skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Acid or base? How do plants regulate the ecology of their phylloplane?
Abstract Plants interface with and modify the external environment across their surfaces, and in so doing, can control or mitigate the impacts of abiotic stresses and also mediate their interactions with other organisms. Botanically, it is known that plant roots have a multi-faceted ability to modify rhizosphere conditions like pH, a factor with a large effect on a plant’s biotic interactions with microbes. But plants can also modify pH levels on the surfaces of their leaves. Plants can neutralize acid rain inputs in a period of hours, and either acidify or alkalinize the pH of neutral water droplets in minutes. The pH of the phylloplane—that is, the outermost surface of the leaf—varies across species, from incredibly acidic (carnivorous plants: as low as pH 1) to exceptionally alkaline (species in the plant family, Malvaceae, up to pH 11). However, most species mildly acidify droplets on the phylloplane by 1.5 orders of magnitude in pH. Just as rhizosphere pH helps shape the plant microbiome and is known to influence belowground interactions, so too can phylloplane pH influence aboveground interactions in plant canopies. In this review, we discuss phylloplane pH regulation from the physiological, molecular, evolutionary, and ecological perspectives and address knowledge gaps and identify future research directions.  more » « less
Award ID(s):
2030871
PAR ID:
10296144
Author(s) / Creator(s):
;
Editor(s):
Crous, Kristine
Date Published:
Journal Name:
AoB PLANTS
Volume:
13
Issue:
4
ISSN:
2041-2851
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. null (Ed.)
    Abstract 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. 
    more » « less
  3. Heck, Michelle (Ed.)
    ABSTRACT Plant-associated microbial assemblages are known to shift at time scales aligned with plant phenology, as influenced by the changes in plant-derived nutrient concentrations and abiotic conditions observed over a growing season. But these same factors can change dramatically in a sub-24-hour period, and it is poorly understood how such diel cycling may influence plant-associated microbiomes. Plants respond to the change from day to night via mechanisms collectively referred to as the internal “clock,” and clock phenotypes are associated with shifts in rhizosphere exudates and other changes that we hypothesize could affect rhizosphere microbes. The mustardBoechera strictahas wild populations that contain multiple clock phenotypes of either a 21- or a 24-hour cycle. We grew plants of both phenotypes (two genotypes per phenotype) in incubators that simulated natural diel cycling or that maintained constant light and temperature. Under both cycling and constant conditions, the extracted DNA concentration and the composition of rhizosphere microbial assemblages differed between time points, with daytime DNA concentrations often triple what were observed at night and microbial community composition differing by, for instance, up to 17%. While we found that plants of different genotypes were associated with variation in rhizosphere assemblages, we did not see an effect on soil conditioned by a particular host plant circadian phenotype on subsequent generations of plants. Our results suggest that rhizosphere microbiomes are dynamic at sub-24-hour periods, and those dynamics are shaped by diel cycling in host plant phenotype. IMPORTANCEWe find that the rhizosphere microbiome shifts in composition and extractable DNA concentration in sub-24-hour periods as influenced by the plant host’s internal clock. These results suggest that host plant clock phenotypes could be an important determinant of variation in rhizosphere microbiomes. 
    more » « less
  4. Abstract The rhizosphere has been called “one of the most complex ecosystems on earth” because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed aplant‐centric perspective when trying to harness the potential of microbiome‐derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, amicrobe‐centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context‐dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production. 
    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