsis do not operate as primary mechanisms of AM incompatibility nor of growth antagonism. Our study reveals that, although incompatible, nonhost plants can harbor hidden tools that promote initial steps of AM colonization. Moreover, it uncovered the coumarin scopoletin as a novel signal in the pre-penetration dialogue, with possible implications for the chemical communication in plant-mycorrhizal fungi associations.
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http://dx.doi.org/10.1007/s11103-021-01143-xDOI Listing
April 2021

Erosion reduces soil microbial diversity, network complexity and multifunctionality.

ISME J 2021 Mar 12. Epub 2021 Mar 12.

State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, Shaanxi, China.

While soil erosion drives land degradation, the impact of erosion on soil microbial communities and multiple soil functions remains unclear. This hinders our ability to assess the true impact of erosion on soil ecosystem services and our ability to restore eroded environments. Here we examined the effect of erosion on microbial communities at two sites with contrasting soil texture and climates. Eroded plots had lower microbial network complexity, fewer microbial taxa, and fewer associations among microbial taxa, relative to non-eroded plots. Soil erosion also shifted microbial community composition, with decreased relative abundances of dominant phyla such as Proteobacteria, Bacteroidetes, and Gemmatimonadetes. In contrast, erosion led to an increase in the relative abundances of some bacterial families involved in N cycling, such as Acetobacteraceae and Beijerinckiaceae. Changes in microbiota characteristics were strongly related with erosion-induced changes in soil multifunctionality. Together, these results demonstrate that soil erosion has a significant negative impact on soil microbial diversity and functionality.
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http://dx.doi.org/10.1038/s41396-021-00913-1DOI Listing
March 2021

Widespread Occurrence of Pesticides in Organically Managed Agricultural Soils-the Ghost of a Conventional Agricultural Past?

Environ Sci Technol 2021 03 3;55(5):2919-2928. Epub 2021 Feb 3.

Plant-Soil-Interactions, Agroscope, Zurich, Switzerland.

Pesticides are applied in large quantities to agroecosystems worldwide. To date, few studies assessed the occurrence of pesticides in organically managed agricultural soils, and it is unresolved whether these pesticide residues affect soil life. We screened 100 fields under organic and conventional management with an analytical method containing 46 pesticides (16 herbicides, 8 herbicide transformation products, 17 fungicides, seven insecticides). Pesticides were found in all sites, including 40 organic fields. The number of pesticide residues was two times and the concentration nine times higher in conventional compared to organic fields. Pesticide number and concentrations significantly decreased with the duration of organic management. Even after 20 years of organic agriculture, up to 16 different pesticide residues were present. Microbial biomass and specifically the abundance of arbuscular mycorrhizal fungi, a widespread group of beneficial plant symbionts, were significantly negatively linked to the amount of pesticide residues in soil. This indicates that pesticide residues, in addition to abiotic factors such as pH, are a key factor determining microbial soil life in agroecosystems. This comprehensive study demonstrates that pesticides are a hidden reality in agricultural soils, and our results suggest that they have harmful effects on beneficial soil life.
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http://dx.doi.org/10.1021/acs.est.0c06405DOI Listing
March 2021

Relative qPCR to quantify colonization of plant roots by arbuscular mycorrhizal fungi.

Mycorrhiza 2021 Mar 21;31(2):137-148. Epub 2021 Jan 21.

Plant Soil Interactions, Department of Agroecology and Environment, Agroscope, Zurich, Switzerland.

