Seasonal activities of the phyllosphere microbiome of perennial crops

Howe, Adina; Stopnišek, Nejc; Dooley, Shane K.; Yang, Fan; Grady, Keara L.; Shade, Ashley

doi:10.1038/s41467-023-36515-y

Cited by 16 publications

(12 citation statements)

References 119 publications

(138 reference statements)

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“…2). On perennial crops, similar results were observed on plant leaves (32) with a strong bacterial communities' variation over seasons. It is therefore evident that studying holobionts over several seasons/years and host compartments is crucial to dissect the genomic architecture regulating the host-microbiome interactions.…”

Section: Discussionsupporting

confidence: 77%

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Maillet,

Norest,

Kautsky

et al. 2023

Preprint

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Plants as animals are strictly associated with a cortege of microbial communities influencing their health, fitness and evolution. Therefore, scientists refer to all living organisms as holobionts; complex genetic units that coevolve simultaneously. This is what has been recently proposed as the hologenome theory of evolution. This exciting and attractive theory has important implications on animal and plant health; however, it still needs consistent proof to be validated. Indeed, holobionts are still poorly studied in their natural habitats where coevolution and natural selective processes occur. Compared to animals and crops, wild plant populations are an excellent and unique model to explore the hologenome theory. These sessile holobionts have strictly coevolved with their microbiota for decades and natural selection and adaptive processes acting on wild plants are likely to regulate the plant-microbe interactions. Here we conducted for the first time a microbiota survey, plant genome sequencing and Genome-Environmental Analysis (GEA) of 26 natural populations of the non-model plant speciesBrassica rapa. We collected plants over two seasons in Italy and France, and analyzed the microbiota on two plant compartments (root and rhizosphere). We identified that plant compartment and season modulateB. rapamicrobiota. More importantly, when conducting GEA we evidenced neat peaks of association correlating with both fungal and bacterial microbiota. Surprisingly, we found 13 common genes between fungal and bacterial diversity descriptors that we referred under the name of Holobiont Generalist Genes (HGG). These genes might strongly regulate the diversity and composition of plant microbiota at the inter-kingdom level.Significance StatementThe novel hologenome concept claims that hosts and their associated microbes (considered as holobionts) are a unique evolutionary unit on which natural selection acts. Thus, the hologenome theory assumes that hosts and microbiomes simultaneously coevolve. This novel vision of universal evolutionary entities is promising for both animal and plant health purposes. However, it is still quietly controversial as it suffers from a lack of tangible evidence. How can we enrich the debate on holobionts? How can we translate this concept in discoveries that can change farming practices? Our study is filling the gaps of the hologenome theory by showing that certain genes under natural selection and regulating plant microbiota are generalist in response to fungal and bacterial communities.

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Section: Discussionsupporting

confidence: 77%

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Maillet,

Norest,

Kautsky

et al. 2023

Preprint

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“…These key taxa were disproportionately from speci c taxonomic clades within both the bacteria (Hymenobacter) and fungi (Tremellales). The role of Hymenobacter within the leaf microbiome is not well known, but they are common within them (Noble et al, 2020) and are predicted from their genomes to affect the host biosynthetic pathways (such as isoprenoid biosynthesis) (Howe et al, 2023). Given the notable number of correlations between Hymenobacter ASVs and leaf metabolites, results here further suggest members of the genus in uence the leaf metabolome and are worthy of further studies.…”

Section: Discussionmentioning

confidence: 71%

Above and Belowground Microbes Are Associated With Variation of the Leaf Metabolome; But Herbivory Has Nominal Effects

Barnes,

Hilton,

Nielsen

et al. 2023

Preprint

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Background Microbes are associated with nearly every plant surface and affect the host’s functioning. While many studies to date have investigated the composition of the plant microbiome and compared it with the plant’s metabolome (a measure of the host functioning), a holistic understanding which considers interactions both above and belowground is lacking. In this work, we hypothesise that soil is a reservoir for both root and leaf microbes, and that herbivory disrupts the regulation of the leaf microbial community. We further hypothesise that plant-associated microbial communities will correlate with the leaf metabolome, but the root microbiota will better correlate with the leaf metabolome than the leaf microbiota. To test these hypotheses, fungal and bacterial communities of herbivore-damaged and undamaged leaves, roots and the surrounding soil was characterised across 15 Plantago major populations sampled from across geographical and environmental gradients from Denmark. Microbial communities were then compared against untargeted and targeted (anti-herbivory/microbials) leaf metabolomic data. Results We found that the fungal communities showed significant inter-connectivity above and belowground, while bacteria were mainly specialised to each sample type. Herbivory had no effect on leaf microbiome or the metabolome. Fungal root endophytes (Glomeromycotina arbuscular mycorrhizal fungi) and leaf bacteria correlated most strongly with the overall leaf metabolome. However, there were specific pathogenic fungi found in the leaf associated with the abundance of specific metabolites. Conclusions In this study, demonstrate the complexity of plant metabolome-microbiome interactions, and the need to fully integrate the microbiome of different tissue types to fully understand plant’s secondary metabolome. The decreasing costs of -omics methods and high-performance computing costs has made it possible to perform multi-omic, multi-tissue approaches at large-scale, as in this work. It is therefore possible to identify novel plant-microbe interactions, even from plants sampled outside of controlled environments.

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“…In recent years, much attention has been paid to leaf colonizers and the factors that drive leaf colonization at the population and the community level. For example, the host plant species influences leaf colonization and bacterial community composition [ 2 – 4 ], leading to recurring patterns of bacterial communities on leaves, at least at low phylogenetic resolution, from year to year [ 5 , 6 ].…”

Section: Introductionmentioning

confidence: 99%

Hitching a Ride in the Phyllosphere: Surfactant Production of Pseudomonas spp. Causes Co-swarming of Pantoea eucalypti 299R

Kunzler,

Schlechter,

Schreiber

et al. 2024

Microb Ecol

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Here, we demonstrate the beneficial effect of surfactant-producing pseudomonads on Pantoea eucalypti 299R. We conducted a series of experiments in environments of increasing complexity. P. eucalypti 299R (Pe299R), and Pseudomonas sp. FF1 (Pff1) or Pe299R and surfactant-production deficient Pseudomonas sp. FF1::ΔviscB (Pff1ΔviscB) were co-inoculated in broth, on swarming agar plates, and on plants. In broth, there were no differences in the growth dynamics of Pe299R when growing in the presence of Pff1 or Pff1ΔviscB. By contrast, on swarming agar plates, Pe299R was able to co-swarm with Pff1 which led to a significant increase in Pe299R biomass compared to Pe299R growing with Pff1ΔviscB or in monoculture. Finally in planta, and using the single-cell bioreporter for reproductive success (CUSPER), we found a temporally distinct beneficial effect of Pff1 on co-inoculated Pe299R subpopulations that did not occur in the presence of Pff1ΔviscB. We tested three additional surfactant-producing pseudomonads and their respective surfactant knockout mutants on PE299R on swarming agar showing similar results. This led us to propose a model for the positive effect of surfactant production during leaf colonization. Our results indicate that co-motility might be common during leaf colonization and adds yet another facet to the already manyfold roles of surfactants.

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Seasonal activities of the phyllosphere microbiome of perennial crops

Cited by 16 publications

References 119 publications

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Above and Belowground Microbes Are Associated With Variation of the Leaf Metabolome; But Herbivory Has Nominal Effects

Hitching a Ride in the Phyllosphere: Surfactant Production of Pseudomonas spp. Causes Co-swarming of Pantoea eucalypti 299R

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