skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.


Title: Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
Abstract

Plants deploy both primary and species-specific, specialized metabolites to communicate with other organisms and adapt to environmental challenges, including interactions with soil-dwelling microbial communities. However, the role of specialized metabolites in modulating plant-microbiome interactions often remains elusive. In this study, we report that maize (Zea mays) diterpenoid metabolites with known antifungal bioactivities also influence rhizosphere bacterial communities. Metabolite profiling showed that dolabralexins, antibiotic diterpenoids that are highly abundant in roots of some maize varieties, can be exuded from the roots. Comparative 16S rRNA gene sequencing determined the bacterial community composition of the maize mutantZman2(anther ear 2), which is deficient in dolabralexins and closely related bioactive kauralexin diterpenoids. TheZman2rhizosphere microbiome differed significantly from the wild-type sibling with the most significant changes observed for Alphaproteobacteria of the order Sphingomonadales. Metabolomics analyses support that these differences are attributed to the diterpenoid deficiency of theZman2mutant, rather than other large-scale metabolome alterations. Together, these findings support physiological functions of maize diterpenoids beyond known chemical defenses, including the assembly of the rhizosphere microbiome.

 
more » « less
Award ID(s):
1758976
NSF-PAR ID:
10360672
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
11
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Root exudates shape the rhizosphere microbiome, but little is known about the specific compounds in root exudates that are important. Here, we investigated the impacts of the plant-synthesized phytohormones indole-3-acetic acid (IAA) and abscisic acid (ABA) exuded by roots on the maize rhizobacterial communities. To identify maize genotypes that differed in the root exudate concentrations of IAA and ABA, we screened hundreds of inbred lines using a semi-hydroponic system. Twelve genotypes with variable exudate concentrations of IAA and ABA were selected for a replicated field experiment. Bulk soil, rhizosphere, and root endosphere samples were collected at two vegetative and one reproductive maize developmental stage. IAA and ABA concentrations in rhizosphere samples were quantified by liquid chromatography–mass spectrometry. The bacterial communities were analyzed by V4 16S rRNA amplicon sequencing. Results indicated that IAA and ABA concentrations in root exudates significantly affected the rhizobacterial communities at specific developmental stages. ABA impacted the rhizosphere bacterial communities at later developmental stages, whereas IAA affected the rhizobacterial communities at the vegetative stages. This study contributed to our knowledge about the influence that specific root exudate compounds have on the rhizobiome composition, showing that the phytohormones IAA and ABA exuded by roots have a role in the plant–microbiome interactions.

     
    more » « less
  2. Hom, Erik F. (Ed.)
    ABSTRACT

    Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory toFerrovibriumand tested Firmicutes. While fungal isolates ofPenicilliumandPericoniawere also more inhibited by higher concentrations (200 µM) of nerolidol,Clonostachyswas enhanced at this higher level and together withHumicolawas inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect onOrbiliaat both tested concentrations but had a promotive effect at 100 µM onPenicilliumandPericonia. Similarly, linalool at 100 µM had significant growth promotion inMortierella, but an inhibitory effect forOrbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome.

    Importance

    Terpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a “rhizobox” mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production.

     
    more » « less
  3. Arias, Renee S. (Ed.)
    ABSTRACT

    Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.

    IMPORTANCE

    In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.

     
    more » « less
  4. Summary

    Soil communities are diverse taxonomically and functionally. This ecosystem experiences highly complex networks of interactions, but may also present functionally independent entities. Plant roots, a metabolically active hotspot in the soil, take an essential part in below‐ground interactions. While plants are known to release an extremely high portion of the fixated carbon to the soil, less information is known about the composition and role of C‐containing compounds in the rhizosphere, in particular those involved in chemical communication. Specialized metabolites (or secondary metabolites) produced by plants and their associated microbes have a critical role in various biological activities that modulate the behavior of neighboring organisms. Thus, elucidating the chemical composition and function of specialized metabolites in the rhizosphere is a key element in understanding interactions in this below‐ground environment. Here, we review key classes of specialized metabolites that occur as mostly non‐volatile compounds in root exudates or are emitted as volatile organic compounds (VOCs). The role of these metabolites in below‐ground interactions and response to nutrient deficiency, as well as their tissue and cell type‐specific biosynthesis and release are discussed in detail.

     
    more » « less
  5. Abstract

    The rhizosphere microbiome influences many aspects of plant fitness, including production of secondary compounds and defence against insect herbivores. Plants also modulate the composition of the microbial community in the rhizosphere via secretion of root exudates. We tested both the effect of the rhizosphere microbiome on plant traits, and host plant effects on rhizosphere microbes using recombinant inbred lines (RILs) ofBrassica rapathat differ in production of glucosinolates (GLS), secondary metabolites that contribute to defence against insect herbivores. First, we investigated the effect of genetic variation in GLS production on the composition of the rhizosphere microbiome. Using a Bayesian Dirichlet‐multinomial regression model (DMBVS), we identified both negative and positive associations between bacteria from six genera and the concentration of five GLS compounds produced in plant roots. Additionally, we tested the effects of microbial inoculation (an intact vs. disrupted soil microbiome) on GLS production and insect damage in these RILs. We found a significant microbial treatment × genotype interaction, in which total GLS was higher in the intact relative to the disrupted microbiome treatment in some RILs. However, despite differences in GLS production between microbial treatments, we observed no difference in insect damage between treatments. Together, these results provide evidence for a full feedback cycle of plant–microbe interactions mediated by GLS; that is, GLS compounds produced by the host plant “feed‐down” to influence rhizosphere microbial community and rhizosphere microbes “feed‐up” to influence GLS production.

     
    more » « less