Arbuscular mycorrhiza fungi (AMF) are beneficial soil fungi that can promote the growth of their host plants. Accurate quantification of AMF in plant roots is important because the level of colonization is often indicative of the activity of these fungi. Root colonization is traditionally measured with microscopy methods which visualize fungal structures inside roots. Microscopy methods are labor-intensive, and results depend on the observer. In this study, we present a relative qPCR method to quantify AMF in which we normalized the AMF qPCR signal relative to a plant gene. First, we validated the primer pair AMG1F and AM1 in silico, and we show that these primers cover most AMF species present in plant roots without amplifying host DNA. Next, we compared the relative qPCR method with traditional microscopy based on a greenhouse experiment with Petunia plants that ranged from very high to very low levels of AMF root colonization. Finally, by sequencing the qPCR amplicons with MiSeq, we experimentally confirmed that the primer pair excludes plant DNA while amplifying mostly AMF. Most importantly, our relative qPCR approach was capable of discriminating quantitative differences in AMF root colonization and it strongly correlated (Spearman Rho = 0.875) with quantifications by traditional microscopy. Finally, we provide a balanced discussion about the strengths and weaknesses of microscopy and qPCR methods. In conclusion, the tested approach of relative qPCR presents a reliable alternative method to quantify AMF root colonization that is less operator-dependent than traditional microscopy and offers scalability to high-throughput analyses.
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http://dx.doi.org/10.1007/s00572-020-01014-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7910240PMC
March 2021

Agricultural diversification promotes multiple ecosystem services without compromising yield.

Sci Adv 2020 Nov 4;6(45). Epub 2020 Nov 4.

Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

Enhancing biodiversity in cropping systems is suggested to promote ecosystem services, thereby reducing dependency on agronomic inputs while maintaining high crop yields. We assess the impact of several diversification practices in cropping systems on above- and belowground biodiversity and ecosystem services by reviewing 98 meta-analyses and performing a second-order meta-analysis based on 5160 original studies comprising 41,946 comparisons between diversified and simplified practices. Overall, diversification enhances biodiversity, pollination, pest control, nutrient cycling, soil fertility, and water regulation without compromising crop yields. Practices targeting aboveground biodiversity boosted pest control and water regulation, while those targeting belowground biodiversity enhanced nutrient cycling, soil fertility, and water regulation. Most often, diversification practices resulted in win-win support of services and crop yields. Variability in responses and occurrence of trade-offs highlight the context dependency of outcomes. Widespread adoption of diversification practices shows promise to contribute to biodiversity conservation and food security from local to global scales.
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http://dx.doi.org/10.1126/sciadv.aba1715DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7673676PMC
November 2020

Correction to: Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming.

Microbiome 2020 May 17;8(1):66. Epub 2020 May 17.

Plant-Soil Interactions, Department of Agroecology and Environment, Agroscope, Zurich, Switzerland.

An amendment to this paper has been published and can be accessed via the original article.
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http://dx.doi.org/10.1186/s40168-020-00855-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7232831PMC
May 2020

Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning.

Nat Commun 2019 10 24;10(1):4841. Epub 2019 Oct 24.

Plant Soil Interactions, Division Agroecology and Environment, Agroscope, Reckenholzstrasse 191, CH-8046, Zürich, Switzerland.

The soil microbiome is highly diverse and comprises up to one quarter of Earth's diversity. Yet, how such a diverse and functionally complex microbiome influences ecosystem functioning remains unclear. Here we manipulated the soil microbiome in experimental grassland ecosystems and observed that microbiome diversity and microbial network complexity positively influenced multiple ecosystem functions related to nutrient cycling (e.g. multifunctionality). Grassland microcosms with poorly developed microbial networks and reduced microbial richness had the lowest multifunctionality due to fewer taxa present that support the same function (redundancy) and lower diversity of taxa that support different functions (reduced  functional uniqueness). Moreover, different microbial taxa explained different ecosystem functions pointing to the significance of functional diversity in microbial communities. These findings indicate the importance of microbial interactions within and among fungal and bacterial communities for enhancing ecosystem performance and demonstrate that the extinction of complex ecological associations belowground can impair ecosystem functioning.
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http://dx.doi.org/10.1038/s41467-019-12798-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813331PMC
October 2019

Drought modulates interactions between arbuscular mycorrhizal fungal diversity and barley genotype diversity.

Sci Rep 2019 07 4;9(1):9650. Epub 2019 Jul 4.

