Summary The scope of plant control over its microbiome is a central question in evolutionary biology and agriculture. Leaf traits are known to shape pathogen colonization and disease development, but their impact on the broader community of largely non‐pathogenic fungi that colonize plant leaves remains an open question.We used reciprocal common gardens of the model tree,Populus trichocarpa(black cottonwood), to examine relationships between leaf traits and the leaf mycobiome in two strongly contrasting environments. We measured six leaf traits (stomatal length, stomatal density, carbon‐to‐nitrogen ratio, leaf thickness, leaf dry matter content, and specific leaf area) and used fungal marker gene sequencing to characterize leaf fungal communities for 57 tree genotypes replicated in one mesic and one xeric common garden (809 trees).Several leaf traits covaried with the leaf mycobiome, yet one relationship was paramount: plant genotypes with longer, sparser leaf stomata hosted a greater richness and diversity of more similar fungal species compared to plant genotypes with shorter, denser leaf stomata.These relationships, while modulated by the environment plants were sourced from and grown in, suggest that stomatal traits may be a general mechanism through which plants and the leaf mycobiome influence one another.
more »
« less
Heterosis of leaf and rhizosphere microbiomes in field‐grown maize
Summary Macroorganisms’ genotypes shape their phenotypes, which in turn shape the habitat available to potential microbial symbionts. This influence of host genotype on microbiome composition has been demonstrated in many systems; however, most previous studies have either compared unrelated genotypes or delved into molecular mechanisms. As a result, it is currently unclear whether the heritability of host‐associated microbiomes follows similar patterns to the heritability of other complex traits.We take a new approach to this question by comparing the microbiomes of diverse maize inbred lines and their F1hybrid offspring, which we quantified in both rhizosphere and leaves of field‐grown plants using 16S‐v4 and ITS1 amplicon sequencing.We show that inbred lines and hybrids differ consistently in the composition of bacterial and fungal rhizosphere communities, as well as leaf‐associated fungal communities. A wide range of microbiome features display heterosis within individual crosses, consistent with patterns for nonmicrobial maize phenotypes. For leaf microbiomes, these results were supported by the observation that broad‐sense heritability in hybrids was substantially higher than narrow‐sense heritability.Our results support our hypothesis that at least some heterotic host traits affect microbiome composition in maize.
more »
« less
- Award ID(s):
- 1656006
- PAR ID:
- 10368445
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 228
- Issue:
- 3
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 1055-1069
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Background and AimsNitrogenous fertilizers provide a short-lived benefit to crops in agroecosystems, but stimulate nitrification and denitrification, processes that result in nitrate pollution, N2O production, and reduced soil fertility. Recent advances in plant microbiome science suggest that genetic variation in plants can modulate the composition and activity of rhizosphere N-cycling microorganisms. Here we attempted to determine whether genetic variation exists inZea maysfor the ability to influence the rhizosphere nitrifier and denitrifier microbiome under “real-world” conventional agricultural conditions. MethodsTo capture an extensive amount of genetic diversity within maize we grew and sampled the rhizosphere microbiome of a diversity panel of germplasm that included ex-PVP inbreds (Z. maysssp.mays), ex-PVP hybrids (Z. maysssp.mays), and teosinte (Z. maysssp. mexicanaandZ. maysssp.parviglumis). From these samples, we characterized the microbiome, a suite of microbial genes involved in nitrification and denitrification and carried out N-cycling potential assays. ResultsHere we are showing that populations/genotypes of a single species can vary in their ecological interaction with denitrifers and nitrifers. Some hybrid and teosinte genotypes supported microbial communities with lower potential nitrification and potential denitrification activity in the rhizosphere, while inbred genotypes stimulated/did not inhibit these N-cycling activities. These potential differences translated to functional differences in N2O fluxes, with teosinte plots producing less GHG than maize plots. ConclusionTaken together, these results suggest thatZeagenetic variation can lead to changes in N-cycling processes that result in N leaching and N2O production, and thereby are selectable targets for crop improvement. Understanding the underlying genetic variation contributing to belowground microbiome N-cycling into our conventional agricultural system could be useful for sustainability.more » « less
-
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
-
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
-
Summary Nitrogen (N2)‐fixing moss microbial communities play key roles in nitrogen cycling of boreal forests. Forest type and leaf litter inputs regulate moss abundance, but how they control moss microbiomes and N2‐fixation remains understudied. We examined the impacts of forest type and broadleaf litter on microbial community composition and N2‐fixation rates ofHylocomium splendensandPleurozium schreberi.We conducted a moss transplant and leaf litter manipulation experiment at three sites with paired paper birch (Betula neoalaskana) and black spruce (Picea mariana) stands in Alaska. We characterized bacterial communities using marker gene sequencing, determined N2‐fixation rates using stable isotopes (15N2) and measured environmental covariates.Mosses native to and transplanted into spruce stands supported generally higher N2‐fixation and distinct microbial communities compared to similar treatments in birch stands. High leaf litter inputs shifted microbial community composition for both moss species and reduced N2‐fixation rates forH. splendens, which had the highest rates. N2‐fixation was positively associated with several bacterial taxa, including cyanobacteria.The moss microbiome and environmental conditions controlled N2‐fixation at the stand and transplant scales. Predicted shifts from spruce‐ to deciduous‐dominated stands will interact with the relative abundances of mosses supporting different microbiomes and N2‐fixation rates, which could affect stand‐level N inputs.more » « less
An official website of the United States government
