Improving rice drought tolerance through host-mediated microbiome selection

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    eLife assessment

    This valuable study reports on a series of artificial selection experiments for microbiomes that confer drought tolerance to rice plants. A major strength is the solid experimental design with multiple soils, which will likely guide others in designing their experiments, but the study has also shortcomings in that the rescuing effect is not benchmarked against healthy well-watered plants, the sterilized controls do not add much information, and the dispersal between inocula confounds the interpretation of the results. In addition, while the type of work presented here is a first step towards the eventual goal of plant microbiome engineering, that goal is still mainly an ambition. The abstract would benefit from this being made clear, and the presentation would overall benefit from more extensive consideration of recent developments in the field.

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Abstract

Plant microbiome engineering remains a significant challenge due to challenges associated with accurately predicting microbiome assembly and function in complex, heterogeneous soil environments. However, host-mediated selection can simplify the process by using plant host phenotype as a reporter of microbiome function; by iteratively selecting microbiomes from hosts with desired phenotypes and using them to inoculate subsequent cohorts of hosts, artificial selection can steer the microbiome towards a composition producing optimized plant phenotypes. In this study, we inoculated rice with wild microbial communities from fallow rice field, desert, and serpentine seep field soils. By challenging these plants with drought and iteratively selecting microbiomes from the least drought stressed plants across multiple generations, we derived simplified microbiomes that enhanced both the growth and drought tolerance of rice. Across selection cycles, microbiomes within and between soil treatments became increasingly similar, implicating both dispersal and selection as drivers of community composition. With amplicon sequencing data we identified specific bacterial taxa associated with improved rice drought phenotypes; while many of these taxa have been previously described as plant growth promoters, we also identified novel taxa exhibiting strong positive correlation with improved drought performance. Lastly, we resolved 272 metagenome-assembled genomes (MAGs) and used these MAGs to identify functions enriched in bacteria driving enhanced drought tolerance. The most significantly enriched functions—particularly glycerol-3-phosphate and iron transport—have been previously implicated as potential mediators of plant-microbe interactions during drought. Altogether, these data demonstrate that host-mediated selection provides an efficient framework for microbiome engineering through the identification of both individual taxa and simplified communities associated with enhanced plant phenotypes.

Article activity feed

  1. eLife assessment

    This valuable study reports on a series of artificial selection experiments for microbiomes that confer drought tolerance to rice plants. A major strength is the solid experimental design with multiple soils, which will likely guide others in designing their experiments, but the study has also shortcomings in that the rescuing effect is not benchmarked against healthy well-watered plants, the sterilized controls do not add much information, and the dispersal between inocula confounds the interpretation of the results. In addition, while the type of work presented here is a first step towards the eventual goal of plant microbiome engineering, that goal is still mainly an ambition. The abstract would benefit from this being made clear, and the presentation would overall benefit from more extensive consideration of recent …

  2. Reviewer #1 (Public Review):

    Summary:
    The study claims to explore plant microbiome engineering using host-mediated selection as a strategy to enhance rice growth and drought tolerance.

    Strengths:

    The authors have derived and identified simplified microbiomes from wild microbial communities of rice fields, deserts, and serpentine seep soils by selecting microbiomes from plants with desired phenotypes across generations. Metagenome-assembled genomes revealed enriched functions, such as glycerol-3-phosphate and iron transport, known to mediate plant-microbe interactions during drought.

    Weaknesses:

    The findings demonstrate the efficacy of host-mediated microbiome selection, but the engineering part for enhancing rice performance under drought-stress conditions has not been provided. The proposed mechanisms rely on correlations but not …

  3. Reviewer #2 (Public Review):

    Summary:

    In this study, Styer et al. impose artificial selection on root-associated microbiomes to increase drought tolerance in rice plants using different soils as starting microbiomes. Using NDVI and biomass as a proxy for plant health, they find that iterative passaging of the microbiomes of the best-performing plants increased plant resilience to drought stress in a soil-dependent manner. The study makes use of numerous controls. The authors survey the microbiota of the plants across generations, using an array of interesting analyses to characterize their observations. Firstly, the authors find that the acquired microbiomes are divergent towards the beginning of the selection experiment, but nearly converge later suggesting that the selected communities become more similar over time. One reason is that …

  4. Reviewer #3 (Public Review):

    Summary:

    In this work, Styer et al. explore host selection as a means for recruiting microbes that may aid their host under stressful conditions, in this case under drought stress, as an alternative to target-SynCom design. They do so by subjecting rice plants to several generations of soil transplantation, and by using the most successful rice plants as donors for the next generation. By using several NGS approaches and very thorough bioinformatics analysis, the authors identify potential microbial taxa and the associated functions enriched in the conditions of interest.

    Strengths:

    In general, I think this approach was very much needed in the field as an alternative to SynComs, which are still not readily usable in croplands. This work sets the grounds for future similar approaches, using different stresses …