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.

Droughts associated with climate change alter ecosystem functions, especially in systems characterized by low biodiversity, such as agricultural fields. Management strategies aimed at buffering climate change effects include the enhancement of intraspecific crop diversity as well as the diversity of beneficial interactions with soil biota, such as arbuscular mycorrhizal fungi (AMF). However, little is known about reciprocal relations of crop and AMF diversity under drought conditions. To explore the interactive effects of plant genotype richness and AMF richness on plant yield under ambient and drought conditions, we established fully crossed diversity gradients in experimental microcosms. We expected highest crop yield and drought tolerance at both high barley and AMF diversity. While barley richness and AMF richness altered the performance of both barley and AMF, they did not mitigate detrimental drought effects on the plant and AMF. Root biomass increased with mycorrhiza colonization rate at high AMF richness and low barley richness. AMF performance increased under higher richness of both barley and AMF. Our findings indicate that antagonistic interactions between barley and AMF may occur under drought conditions, particularly so at higher AMF richness. These results suggest that unexpected alterations of plant-soil biotic interactions could occur under climate change.
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http://dx.doi.org/10.1038/s41598-019-45702-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6609766PMC
July 2019

Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism.

New Phytol 2019 07 13;223(2):867-881. Epub 2019 Apr 13.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, 3508 TB, Utrecht, the Netherlands.

Approximately 29% of all vascular plant species are unable to establish an arbuscular mycorrhizal (AM) symbiosis. Despite this, AM fungi (Rhizophagus spp.) are enriched in the root microbiome of the nonhost Arabidopsis thaliana, and Arabidopsis roots become colonized when AM networks nurtured by host plants are available. Here, we investigated the nonhost-AM fungus interaction by analyzing transcriptional changes in Rhizophagus, Arabidopsis and the host plant Medicago truncatula while growing in the same mycorrhizal network. In early interaction stages, Rhizophagus activated the Arabidopsis strigolactone biosynthesis genes CCD7 and CCD8, suggesting that detection of AM fungi is not completely impaired. However, in colonized Arabidopsis roots, fungal nutrient transporter genes GintPT, GintAMT2, GintMST2 and GintMST4, essential for AM symbiosis, were not activated. RNA-seq transcriptome analysis pointed to activation of costly defenses in colonized Arabidopsis roots. Moreover, Rhizophagus colonization caused a 50% reduction in shoot biomass, but also led to enhanced systemic immunity against Botrytis cinerea. This suggests that early signaling between AM fungi and Arabidopsis is not completely impaired and that incompatibility appears at later interaction stages. Moreover, Rhizophagus-mediated defenses coincide with reduced Arabidopsis growth, but also with systemic disease resistance, highlighting the multifunctional role of AM fungi in host and nonhost interactions.
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http://dx.doi.org/10.1111/nph.15798DOI Listing
July 2019

Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots.

ISME J 2019 07 8;13(7):1722-1736. Epub 2019 Mar 8.

Agroscope, Department of Agroecology & Environment, Reckenholzstrasse 191, 8046, Zürich, Switzerland.

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 (R = 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.
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http://dx.doi.org/10.1038/s41396-019-0383-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6591126PMC
July 2019

The impact of long-term organic farming on soil-derived greenhouse gas emissions.

Sci Rep 2019 02 8;9(1):1702. Epub 2019 Feb 8.

Department of Soil Sciences, Research Institute of Organic Agriculture (FiBL), Ackerstrasse, CH-5070, Frick, Switzerland.

