Although the importance of the soil microbiome in mediating plant community structures and functions has been increasingly emphasized in ecological studies, the biological processes driving crop diversity overyielding remain unexplained in agriculture. Based on the plant–soil feedback (PSF) theory and method, we quantified to what extent and how soil microbes contributed to intercropping overyielding. Soils were collected as inocula and sequenced from a unique 10‐year field experiment, consisting of monoculture, intercropping and rotation planted with wheat ( In wheat & faba bean (W&F) and maize & faba bean (M&F) systems, soil microbes drove intercropping overyielding compared to monoculture, with 28%–51% of the overyielding contributed by microbial legacies. The overyielding effects resulted from negative PSFs in both systems, as crops, in particular faba bean grew better in soils conditioned by other crops than itself. Moreover, faba bean grew better in soils from intercropping or rotation than from the average of monocultures, indicating a strong positive legacy effect of multispecies cropping systems. However, with positive PSF and negative legacy benefit effect of intercropping/rotation, we did not observe significant overyielding in the W&M system. With more bacterial and fungal dissimilarities by metabarcoding in heterospecific than its own soil, the better it improved faba bean growth. More detailed analysis showed faba bean monoculture soil accumulated more putative pathogens with higher
Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination. We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs. We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.
- Award ID(s):
- 1655972
- NSF-PAR ID:
- 10460299
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 9
- Issue:
- 16
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 9298-9311
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Triticum aestivum) , maize (Zea mays) or faba bean (Vicia faba ). A PSF greenhouse study was conducted to test microbial effects on three crops' growth in monoculture or intercropping.Fusarium relative abundance and moreFusarium oxysporum gene copies by qPCR, while in heterospecific soils, there were less pathogenic effects when cereals were engaged. Further analysis in maize/faba bean intercropping also showed an increase of rhizobia relative abundance.Synthesis and applications . Our results demonstrate a soil microbiome‐mediated advantage in intercropping through suppression of the negative PSF of pathogens and increasing beneficial microbes. As microbial mediation of overyielding is context‐dependent, we conclude that the dynamics of both beneficial and pathogenic microbes should be considered in designing cropping systems for sustainable agriculture, particularly including combinations of legumes and cereals. -
more » « less
Abstract Previous theoretical work has highlighted the potential for natural enemies to mediate the coexistence of species with similar life histories via density‐dependent effects on survivorship. For plant pathogens to play this role, they must differ in their ability to infect or induce disease in different host plant species. In tropical forests characterized by high diversity, these effects must extend to phylogenetically closely related species pairs. Mortality at the seed and seedling stage strongly influences the abundance and distribution of tropical tree species, but the host preferences and spatial distributions of fungi are rarely determined.
We examined how host species identity, relatedness and seed viability influence the composition of fungal communities associated with seeds of four co‐occurring pioneer trees (
Cecropia insignis ,C. longipes ,C. peltata andJacaranda copaia ). Seeds were buried in mesh bags in five common gardens in the understorey of a lowland tropical forest in Panama and retrieved at intervals from 1 to 30 months. A subset of the seeds in each bag was used to determine germination success. One half of each remaining seed was tested for viability; and the other half was used to culture and identify seed‐infecting fungi.Seeds were infected by fungi after burial. Although fungal communities differed in viable versus dead seeds, and across burial locations, community composition primarily varied as a function of plant species identity (30.7% of variation in community composition vs. 4.5% for viability and location together), even for congeneric
Cecropia species. Phylogenetic reconstruction showed that relatedness of fungi mostly reflected differences betweenJacaranda (Bignoniaceae) andCecropia (Urticaceae).Although the proportion of germinable seeds decreased gradually over time for all species, intraspecific variation in survival was high at the same location (e.g. ranging from 0% to 100% for
