Applied implications
The research program outlined above serves the ultimate goal of unraveling how plant genotypes, microbial genotypes (or communities), and the environment interact to determine adaptive outcomes. This is important for understanding first principles of evolutionary ecology but also is a shared goal with agronomists interested in using microbial technologies for enhanced crop production (Busby et al. 2017; Toju et al. 2018). Microbes have the potential to make crops more productive, less susceptible to disease, and more drought tolerant (Bakker et al. 2012; Reid & Greene 2012). Additionally, microbes are increasingly recognized as an important factor in plant restoration and conservation (Ji et al. 2010; Middleton et al. 2015; Cheeke et al. 2019). In one example, Douglas-fir trees, transplanted in a provenance trial, decreased in height as much as 15% as ectomycorrhizal communities diverged from communities at their home sites (Kranabetter et al. 2015), indicating that assisted migration will be inhibited when coevolved/coadapted plant microbe interactions are disrupted. Despite a growing appreciation of the importance of microbes in applied contexts, microbial technologies have been hampered by the complexity of the plant microbiome, the context dependency of plant-microbe interactions, and the difficulties of successfully establishing introduced microbial communities.
To better understand the effects of microbes so that we can harness them as technologies, we need to be able to identify and isolate important members of the microbial community and determine whether their effects are generalized vs. host-genotype specific. The age of informatics has allowed us a glimpse into the diversity and complexity of the microbiome, but much work remains to disentangle single species from multi-species effects and how relevant microbial genotypic diversity is for adaptive benefits. For example, we know relatively little about intra-specific diversity in many microbial taxa, including important groups such as arbuscular mycorrhizal fungi (Johnson et al. 2012) or how diversity (whether intra- or interspecific) maps onto microbial function and influences the likelihood of microbe-mediated local adaptation or microbe-mediated adaptive plasticity in plants.
A further challenge is understanding context dependency in plant-microbe interactions. Plants do not universally benefit from interactions with microbes (even those generally referred to as mutualists), but rather these interactions, like many species’ interactions, are highly context dependent (Johnson 1993; Bronstein 1994; Chamberlain et al.2014). One of the top research priorities into microbe-mediated adaptation should be efforts to delineate this context dependency. Factors that could drive context-dependency in plant-microbe relationships include plant characteristics such as mating system, invasive status, life-history strategy, as well as microbial characteristics such as vertical/horizontal transmission, obligate/facultative, microbial species interactions, and priority effects, and habitat characteristics such as aridity, nutrient availability, and competition. In short, although the body of data suggests that microbial communities commonly shift in response to environmental change (Allison & Martiny 2008) and that microbes can influence plant phenotypes and plant fitness (Goh et al. 2013; Hawkes et al. 2020; Kolodny & Schulenburg 2020; Petipas et al. 2020b), we still have little understanding about how and when microbial communities are likely to change in ways that influence microbe-mediated local adaptation or microbe-mediated adaptive plasticity in plants.