Agricultural practices contribute considerably to emissions of greenhouse gases. So far, knowledge on the impact of organic compared to non-organic farming on soil-derived nitrous oxide (NO) and methane (CH) emissions is limited. We investigated NO and CH fluxes with manual chambers during 571 days in a grass-clover- silage maize - green manure cropping sequence in the long-term field trial "DOK" in Switzerland. We compared two organic farming systems - biodynamic (BIODYN) and bioorganic (BIOORG) - with two non-organic systems - solely mineral fertilisation (CONMIN) and mixed farming including farmyard manure (CONFYM) - all reflecting Swiss farming practices-together with an unfertilised control (NOFERT). We observed a 40.2% reduction of NO emissions per hectare for organic compared to non-organic systems. In contrast to current knowledge, yield-scaled cumulated NO emissions under silage maize were similar between organic and non-organic systems. Cumulated on area scale we recorded under silage maize a modest CH uptake for BIODYN and CONMIN and high CH emissions for CONFYM. We found that, in addition to N input, quality properties such as pH, soil organic carbon and microbial biomass significantly affected NO emissions. This study showed that organic farming systems can be a viable measure contributing to greenhouse gas mitigation in the agricultural sector.
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http://dx.doi.org/10.1038/s41598-018-38207-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6368562PMC
February 2019

Why farmers should manage the arbuscular mycorrhizal symbiosis.

New Phytol 2019 05 18;222(3):1171-1175. Epub 2019 Jan 18.

Institute of Biology, Freie Universität Berlin, Altensteinstr. 6, D-14195, Berlin, Germany.

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http://dx.doi.org/10.1111/nph.15602DOI Listing
May 2019

Reply to 'Can we predict microbial keystones?'

Nat Rev Microbiol 2019 03;17(3):194

Plant-Soil Interactions, Department of Agroecology and Environment, Agroscope, Reckenholz, Zürich, Switzerland.

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http://dx.doi.org/10.1038/s41579-018-0133-xDOI Listing
March 2019

Linking microbial co-occurrences to soil ecological processes across a woodland-grassland ecotone.

Ecol Evol 2018 Aug 22;8(16):8217-8230. Epub 2018 Jul 22.

CSIRO Agriculture and Food Canberra ACT Australia.

Ecotones between distinct ecosystems have been the focus of many studies as they offer valuable insights into key drivers of community structure and ecological processes that underpin function. While previous studies have examined a wide range of above-ground parameters in ecotones, soil microbial communities have received little attention. Here we investigated spatial patterns, composition, and co-occurrences of archaea, bacteria, and fungi, and their relationships with soil ecological processes across a woodland-grassland ecotone. Geostatistical kriging and network analysis revealed that the community structure and spatial patterns of soil microbiota varied considerably between three habitat components across the ecotone. Woodland samples had significantly higher diversity of archaea while the grassland samples had significantly higher diversity of bacteria. Microbial co-occurrences reflected differences in soil properties and ecological processes. While microbial networks were dominated by bacterial nodes, different ecological processes were linked to specific microbial guilds. For example, soil phosphorus and phosphatase activity formed the largest clusters in their respective networks, and two lignolytic enzymes formed joined clusters. Bacterial ammonia oxidizers were dominant over archaeal oxidizers and showed a significant association ( < 0.001) with potential nitrification (PNR), with the PNR subnetwork being dominated by . The top ten keystone taxa comprised six bacterial and four fungal OTUs, with Random Forest Analysis revealing soil carbon and nitrogen as the determinants of the abundance of keystone taxa. Our results highlight the importance of assessing interkingdom associations in soil microbial networks. Overall, this study shows how ecotones can be used as a model to delineate microbial structural patterns and ecological processes across adjoining land-uses within a landscape.
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http://dx.doi.org/10.1002/ece3.4346DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145019PMC
August 2018

A global meta-analysis of yield stability in organic and conservation agriculture.

Nat Commun 2018 09 7;9(1):3632. Epub 2018 Sep 7.

Plant-Soil-Interactions, Research Division Agroecology and Environment, Agroscope, CH 8046, Zurich, Switzerland.

