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.