Using transects to disentangle the environmental drivers of plant microbiome assembly

Abstract Background: Plant microbiome is an integral part of the host influencing its growth and health. The increasing evidence indicates that plant rhizosphere may recruit beneficial microbes to suppress soil-borne pathogen, but the ecological mechanisms that govern plant microbiome assembly and functions under disease in both below and aboveground compartments are not fully understood. Here we examined both bacterial and fungal communities from soils (rhizosphere and bulk soil) and multiple plant compartments (e.g. root, stem, and fruit) of chili pepper (Capsicum annuum L.) at two pepper production sites, and explored how Fusarium wilt disease (FWD) affect the assembly, co-occurrence patterns, and ecological functions of plant-associated microbiomes. Results: Our data demonstrated that FWD had less impact on reproductive organ (fruit) than on vegetative organs (root and stem), with the strongest impact in the stem upper epidermis. Fungal intra-kingdom networks presented lower stabilities and their communities were more sensitive to FWD than the bacterial communities. Moreover, the diseased pepper was more susceptible to colonization by other pathogenic fungi, but they may recruit potential beneficial bacteria to facilitate host or offspring survival, and FWD may enhance the ecological importance of fungal taxa in the interkingdom network. Further, metagenomic analysis revealed that several potential protective functional genes encoding detoxify and biofilm formation were significantly enriched in the diseased pepper.Conclusion: Together, these results significantly advance our understanding of pepper microbiome assembly and functions under biotic stress. Our work highlights the diseased plant and the aboveground compartments harbor a potential of beneficial microbiomes and functions that, in concert, can provide potential critical data for harnessing the plant microbiome for sustainable agriculture.

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Fire alters plant microbiome assembly patterns: integrating the plant and soil microbial response to disturbance

New Phytologist ◽

10.1111/nph.17248 ◽

2021 ◽

Author(s):

Nicholas C. Dove ◽

Dawn M. Klingeman ◽

Alyssa A. Carrell ◽

Melissa A. Cregger ◽

Christopher W. Schadt

Keyword(s):

Soil Microbial ◽

Microbial Response ◽

Microbiome Assembly ◽

Plant Microbiome

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Endophytic microbiome variation at the level of a single plant seed

10.1101/2021.04.27.441449 ◽

2021 ◽

Author(s):

AF Bintarti ◽

A Sulesky-Grieb ◽

N Stopnisek ◽

A Shade

Keyword(s):

Common Bean ◽

Individual Plant ◽

Metagenomic Dna ◽

Plant Seed ◽

Individual Seed ◽

Bean Plants ◽

Plant Level ◽

The Individual ◽

Microbiome Assembly ◽

Plant Microbiome

AbstractLike other plant compartments, the seed harbors a microbiome. The members of the seed microbiome are the first to colonize a germinating seedling, and they initiate the trajectory of microbiome assembly for the next plant generation. Therefore, the members of the seed microbiome are important for the dynamics of plant microbiome assembly and the vertical transmission of potentially beneficial symbionts. However, it remains challenging to assess the microbiome at the individual seed level (and, therefore, for the future individual plant) due to low endophytic microbial biomass, seed exudates that can select for particular members, and high plant and plastid contamination of resulting reads. Here, we report a protocol for extracting metagenomic DNA from an individual seed (common bean, Phaseolus vulgaris L.) with minimal disruption of host tissue, which we expect to be generalizable to other medium-and large-seed plant species. We applied this protocol to quantify the 16S rRNA V4 and ITS2 amplicon composition and variability for individual seeds harvested from replicate common bean plants grown under standard, controlled conditions to maintain health. Using metagenomic DNA extractions from individual seeds, we compared seed-to-seed, pod-to-pod, and plant-to-plant microbiomes, and found highest microbiome variability at the plant level. This suggests that several seeds from the same plant could be pooled for microbiome assessment, given experimental designs that apply treatments at the maternal plant level. This study adds protocols and insights to the growing toolkit of approaches to understand the plant-microbiome engagements that support the health of agricultural and environmental ecosystems.

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Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

10.1101/2021.12.20.473370 ◽

2021 ◽

Author(s):

Ben O Oyserman ◽

Stalin Sarango Flores ◽

Thom Griffioen ◽

Elmar van der Wijk ◽

Lotte Pronk ◽

...