One of the primary challenges of our time is to enhance global food production and security. Most assessments in agricultural systems focus on plant yield. Yet, these analyses neglect temporal yield stability, or the variability and reliability of production across years. Here we perform a meta-analysis to assess temporal yield stability of three major cropping systems: organic agriculture and conservation agriculture (no-tillage) vs. conventional agriculture, comparing 193 studies based on 2896 comparisons. Organic agriculture has, per unit yield, a significantly lower temporal stability (-15%) compared to conventional agriculture. Thus, although organic farming promotes biodiversity and is generally more environmentally friendly, future efforts should focus on reducing its yield variability. Our analysis further indicates that the use of green manure and enhanced fertilisation can reduce the yield stability gap between organic and conventional agriculture. The temporal stability (-3%) of no-tillage does not differ significantly from those of conventional tillage indicating that a transition to no-tillage does not affect yield stability.
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http://dx.doi.org/10.1038/s41467-018-05956-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128901PMC
September 2018

Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota.

Nat Commun 2018 07 16;9(1):2738. Epub 2018 Jul 16.

Institute of Plant Sciences, University of Bern, 3013, Bern, Switzerland.

By changing soil properties, plants can modify their growth environment. Although the soil microbiota is known to play a key role in the resulting plant-soil feedbacks, the proximal mechanisms underlying this phenomenon remain unknown. We found that benzoxazinoids, a class of defensive secondary metabolites that are released by roots of cereals such as wheat and maize, alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next plant generation. Complementation experiments demonstrate that the benzoxazinoid breakdown product 6-methoxy-benzoxazolin-2-one (MBOA), which accumulates in the soil during the conditioning phase, is both sufficient and necessary to trigger the observed phenotypic changes. Sterilization, fungal and bacterial profiling and complementation experiments reveal that MBOA acts indirectly by altering root-associated microbiota. Our results reveal a mechanism by which plants determine the composition of rhizosphere microbiota, plant performance and plant-herbivore interactions of the next generation.
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http://dx.doi.org/10.1038/s41467-018-05122-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048113PMC
July 2018

Impact of organic and conventional farming systems on wheat grain uptake and soil bioavailability of zinc and cadmium.

Sci Total Environ 2018 Oct 26;639:608-616. Epub 2018 May 26.

Soil Protection, Institute of Terrestrial Ecosystems, ETH Zürich, Universitätstrasse 16, 8092 Zurich, Switzerland. Electronic address:

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http://dx.doi.org/10.1016/j.scitotenv.2018.05.187DOI Listing
October 2018

Keystone taxa as drivers of microbiome structure and functioning.

Nat Rev Microbiol 2018 09;16(9):567-576

Department of Agroecology and Environment, Agroscope, Zurich, Switzerland.

Microorganisms have a pivotal role in the functioning of ecosystems. Recent studies have shown that microbial communities harbour keystone taxa, which drive community composition and function irrespective of their abundance. In this Opinion article, we propose a definition of keystone taxa in microbial ecology and summarize over 200 microbial keystone taxa that have been identified in soil, plant and marine ecosystems, as well as in the human microbiome. We explore the importance of keystone taxa and keystone guilds for microbiome structure and functioning and discuss the factors that determine their distribution and activities.
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http://dx.doi.org/10.1038/s41579-018-0024-1DOI Listing
September 2018

Non-Mycorrhizal Plants: The Exceptions that Prove the Rule.

Trends Plant Sci 2018 07 9;23(7):577-587. Epub 2018 May 9.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, PO Box 800.56, 3508 TB Utrecht, The Netherlands; These two authors are shared last authors. Electronic address:

The widespread symbiotic interaction between plants and arbuscular mycorrhizal (AM) fungi relies on a complex molecular dialog with reciprocal benefits in terms of nutrition, growth, and protection. Approximately 29% of all vascular plant species do not host AM symbiosis, including major crops. Under certain conditions, however, presumed non-host plants can become colonized by AM fungi and develop rudimentary AM (RAM) phenotypes. Here we zoom in on the mustard family (Brassicaceae), which harbors AM hosts, non-hosts, and presumed non-host species such as Arabidopsis thaliana, for which conditional RAM colonization has been described. We advocate that RAM phenotypes and redundant genomic elements of the symbiotic 'toolkit' are missing links that can help to unravel genetic constraints that drive the evolution of symbiotic incompatibility.
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http://dx.doi.org/10.1016/j.tplants.2018.04.004DOI Listing
July 2018

Conservation tillage and organic farming induce minor variations in Pseudomonas abundance, their antimicrobial function and soil disease resistance.

