Functional team selection as a framework for local adaptation in plants and their belowground microbiomes

Abstract

Multicellular organisms are hosts to diverse communities of smaller organisms known as microbiomes. Plants have distinctive microbiomes that can provide important functions related to nutrition, defense, and stress tolerance. Empirical studies provide convincing evidence that in some-but not all-circumstances, belowground microbiomes help plants adapt to their local environment. The purpose of this review is to develop functional team selection (FTS) as a framework to help predict the conditions necessary for root microbiomes to generate local adaptation for their plant hosts. FTS envisions plants and their microbiomes as complex adaptive systems, and plant adaptations as emergent properties of these systems. If plants have the capacity to recognize and cultivate beneficial microbes and suppress pathogens, then it is possible for plants to evolve the capacity to gain adaptations by curating their microbiome. In resource-limited and stressful environments, the emergent functions of complex microbial systems may contribute to positive feedback linked to plant vigor, and ultimately, local adaptation. The key factors in this process are: (i) selective force, (ii) host constitution, (iii) microbial diversity, and (iv) time. There is increasing interest in harnessing beneficial microbial interactions in agriculture and many microbial growth-promoting products are commercially available, but their use is controversial because a large proportion of these products fail to consistently enhance plant growth. The FTS framework may help direct the development of durable plant-microbiome systems that enhance crop production and diminish pathogens. It may also provide valuable insights for understanding and managing other kinds of host-microbe systems.

Keywords: complex adaptive systems; cry-for-help hypothesis; host-mediated microbiome engineering; law of increasing functional information; local adaptation; mycorrhizae; niche construction theory; plant growth-promoting bacteria; plant–soil-feedback; syntrophy.

Figure 1

A plant holobiont is a complex system composed of a host plant plus diverse communities of interacting microorganisms both above- and belowground. The holobiont is an open system and external environmental factors (outer circle) generate selection pressures on the system. This review focuses on the root-associated microbiome comprised of interacting communities of eukaryotes (fungi, micro-invertebrates, and protists), prokaryotes (bacteria and archaea), and viruses. Functional plant-microbiome teams fit all the criteria to be considered complex adaptive systems [113, 128] composed of organisms that work together to improve plant fitness and generate adaptive traits for the host.

Figure 2

Functional team selection can drive the assembly and maintenance of communities of belowground microorganisms that improve host plant fitness when: (i) there is a selective force (e.g. limited soil resources and/or stress) that can be ameliorated by microbiome function, (ii) plant hosts can curate their microbiome (i.e. plants can selectively recruit beneficial microorganisms and deter detrimental ones), (iii) there is sufficient microbial diversity to provide adaptive functions, and (iv) there is sufficient time for a functional team to evolve (top panel). No functional team is predicted to evolve in the absence of these four requirements (middle panel). A dysfunctional team dominated by antagonistic interactions may occur when luxury supplies of essential resources and lack of environmental stress precludes selection for beneficial plant-microbe interactions. Over time, this dynamic may reduce crop yields in agricultural systems and contribute to plant succession in natural ecosystems (bottom panel).

Figure 3

Functional team selection (FTS) helps establish the criteria required for the assembly of host-microbiome systems that improve plant performance and may generate local adaptation. The driving factors in this process are: (i) selective force, (ii) host constitution (whether the host is able to curate its microbiome), (iii) microbial diversity, and (iv) time. This decision tree illustrates how the FTS framework can be used to predict whether functional teams are expected to assemble, and in turn, whether plant–soil-feedback (PSF) will be positive and generate local adaptation, neutral with no functional team, or negative with a dysfunctional team that may contribute to plant succession or yield decline in crops.