Keyword(s):

Quantitative Traits ◽

Genetic Basis ◽

Genetic Factors ◽

Breeding Programs ◽

Plant Polysaccharides ◽

Rhizosphere Microbiome ◽

Iron Sulfur ◽

Tomato Gene ◽

Microbiome Assembly ◽

Plant Microbiome

Microbiomes play a pivotal role in plant growth and health, but the genetic factors involved in microbiome assembly remain largely elusive. Here, 16S amplicon and metagenomic features of the rhizosphere microbiome were mapped as quantitative traits of a recombinant inbred line population of a cross between wild and domesticated tomato. Gene content analysis of prioritized tomato QTLs suggested a genetic basis for differential recruitment of various rhizobacterial lineages, including a Streptomyces-associated 6.31-Mbp region harboring tomato domestication sweeps and encoding, among others, the iron regulator FIT and the aquaporin SlTIP2.3. Within metagenome-assembled genomes of the rhizobacterial lineages Streptomyces and Cellvibrio, we identified microbial genes involved in metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, whose genetic variation associated with either modern or wild tomato QTLs. Integrating 'microbiomics' and quantitative plant genetics pinpointed putative plant and reciprocal microbial traits underlying microbiome assembly, thereby providing the first step towards plant-microbiome breeding programs.

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Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis

Science ◽

10.1126/science.abd0695 ◽

2020 ◽

Vol 371 (6525) ◽

pp. eabd0695 ◽

Cited By ~ 1

Author(s):

Isai Salas-González ◽

Guilhem Reyt ◽

Paulina Flis ◽

Valéria Custódio ◽

David Gopaulchan ◽

...

Keyword(s):

Regulatory Mechanism ◽

Nutrient Balance ◽

Mineral Nutrient ◽

Cell Layers ◽

Endodermal Differentiation ◽

Nutrient Homeostasis ◽

Microbiome Assembly ◽

Root Endodermis ◽

Homeostatic Mechanisms ◽

Plant Microbiome

Plant roots and animal guts have evolved specialized cell layers to control mineral nutrient homeostasis. These layers must tolerate the resident microbiota while keeping homeostatic integrity. Whether and how the root diffusion barriers in the endodermis, which are critical for the mineral nutrient balance of plants, coordinate with the microbiota is unknown. We demonstrate that genes controlling endodermal function in the model plant Arabidopsis thaliana contribute to the plant microbiome assembly. We characterized a regulatory mechanism of endodermal differentiation driven by the microbiota with profound effects on nutrient homeostasis. Furthermore, we demonstrate that this mechanism is linked to the microbiota’s capacity to repress responses to the phytohormone abscisic acid in the root. Our findings establish the endodermis as a regulatory hub coordinating microbiota assembly and homeostatic mechanisms.

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Endophytic microbiome variation among single plant seeds

Phytobiomes Journal ◽

10.1094/pbiomes-04-21-0030-r ◽

2021 ◽

Author(s):

Ari Fina Bintarti ◽

Abby Sulesky-Grieb ◽

Nejc Stopnišek ◽

Ashley Shade

Keyword(s):

Common Bean ◽

Phaseolus Vulgaris L ◽

Plant Seeds ◽

Individual Seed ◽

Bean Plants ◽

Plant Level ◽

The Individual ◽

Microbial Dna ◽

Microbiome Assembly ◽

Plant Microbiome

Like other plant compartments, the seed harbors a microbiome. Seed microbiome members are the first to colonize a germinating seedling, and they may initiate the trajectory of microbiome assembly for the next plant generation. Therefore, the members of the seed microbiome are important for the dynamics of plant microbiome assembly and the vertical transmission of potentially beneficial symbionts. However, it remains challenging to assess the microbiome at the individual seed level (and, therefore, for the future individual plants) due to low endophytic microbial biomass, seed exudates that can select for particular members, and high plant and plastid contamination of resulting reads. Here, we report a protocol for extracting microbial DNA from an individual seed (common bean, Phaseolus vulgaris L.) with minimal disruption of host tissue, which we expect to be generalizable to other medium- and large-seed plant species. We applied this protocol to determine the 16S rRNA V4 and rRNA ITS2 amplicon composition and examine the variability of individual seeds harvested from replicate common bean plants grown under standard, controlled conditions to maintain health. Using DNA extractions from individual seeds, we compared seed-to-seed, pod-to-pod, and plant-to-plant microbiomes, and found highest microbiome variability at the plant level. This suggests that several seeds from the same plant could be pooled for microbiome assessment, given experimental designs that apply treatments at the parent plant level. This study adds protocols and insights to the growing toolkit of approaches to understand the plant-microbiome engagements that support the health of agricultural and environmental ecosystems.