FEMS Microbiol Ecol 2018 08;94(8)

ETH Zürich, Plant Pathology, Institute of Integrative Biology, Universitätsstrasse 2, 8092 Zürich, Switzerland.

Conservation tillage and organic farming are strategies used worldwide to preserve the stability and fertility of soils. While positive effects on soil structure have been extensively reported, the effects on specific root- and soil-associated microorganisms are less known. The aim of this study was to investigate how conservation tillage and organic farming influence the frequency and activity of plant-beneficial pseudomonads. Amplicon sequencing using the 16S rRNA gene revealed that Pseudomonas is among the most abundant bacterial taxa in the root microbiome of field-grown wheat, independent of agronomical practices. However, pseudomonads carrying genes required for the biosynthesis of specific antimicrobial compounds were enriched in samples from conventionally farmed plots without tillage. In contrast, disease resistance tests indicated that soil from conventional no tillage plots is less resistant to the soilborne pathogen Pythium ultimum compared to soil from organic reduced tillage plots, which exhibited the highest resistance of all compared cropping systems. Reporter strain-based gene expression assays did not reveal any differences in Pseudomonas antimicrobial gene expression between soils from different cropping systems. Our results suggest that plant-beneficial pseudomonads can be favoured by certain soil cropping systems, but soil resistance against plant diseases is likely determined by a multitude of biotic factors in addition to Pseudomonas.
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http://dx.doi.org/10.1093/femsec/fiy075DOI Listing
August 2018

Correction to: Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming.

Microbiome 2018 04 24;6(1):74. Epub 2018 Apr 24.

Plant-Soil Interactions, Department of Agroecology and Environment, Agroscope, Zurich, Switzerland.

Following publication of the original article [1], the authors reported that while the ordination graphs are all correct, the symbols in the legend are wrong.
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http://dx.doi.org/10.1186/s40168-018-0456-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5913793PMC
April 2018

Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming.

Microbiome 2018 01 16;6(1):14. Epub 2018 Jan 16.

Plant-Soil Interactions, Department of Agroecology and Environment, Agroscope, Zurich, Switzerland.

Background: Harnessing beneficial microbes presents a promising strategy to optimize plant growth and agricultural sustainability. Little is known to which extent and how specifically soil and plant microbiomes can be manipulated through different cropping practices. Here, we investigated soil and wheat root microbial communities in a cropping system experiment consisting of conventional and organic managements, both with different tillage intensities.

Results: While microbial richness was marginally affected, we found pronounced cropping effects on community composition, which were specific for the respective microbiomes. Soil bacterial communities were primarily structured by tillage, whereas soil fungal communities responded mainly to management type with additional effects by tillage. In roots, management type was also the driving factor for bacteria but not for fungi, which were generally determined by changes in tillage intensity. To quantify an "effect size" for microbiota manipulation, we found that about 10% of variation in microbial communities was explained by the tested cropping practices. Cropping sensitive microbes were taxonomically diverse, and they responded in guilds of taxa to the specific practices. These microbes also included frequent community members or members co-occurring with many other microbes in the community, suggesting that cropping practices may allow manipulation of influential community members.

Conclusions: Understanding the abundance patterns of cropping sensitive microbes presents the basis towards developing microbiota management strategies for smart farming. For future targeted microbiota management-e.g., to foster certain microbes with specific agricultural practices-a next step will be to identify the functional traits of the cropping sensitive microbes.
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http://dx.doi.org/10.1186/s40168-017-0389-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5771023PMC
January 2018

Plant-Soil Feedback: Bridging Natural and Agricultural Sciences.

