Research priorities for harnessing plant microbiomes in sustainable agriculture

Abstract

Feeding a growing world population amidst climate change requires optimizing the reliability, resource use, and environmental impacts of food production. One way to assist in achieving these goals is to integrate beneficial plant microbiomes-i.e., those enhancing plant growth, nutrient use efficiency, abiotic stress tolerance, and disease resistance-into agricultural production. This integration will require a large-scale effort among academic researchers, industry researchers, and farmers to understand and manage plant-microbiome interactions in the context of modern agricultural systems. Here, we identify priorities for research in this area: (1) develop model host-microbiome systems for crop plants and non-crop plants with associated microbial culture collections and reference genomes, (2) define core microbiomes and metagenomes in these model systems, (3) elucidate the rules of synthetic, functionally programmable microbiome assembly, (4) determine functional mechanisms of plant-microbiome interactions, and (5) characterize and refine plant genotype-by-environment-by-microbiome-by-management interactions. Meeting these goals should accelerate our ability to design and implement effective agricultural microbiome manipulations and management strategies, which, in turn, will pay dividends for both the consumers and producers of the world food supply.

Fig 1. Genotype, environment, management method, and microbiome interact to influence yield.

(A) Plant genotype and environmental properties (both biotic and abiotic) synergistically determine plant phenotypes. (B) Plant phenotypic traits influence the subset of microbes from the ambient community—which itself may partly reflect deterministic evolutionary processes like local adaptation to abiotic stresses—that colonize organs to form the crop microbiome. (C) The definition of a “healthy” or “beneficial” microbiome—one that improves yield—likely depends on the particular environmental challenges (both biotic and abiotic) experienced by a plant and the degree to which the plant’s phenotype is already adapted to those challenges. (D, E) Management methods primarily influence yield by altering the dynamics of genotype x environment x microbiome interactions, but can also modify the crop microbiome directly (e.g., microbial seed coating or other microbiome applications that may result from the stated research priorities).

Fig 2. Outcomes of inoculation with a microbial consortium.

(A) Illustration of varying outcomes of inoculating with a five-member consortium (colored non-rod shapes) in the presence of a diverse environmental microbial pool (gray rod shapes). Three cultivars are depicted growing in three different regimes: a normal year, a drought year, and low-input management. Genotype effects: In a normal year, Cultivar A is colonized by all five members of the inoculant consortium, while cultivar B is colonized only by yellow spheres and cultivar C is colonized only by teal stars. Environment/management effects: Compared to the normal year, the drought year shows higher colonization by blue ovals and the environmental microbial pool, while under low-input management all cultivars show increased colonization by the green spiky ovals, e.g., a nitrogen-fixer. A genotype-by-environment interaction is depicted by cultivar B only associating with the cyan clouds under low-input management, while cultivar C does not. We note that while interactions between microbes are not shown explicitly, these could be useful in efforts to manipulate microbiomes; e.g., the yellow circles and the cyan clouds always occur together. (B) Temporal dynamics of two communities after a disturbance event (e.g., pathogen attack, high temperature). The more resilient community recovers to its initial state after perturbation, while the less resilient community does not and is displaced entirely by members of the environmental microbial pool. We note that if the growth benefits are provided early in growth by the inoculum, an ecologically fragile community may still be able to enhance crop productivity.