skip to main content


Title: Water stress and disruption of mycorrhizas induce parallel shifts in phyllosphere microbiome composition
Summary

Water and nutrient acquisition are key drivers of plant health and ecosystem function. These factors impact plant physiology directly as well as indirectly through soil‐ and root‐associated microbial responses, but how they in turn affect aboveground plant–microbe interactions are not known.

Through experimental manipulations in the field and growth chamber, we examine the interacting effects of water stress, soil fertility, and arbuscular mycorrhizal fungi on bacterial and fungal communities of the tomato (Solanum lycopersicum) phyllosphere.

Both water stress and mycorrhizal disruption reduced leaf bacterial richness, homogenized bacterial community composition among plants, and reduced the relative abundance of dominant fungal taxa. We observed striking parallelism in the individual microbial taxa in the phyllosphere affected by irrigation and mycorrhizal associations.

Our results show that soil conditions and belowground interactions can shape aboveground microbial communities, with important potential implications for plant health and sustainable agriculture.

 
more » « less
NSF-PAR ID:
10367526
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
234
Issue:
6
ISSN:
0028-646X
Page Range / eLocation ID:
p. 2018-2031
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    Allelopathy is a common and important stressor that shapes plant communities and can alter soil microbiomes, yet little is known about the direct effects of allelochemical addition on bacterial and fungal communities or the potential for allelochemical‐selected microbiomes to mediate plant performance responses, especially in habitats naturally structured by allelopathy.

    Here, we present the first community‐wide investigation of microbial mediation of allelochemical effects on plant performance by testing how allelopathy affects soil microbiome structure and how these microbial changes impact germination and productivity across 13 plant species.

    The soil microbiome exhibited significant changes to ‘core’ bacterial and fungal taxa, bacterial composition, abundance of functionally important bacterial and fungal taxa, and predicted bacterial functional genes after the addition of the dominant allelochemical native to this habitat. Furthermore, plant performance was mediated by the allelochemical‐selected microbiome, with allelopathic inhibition of plant productivity moderately mitigated by the microbiome.

    Through our findings, we present a potential framework to understand the strength of plant–microbial interactions in the presence of environmental stressors, in which frequency of the ecological stress may be a key predictor of microbiome‐mediation strength.

     
    more » « less
  2. Summary

    Habitat restoration may depend on the recovery of plant microbial symbionts such as arbuscular mycorrhizal (AM) fungi, but this requires a better understanding of the rules that govern their community assembly.

    We examined the interactions of soil and host‐associated AM fungal communities between remnant and restored patches of subtropical montane forests.

    While AM fungal richness did not differ between habitat types, community membership did and was influenced by geography, habitat and host. These differences were largely driven by rare host‐specific AM fungi that displayed near‐complete turnover between forest types, while core AM fungal taxa were highly abundant and ubiquitous. The bipartite networks in the remnant forest were more specialized and hosts more specific than in the restored forest. Host‐associated AM fungal communities nested within soil communities in both habitats, but only significantly so in the restored forest.

    Our results provide evidence that restored and remnant forests harbour the same core fungal symbionts, while rare host‐specific taxa differ, and that geography, host identity and taxonomic resolution strongly affect the observed distribution patterns of these fungi. We suggest that host‐specific interactions with AM fungi, as well as spatial processes, should be explicitly considered to effectively re‐establish target host and symbiont communities.

     
    more » « less
  3. Abstract

    In recent times, interest has grown in understanding how microbiomes – the collection of microorganisms in a specific environment – influence the survivability or fitness of their plant and animal hosts. The profound diversity of bacterial and fungal species found in certain environments, such as soil, provides a large pool of potential microbial partners that can interact in ways that reveal patterns of associations linking host–microbiome traits developed over time. However, most microbiome sequence data are reported as a community fingerprint, without analysis of interaction networks across microbial taxa through time.

    To address this knowledge gap, more robust tools are needed to account for microbiome dynamics that could signal a beneficial change to a plant or animal host. In this paper, we discuss applying mathematical tools, such as dynamic network modelling, which involves the use of longitudinal data to study system dynamics and microbiomes that identify potential alterations in microbial communities over time in response to an environmental change. In addition, we discuss the potential challenges and pitfalls of these methodologies, such as handling large amounts of sequencing data and accounting for random processes that influence community dynamics, as well as potential ways to address them.

    Ultimately, we argue that components of microbial community interactions can be characterized through mathematical models to reveal insights into complex dynamics associated with a plant or animal host trait. The inclusion of interaction networks in microbiome studies could provide insights into the behaviour of complex communities in tandem with host trait modification and evolution.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  4. Abstract

    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.

    Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.

     
    more » « less
  5. Abstract

    Global climate change and shifting land‐use are increasing plant stress due to abiotic factors such as drought, heat, salinity and cold, as well as via the intensification of biotic stressors such as herbivores and pathogens. The ability of plants to tolerate such stresses is modulated by the bacteria and fungi that live on or inside of plant tissues and comprise the plant microbiome. However, the impacts of diverse classes of beneficial members of the microbiome and the contrasting stresses that impact plants are most commonly studied independently of each other.

    Our meta‐analysis of 288 experiments across 89 studies moves beyond previous studies in that we simultaneously compare the roles of bacterial versus fungal microbiome members that live within plant tissues and colonize plant surfaces in ameliorating biotic versus abiotic sources of plant stress.

    The magnitude of microbial stress amelioration can be measured as the greater proportional impact of beneficial microbes on plant performance in more stressful environments. In the plant experiments we examine, the magnitude of microbial stress amelioration is substantial: it is 23% of the effect size of the typical impact of stress and 56% of the effect size of beneficial microbiome members in the absence of stress.

    The amount of benefit microbiome members confer to plants differs among classes of microbes, depending on whether plants are grown in stressful or non‐stressful environments. In the absence of stress, beneficial bacteria tend to confer greater plant benefits than do fungi. However, symbiotic fungi, especially arbuscular mycorrhizal fungi, more strongly ameliorate plant stress than do bacteria. In particular, beneficial microbes ameliorate salinity, foliar herbivory and fungal pathogen stress.

    These results highlight the fact that the impacts of beneficial and antagonistic components of the microbiome on plant performance depend on biotic and abiotic environmental contexts. Furthermore, beneficial microbes are especially critical for plant health in stressful environments and thus present opportunities to mitigate negative consequences of global change.

    A freeplain language summarycan be found within the Supporting Information of this article.

     
    more » « less