Trends Ecol Evol 2018 02 11;33(2):129-142. Epub 2017 Dec 11.

Swedish University of Agricultural Sciences, Department of Forest Ecology and Management, 90183, Umeå, Sweden. Electronic address:

In agricultural and natural systems researchers have demonstrated large effects of plant-soil feedback (PSF) on plant growth. However, the concepts and approaches used in these two types of systems have developed, for the most part, independently. Here, we present a conceptual framework that integrates knowledge and approaches from these two contrasting systems. We use this integrated framework to demonstrate (i) how knowledge from complex natural systems can be used to increase agricultural resource-use efficiency and productivity and (ii) how research in agricultural systems can be used to test hypotheses and approaches developed in natural systems. Using this framework, we discuss avenues for new research toward an ecologically sustainable and climate-smart future.
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http://dx.doi.org/10.1016/j.tree.2017.11.005DOI Listing
February 2018

Community Profiling of in Combination with Other Plant-Associated Fungi in Different Crop Species Using SMRT Sequencing.

Front Plant Sci 2017 28;8:2019. Epub 2017 Nov 28.

Plant-Soil Interactions, Research Division Agroecology and Environment, Agroscope, Zurich, Switzerland.

Fusarium head blight, caused by fungi from the genus , is one of the most harmful cereal diseases, resulting not only in severe yield losses but also in mycotoxin contaminated and health-threatening grains. Fusarium head blight is caused by a diverse set of species that have different host ranges, mycotoxin profiles and responses to agricultural practices. Thus, understanding the composition of communities in the field is crucial for estimating their impact and also for the development of effective control measures. Up to now, most molecular tools that monitor communities on plants are limited to certain species and do not distinguish other plant associated fungi. To close these gaps, we developed a sequencing-based community profiling methodology for crop-associated fungi with a focus on the genus . By analyzing a 1600 bp long amplicon spanning the highly variable segments ITS and D1-D3 of the ribosomal operon by PacBio SMRT sequencing, we were able to robustly quantify down to species level through clustering against reference sequences. The newly developed methodology was successfully validated in mock communities and provided similar results as the culture-based assessment of communities by seed health tests in grain samples from different crop species. Finally, we exemplified the newly developed methodology in a field experiment with a wheat-maize crop sequence under different cover crop and tillage regimes. We analyzed wheat straw residues, cover crop shoots and maize grains and we could reveal that the cover crop hairy vetch () acts as a potent alternative host for (OTU ) showing an eightfold higher relative abundance compared with other cover crop treatments. Moreover, as the newly developed methodology also allows to trace other crop-associated fungi, we found that vetch and green fallow hosted further fungal plant pathogens including . Thus, besides their beneficial traits, cover crops can also entail phytopathological risks by acting as alternative hosts for and other noxious plant pathogens. The newly developed sequencing based methodology is a powerful diagnostic tool to trace in combination with other fungi associated to different crop species.
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http://dx.doi.org/10.3389/fpls.2017.02019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5712420PMC
November 2017

Combined Field Inoculations of Bacteria, Arbuscular Mycorrhizal Fungi, and Entomopathogenic Nematodes and their Effects on Wheat Performance.

Front Plant Sci 2017 31;8:1809. Epub 2017 Oct 31.

FARCE Laboratory, University of Neuchâtel, Neuchâtel, Switzerland.