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Disease-induced changes in plant microbiome assembly and functional adaptation

Microbiome ◽

10.1186/s40168-021-01138-2 ◽

2021 ◽

Vol 9 (1) ◽

Author(s):

Min Gao ◽

Chao Xiong ◽

Cheng Gao ◽

Clement K. M. Tsui ◽

Meng-Meng Wang ◽

...

Keyword(s):

Signaling Pathways ◽

Pathogenic Fungi ◽

Functional Adaptation ◽

Diseased Plant ◽

Beneficial Bacteria ◽

Ecological Processes ◽

Beneficial Microbes ◽

Pathogen Invasion ◽

Microbiome Assembly ◽

Plant Microbiome

Abstract Background The plant microbiome is an integral part of the host and increasingly recognized as playing fundamental roles in plant growth and health. Increasing evidence indicates that plant rhizosphere recruits beneficial microbes to the plant to suppress soil-borne pathogens. However, the ecological processes that govern plant microbiome assembly and functions in the below- and aboveground compartments under pathogen invasion are not fully understood. Here, we studied the bacterial and fungal communities associated with 12 compartments (e.g., soils, roots, stems, and fruits) of chili pepper (Capsicum annuum L.) using amplicons (16S and ITS) and metagenomics approaches at the main pepper production sites in China and investigated how Fusarium wilt disease (FWD) affects the assembly, co-occurrence patterns, and ecological functions of plant-associated microbiomes. Results The amplicon data analyses revealed that FWD affected less on the microbiome of pepper reproductive organs (fruit) than vegetative organs (root and stem), with the strongest impact on the upper stem epidermis. Fungal intra-kingdom networks were less stable and their communities were more sensitive to FWD than the bacterial communities. The analysis of microbial interkingdom network further indicated that FWD destabilized the network and induced the ecological importance of fungal taxa. Although the diseased plants were more susceptible to colonization by other pathogenic fungi, their below- and aboveground compartments can also recruit potential beneficial bacteria. Some of the beneficial bacterial taxa enriched in the diseased plants were also identified as core taxa for plant microbiomes and hub taxa in networks. On the other hand, metagenomic analysis revealed significant enrichment of several functional genes involved in detoxification, biofilm formation, and plant-microbiome signaling pathways (i.e., chemotaxis) in the diseased plants. Conclusions Together, we demonstrate that a diseased plant could recruit beneficial bacteria and mitigate the changes in reproductive organ microbiome to facilitate host or its offspring survival. The host plants may attract the beneficial microbes through the modulation of plant-microbiome signaling pathways. These findings significantly advance our understanding on plant-microbiome interactions and could provide fundamental and important data for harnessing the plant microbiome in sustainable agriculture.

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Hormones as go‐betweens in plant microbiome assembly

The Plant Journal ◽

10.1111/tpj.15135 ◽

2020 ◽

Author(s):

Ruth Eichmann ◽

Luke Richards ◽

Patrick Schäfer

Keyword(s):

Microbiome Assembly ◽

Plant Microbiome

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Assembly of the Populus Microbiome Is Temporally Dynamic and Determined by Selective and Stochastic Factors

mSphere ◽

10.1128/msphere.01316-20 ◽

2021 ◽

Author(s):

Nicholas C. Dove ◽

Allison M. Veach ◽

Wellington Muchero ◽

Toni Wahl ◽

James C. Stegen ◽

...

Keyword(s):

Agricultural Crops ◽

Future Health ◽

Microbiome Assembly ◽

Initial Assembly ◽

Plant Microbiome

The initial assembly of the plant microbiome may establish the trajectory of forthcoming microbiome states, which could determine the overall future health of the plant. However, while much is known about the initial microbiome assembly of grasses and agricultural crops, less is known about the initial microbiome of long-lived trees, such as poplar ( Populus spp.).

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