A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota

Abstract

The microbiota thriving in the rhizosphere, the thin layer of soil surrounding plant roots, plays a critical role in plant’s adaptation to the environment. Domestication and breeding selection have progressively differentiated the microbiota of modern crops from the ones of their wild ancestors. However, the impact of eco-geographical constraints faced by domesticated plants and crop wild relatives on recruitment and maintenance of the rhizosphere microbiota remains to be fully elucidated. Here we performed a comparative 16S rRNA gene survey of the rhizosphere of 4 domesticated and 20 wild barley (Hordeum vulgare) genotypes grown in an agricultural soil under controlled environmental conditions. We demonstrated the enrichment of individual bacteria mirrored the distinct eco-geographical constraints faced by their host plants. Unexpectedly, Elite varieties exerted a stronger genotype effect on the rhizosphere microbiota when compared with wild barley genotypes adapted to desert environments with a preferential enrichment for members of Actinobacteria. Finally, in wild barley genotypes, we discovered a limited, but significant, correlation between microbiota diversity and host genomic diversity. Our results revealed a footprint of the host’s adaptation to the environment on the assembly of the bacteria thriving at the root-soil interface. In the tested conditions, this recruitment cue layered atop of the distinct evolutionary trajectories of wild and domesticated plants and, at least in part, is encoded by the barley genome. This knowledge will be critical to design experimental approaches aimed at elucidating the recruitment cues of the barley microbiota across a range of soil types.

Seed-Transmitted Bacteria and Fungi Dominate Juvenile Plant Microbiomes

“…In contrast to these recent discoveries, scientists have traditionally believed that all the rhizosphere microbiome "is recruited from the main reservoir of microorganisms present in soil" (Bakker et al, 2013), with publications on Arabidopsis (Lundberg et al, 2012), soy (Liu et al, 2019), rice (Edwards et al, 2015), and maize (Peiffer et al, 2013) rhizospheres reflecting this assumption. A great many publications survey the rhizosphere microbiomes of other plants, including barley (Terrazas et al, 2020), sorghum (Schlemper et al, 2017), coffee (Caldwell et al, 2015), common bean (Pérez-Jaramillo et al, 2019), sunflower (Leff et al, 2017), and pea (Turner et al, 2013). In our previous studies on bacteria in maize (Johnston-Monje et al, 2016) and fungi in tomato (Johnston-Monje et al, 2017), we have corroborated that soil adds significant microbial diversity to the rhizosphere; however, we also found that the most abundant members of the juvenile maize rhizosphere are seed-transmitted bacteria.…”

Physical geography, isolation by distance and environmental variables shape genomic variation of wild barley (Hordeum vulgare L. ssp. spontaneum) in the Southern Levant

“…Population structure reflects eco-geographical habitats (Hübner et al 2009 , 2012 ) and distinguishes between northern and southern genetic clusters correlated with latitude and precipitation gradients (Jakob et al 2014 ; Russell et al 2016 ). Common garden experiments in previous studies revealed that eco-geography was correlated with morphological traits (Hübner et al 2013 ), phenotypic plasticity (Galkin et al 2018 ), and rhizosphere microbiota (Terrazas et al 2020 ). Moreover, transplantation experiments showed a correlation between the geographical origin of wild barley ecotypes and fitness in different environments, suggesting local adaptation (Volis et al 2002a , b , 2011 ).…”

The plant microbiota signature of the Anthropocene as a challenge for microbiome research

“…So far, there is no clear link between the increased occurrence of r-strategists and specific phenotypic plant traits of extensively bred cultivars; however, it is likely that (i) increased amounts of readily available carbohydrates, (ii) shorter growth periods and faster ripening, and (iii) a loose connection between plants and their indigenous microbiota synergistically facilitate the establishment of microbial communities dominated by r-strategists. This trend can be clearly observed with several crop plants that were subjected to extensive plant breeding [ 45 , 56 ]. Their phenotypes were substantially changed within a relatively short period of time in order to increase the proportion of edible plant tissues.…”