In agricultural ecosystems, pest insects, pathogens, and reduced soil fertility pose major challenges to crop productivity and are responsible for significant yield losses worldwide. Management of belowground pests and diseases remains particularly challenging due to the complex nature of the soil and the limited reach of conventional agrochemicals. Boosting the presence of beneficial rhizosphere organisms is a potentially sustainable alternative and may help to optimize crop health and productivity. Field application of single beneficial soil organisms has shown satisfactory results under optimal conditions. This might be further enhanced by combining multiple beneficial soil organisms, but this remains poorly investigated. Here, we inoculated wheat plots with combinations of three beneficial soil organisms that have different rhizosphere functions and studied their effects on crop performance. Plant beneficial bacteria, arbuscular mycorrhizal fungi (AMF), and entomopathogenic nematodes (EPN), were inoculated individually or in combinations at seeding, and their effects on plant performance were evaluated throughout the season. We used traditional and molecular identification tools to monitor their persistence over the cropping season in augmented and control treatments, and to estimate the possible displacement of native populations. In three separate trials, beneficial soil organisms were successfully introduced into the native populations and readily survived the field conditions. Various , mycorrhiza, and nematode treatments improved plant health and productivity, while their combinations provided no significant additive or synergistic benefits compared to when applied alone. EPN application temporarily displaced some of the native EPN, but had no significant long-term effect on the associated food web. The strongest positive effect on wheat survival was observed for and AMF during a season with heavy natural infestation by the frit fly, , a major pest of cereals. Hence, beneficial impacts differed between the beneficial soil organisms and were most evident for plants under biotic stress. Overall, our findings indicate that in wheat production under the test conditions the three beneficial soil organisms can establish nicely and are compatible, but their combined application provides no additional benefits. Further studies are required, also in other cropping systems, to fine-tune the functional interactions among beneficial soil organisms, crops, and the environment.
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http://dx.doi.org/10.3389/fpls.2017.01809DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5671467PMC
October 2017

Detecting macroecological patterns in bacterial communities across independent studies of global soils.

Nat Microbiol 2018 02 20;3(2):189-196. Epub 2017 Nov 20.

Natural England, Exeter, UK.

The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential 'indicator' taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.
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http://dx.doi.org/10.1038/s41564-017-0062-xDOI Listing
February 2018

Continuum of root-fungal symbioses for plant nutrition.

Proc Natl Acad Sci U S A 2017 10 23;114(44):11574-11576. Epub 2017 Oct 23.

Plant-Soil Interactions, Division of Agroecology and Environment, Agroscope, 8046 Zurich, Switzerland;

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http://dx.doi.org/10.1073/pnas.1716329114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5676940PMC
October 2017

Symbiotic soil fungi enhance ecosystem resilience to climate change.

Glob Chang Biol 2017 12 11;23(12):5228-5236. Epub 2017 Jul 11.

Plant-Soil Interactions, Research Division of Agroecology and Environmental Science, Agroscope, CH - 8046, Zürich, Switzerland.

Substantial amounts of nutrients are lost from soils through leaching. These losses can be environmentally damaging, causing groundwater eutrophication and also comprise an economic burden in terms of lost agricultural production. More intense precipitation events caused by climate change will likely aggravate this problem. So far it is unresolved to which extent soil biota can make ecosystems more resilient to climate change and reduce nutrient leaching losses when rainfall intensity increases. In this study, we focused on arbuscular mycorrhizal (AM) fungi, common soil fungi that form symbiotic associations with most land plants and which increase plant nutrient uptake. We hypothesized that AM fungi mitigate nutrient losses following intensive precipitation events (higher amount of precipitation and rain events frequency). To test this, we manipulated the presence of AM fungi in model grassland communities subjected to two rainfall scenarios: moderate and high rainfall intensity. The total amount of nutrients lost through leaching increased substantially with higher rainfall intensity. The presence of AM fungi reduced phosphorus losses by 50% under both rainfall scenarios and nitrogen losses by 40% under high rainfall intensity. Thus, the presence of AM fungi enhanced the nutrient interception ability of soils, and AM fungi reduced the nutrient leaching risk when rainfall intensity increases. These findings are especially relevant in areas with high rainfall intensity (e.g., such as the tropics) and for ecosystems that will experience increased rainfall due to climate change. Overall, this work demonstrates that soil biota such as AM fungi can enhance ecosystem resilience and reduce the negative impact of increased precipitation on nutrient losses.
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http://dx.doi.org/10.1111/gcb.13785DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5697572PMC
December 2017