Eco-evolutionary interaction between microbiome presence and rapid biofilm evolution determines plant host fitness

Tan, Jiaqi; Kerstetter, Julia E; Turcotte, Martin M.

doi:10.1038/s41559-021-01406-2

Cited by 37 publications

(50 citation statements)

References 55 publications

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“…Another example, is the evolution of complementary traits between plants and mycorrhizal fungi, where fungi depend on the host plant carbon for energy consumption and hosts providing a more hospitable environment for fungi (Brundrett, 2002 ; Hoeksema, 2010 ). However, there is a growing body of literature that considers the microbiome as a superorganism and single unit of selection, in particular within the context of the holobiont framework (Theis et al ., 2016 ; Ravanbakhsh et al ., 2021 ; Tan et al ., 2021 ). When taking this perspective, we think that the patterns of increased diversity with domestication, phylosymbiosis, and a strongly conserved core microbiome across the Malus phylogeny, together with evidence for concurrent plant and microbiome admixture and introgression, provide support for co‐evolution between Malus species and their microbiome during domestication.…”

Section: Discussionmentioning

confidence: 99%

Evidence for host–microbiome co‐evolution in apple

et al. 2021

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Plants evolved in association with a diverse community of microorganisms. The effect of plant phylogeny and domestication on host-microbiome co-evolutionary dynamics are poorly understood.Here we examined the effect of domestication and plant lineage on the composition of the endophytic microbiome of 11 Malus species, representing three major groups: domesticated apple (M. domestica), wild apple progenitors, and wild Malus species.The endophytic community of M. domestica and its wild progenitors showed higher microbial diversity and abundance than wild Malus species. Heirloom and modern cultivars harbored a distinct community composition, though the difference was not significant. A community-wide Bayesian model revealed that the endophytic microbiome of domesticated apple is an admixture of its wild progenitors, with clear evidence for microbiome introgression, especially for the bacterial community. We observed a significant correlation between the evolutionary distance of Malus species and their microbiome.This study supports co-evolution between Malus species and their microbiome during domestication. This finding has major implications for future breeding programs and our understanding of the evolution of plants and their microbiomes.

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Section: Discussionmentioning

confidence: 99%

Evidence for host–microbiome co‐evolution in apple

et al. 2021

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“…Further testing of additional plant-associated bacteria with varying capacity for IAA production would be necessary to build on this initial work to define the threshold level(s) of auxin biosynthesis by the bacteria and its ability to modify host root morphology. As a recent example, microbial-community-derived auxin was posited to play a possible role in increasing Lemna minor fitness as measured by the increased number of plants, although this work relied on only using the Salkowski assay to infer auxin production by the bacteria [ 44 ]. Similarly, Bacillus safensis strains were screened for IAA-producing capability solely using the Salkowski assay, and their function in inducing Cd stress tolerance and promoting plant growth was partly based on the strains’ ability to produce auxins [ 41 , 42 ].…”

Section: Discussionmentioning

confidence: 99%

Auxin-Producing Bacteria from Duckweeds Have Different Colonization Patterns and Effects on Plant Morphology

Gilbert

Poulev

Chrisler

et al. 2022

Plants

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The role of auxin in plant–microbe interaction has primarily been studied using indole-3-acetic acid (IAA)-producing pathogenic or plant-growth-promoting bacteria. However, the IAA biosynthesis pathway in bacteria involves indole-related compounds (IRCs) and intermediates with less known functions. Here, we seek to understand changes in plant response to multiple plant-associated bacteria taxa and strains that differ in their ability to produce IRCs. We had previously studied 47 bacterial strains isolated from several duckweed species and determined that 79% of these strains produced IRCs in culture, such as IAA, indole lactic acid (ILA), and indole. Using Arabidopsis thaliana as our model plant with excellent genetic tools, we performed binary association assays on a subset of these strains to evaluate morphological responses in the plant host and the mode of bacterial colonization. Of the 21 tested strains, only four high-quantity IAA-producing Microbacterium strains caused an auxin root phenotype. Compared to the commonly used colorimetric Salkowski assay, auxin concentration determined by LC–MS was a superior indicator of a bacteria’s ability to cause an auxin root phenotype. Studies with the auxin response mutant axr1-3 provided further genetic support for the role of auxin signaling in mediating the root morphology response to IAA-producing bacteria strains. Interestingly, our microscopy results also revealed new evidence for the role of the conserved AXR1 gene in endophytic colonization of IAA-producing Azospirillum baldaniorum Sp245 via the guard cells.

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“…BC syncom was formed with taxa that represented most of the enriched biofilm and quorum sensing (QS) genes in the phyllosphere 6 . Biofilm formation has been associated with changes in the plant microbiome 23 and the ability of immigrant bacteria to colonize the leaves 24 . Moreover, the genomic annotation of Network and Random syncom members have shown that they possess genes related to biofilm formation and QS (Fig S12 ), which warrants more research to assess their influence on community structure.…”

Section: Importantly Our Work Demonstrates That Phyllospheric Microbi...mentioning

confidence: 99%

Microbiome-inspired phyllospheric synthetic communities increase microbial diversity and productivity of field-grown plants of Agave tequilana

Flores‐Núñez

Camarena‐Pozos

Chávez-González

et al. 2022

Preprint

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Agaves are plants native to North America that sustain life in arid and semi-arid ecosystems. Previous studies revealed that cultivated plants of Agave tequilana had lower microbial diversity and functionality compared to wild species. Here, we tested if microbiome-inspired phyllospheric synthetic communities, based on microbial hubs or enriched phyllospheric microbial functions, could increase microbial diversity and plant fitness in A. tequilana. We applied seven functional and three random syncoms on one-year-old plants of A. tequilana in the field and monitored their development for two years. Phylogenetic analyses revealed that the composition and diversity of the phyllospheric prokaryotic and eukaryotic communities associated with A. tequilana were affected by the season, with greatest diversity observed during the dry months. The addition of functional syncoms promoted phyllospheric microbial communities with a higher diversity, greater capacity to consume carbon sources, and more integrated and complex networks. Additionally, plants treated with functional syncoms had an increased content of sugars (oBrix, a measure of productivity in agaves) in the stems, and higher leaf metabolic diversity. Our work demonstrates that inoculation of syncoms formulated based on functional analyses of microbiome data represents an effective biotechnological tool to improve the sustainability and productivity of crops of arid ecosystems.

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Eco-evolutionary interaction between microbiome presence and rapid biofilm evolution determines plant host fitness

Cited by 37 publications

References 55 publications

Evidence for host–microbiome co‐evolution in apple

Evidence for host–microbiome co‐evolution in apple

Auxin-Producing Bacteria from Duckweeds Have Different Colonization Patterns and Effects on Plant Morphology

Microbiome-inspired phyllospheric synthetic communities increase microbial diversity and productivity of field-grown plants of Agave tequilana

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