Introduction
Plants have evolved alongside microbes for millions of years and have
formed intricate relationships with soil microbial communities via their
root systems. Soil microbial community composition is shaped by soil
abiotic conditions and varying soil types contain microbiomes with
distinct taxonomic distributions (Fierer 2017; Hartman & Tringe 2019).
Plant host genetics also drive the assembly of rhizosphere and
endosphere microbial communities (Jones et al. 2019; Trivedi et
al. 2020), and crop varieties or natural ecotypes (or genotypes)
grown in a common environment can differ in root and rhizosphere
community structure (Bowsher et al. 2020; Li et al. 2018;
Perez-Jaramillò et al. 2017; Wagner et al. 2016). To some degree, the
root microbiome can be thought of as an extended phenotype of the plant.
Plant-soil-microbiome relationships can influence plant traits and there
is strong evidence that microbes can yield positive effects on plant
performance directly or indirectly by impacting plant functional traits
(Egamberdieva et al. 2017; Lau & Lennon 2012; Wagner et al. 2014) or
negatively as pathogens. Plant root associated microbiomes impact root
traits, can increase nutrient acquisition, provide indirect impacts on
shoot traits (such as increasing shoot biomass) and promote tolerance to
abiotic and biotic stress (Friesen et al. 2011; Mendes et al.2013; Santhanam et al. 2015; Sukumar et al. 2013). In synthetic
community research, growing the same genotype in the presence or absence
of differing sets of selected microbiomes produces a wide range of plant
trait modulation (De Souza et al. 2020; Vorholt et al. 2017). Given the
growing evidence of microbial effects on plant growth and development,
it’s possible that plant microbial interactions also play a role in the
process of local adaptation, where plant populations diverge and exhibit
different niche characteristics and habitat preferences (Petipas et
al. 2021).
Many plant species are composed of highly varied ecotypes across their
range, each of which may show a high degree of trait divergence.
Quantitative traits can be profoundly influenced by environmental
factors and the degree to which these factors influence plant traits can
vary widely across genotypes. These types of interactions are termed
genotype-by-environment interaction (GxE; Des Marais et al. 2013). Many
studies focus on local adaptation and GxE in response to changing
habitats or conditions (Leimu & Fischer 2008; Midolo & Wellstein
2020), however, the relative contribution of abiotic and biotic factors
in driving GxE is often unclear (Runquist et al. 2020). Plants encounter
diverse biotic factors including competition, herbivory, pathogens and
an array of microbial communities (Bischoff et al. 2006; Järemo et al.
1999), but little is known about how specific interactions between
plants and microbial communities contribute to adaptation. Numerous
quantitative trait loci (QTL) mapping studies have explored the genetic
architecture of GxE in natural and crop populations for a number of
abiotic factors and this approach has become widely utilized to study
plant responses to abiotic stress and to understand plant trait
plasticity (Des Marais et al. 2016; Vij & Tyagi 2007). Far less
is known about the influence of biotic factors, especially microbiomes.
Additional experimental studies exploring the impact of microbial
communities are critically needed to fully elucidate aspects of
plant-microbe interactions and local adaptation.
Panicum hallii is a diploid, C4, self-fertilizing, North American
native perennial bunch grass that occurs across a large geographical
range with diverse habitats and climate. There are two naturally
occurring ecotypes of P. hallii that are classified as separate
varieties: an upland xeric ecotype, P. hallii var. hallii(hereafter referred to as hallii ) and a lowland mesic ecotype,P. hallii var. filipes (hereafter referred to asfilipes ). These ecotypes display trait divergence in a similar
direction and magnitude to other perennial grass species with upland and
lowland ecotypes, a pattern which is thought to be driven by adaptive
evolution along precipitation gradients across a species range (Gray et
al. 2014; Khasanova et al. 2019; Lowry et al. 2014). Many observations
have shown that both ecotypes of P. hallii display a large degree
of plasticity in several shoot traits in response to changes in abiotic
factors including light (Weng et al. 2019) and precipitation (Lovell et
al. 2018), yet these differences are minor in comparison to the
differences inherent between the ecotypes. Compared to abiotic factors,
little is known about the importance or relative contribution of biotic
environmental variation, especially soil microbiota, in shaping plant
shoot and root traits in the P. hallii system and plants in
general.
Here, we conducted a quantitative genetic experiment to examine the
impact of soil microbiomes and host genetics on root and shoot traits. A
recombinant inbred population (RIL) derived from a cross between the
upland and lowland ecotypes of P. hallii allowed us to identify
plant genomic regions contributing to microbial-mediated traits. To
overcome the limitations of synthetic community approaches and the
complexity of natural soils, we took a hybrid approach of inoculating
sterilized soils with naturally derived microbial communities in a
greenhouse setting. Specifically, we sought to answer four questions: 1)
Does the native soil microbiome drive plasticity in P. halliiabove- and below-ground traits? 2) Are microbiome effects general, or
specifically related to the location of origin of the microbiome? 3) DoP. hallii ecotypes exhibit GxE in response to variable soil
microbiomes? And, 4) Can we map genetic effects and their interactions
with the microbiome to the genome? Overall, our experiment demonstrates
the impact of living soil microbiomes on the quantitative genetic
architecture of both root and shoot traits in P. hallii and
highlights the potential importance of microbiomes in local adaptation.