C. peltata ) suggesting variable exposure or susceptibility to seed pathogens.Synthesis . Our study provides evidence under field conditions that congeneric tree species with similar life history traits differ markedly in seed‐associated fungal communities when exposed to the same soil‐borne fungi. This is a critical first step supporting pathogen‐mediated coexistence of closely related tree species. -
more » « less
Abstract Plants affect associated biotic and abiotic edaphic factors, with reciprocal feedbacks from soil characteristics affecting plants. These two‐way interactions between plants and soils are collectively known as plant–soil feedbacks (PSFs). The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of PSFs, although the strength and direction of feedbacks among sympatric congeners are not well‐understood. We examined plant–soil feedback responses of
Asclepias syriaca , a common clonal milkweed species, with several sympatric congeners across a gradient of increasing phylogenetic distances (A. tuberosa ,A. viridis ,A. sullivantii , andA. verticillata , respectively). Plant–soil feedbacks were measured through productivity and colonization by arbuscular mycorrhizal (AM) fungi.Asclepias syriaca produced less biomass in soils conditioned by the most phylogenetically distant species (A. verticillata ), relative to conspecific‐conditioned soils. Similarly, arbuscular mycorrhizal (AM) fungal colonization ofA. syriaca roots was reduced when grown in soils conditioned byA. verticillata , compared with colonization in plants grown in soil conditioned by any of the other threeAsclepias species, indicating mycorrhizal associations are a potential mechanism of observed positive PSFs. This display of differences between the most phylogenetically distant, but not close or intermediate, paring(s) suggests a potential phylogenetic threshold, although other exogenous factors cannot be ruled out. Overall, these results highlight the potential role of phylogenetic distance in influencing positive PSFs through mutualists. The role of phylogenetic relatedness and evolutionary histories have recently emerged as a potential driver of plant–soil feedbacks (PSFs), although the strength and direction of feedbacks among sympatric congeners are not well‐understood. Congeneric, sympatric milkweeds typically generated positive PSFs in terms of productivity and AM fungal colonization, suggesting the low likelihood of coexistence among tested pairs, with a strength of feedback increasing as the phylogenetic distance increases. -
Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relativesmore » « less
Abstract Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships.
To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory by
Manduca sexta , and the attraction of a parasitoid wasp,Cotesia congregata .Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks.
Plant cultivars had different levels of resistance to herbivory by
M. sexta , but this did not depend on plant domestication or soil type. The parasitoidC. congregata was primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil.Synthesis. These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions. -
more » « less
Abstract Pioneer trees require high‐light environments for successful seedling establishment. Consequently, seeds of these species often persist in the soil seed bank (SSB) for periods ranging from several weeks to decades. How they survive despite extensive pressure from seed predators and soil‐borne pathogens remains an intriguing question.
This study aims to test the hypotheses that decades‐old seeds collected from the SSB in a lowland tropical forest remain viable by (i) escaping infection by fungi, which are major drivers of seed mortality in tropical soils, and/or (ii) maintaining high levels of seed dormancy and seed coat integrity when compared to inviable seeds.
We collected seeds of
Trema micrantha andZanthoxylum ekmanii at Barro Colorado Island, Panama, from sites where adult trees previously occurred in the past 30 years. We used carbon dating to measure seed age and characterized seed coat integrity, seed dormancy and fungal communities.Viable seeds from the SSB ranged in age from 9 to 30 years for
T. micrantha , and 5 to 33 years forZ. ekmanii . We found no evidence that decades‐old seeds maintain high levels of seed dormancy or seed coat integrity. Fungi were rarely detected in fresh seeds (no soil contact), but phylogenetically diverse fungi were detected often in seeds from the SSB. Although fungal infections were more commonly detected in inviable seeds than in viable seeds, a lack of differences in fungal diversity and community composition between viable and inviable seeds suggested that viable seeds are not simply excluding fungal species to survive long periods in the SSB.Synthesis. Our findings reveal the importance of a previously understudied aspect of seed survival, where the impact of seed–microbial interactions may be critical to understand long‐term persistence in the SSB.Read the free
Plain Language Summary for this article on the Journal blog.
