Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere

Abstract

The rhizosphere is strongly influenced by plant-derived phytochemicals exuded by roots and plant species exert a major selective force for bacteria colonizing the root-soil interface. We have previously shown that rhizobacterial recruitment is tightly regulated by plant genetics, by showing that natural variants of Arabidopsis thaliana support genotype-specific rhizobacterial communities while also releasing a unique blend of exudates at six weeks post-germination. To further understand how exudate release is controlled by plants, changes in rhizobacterial assemblages of two Arabidopsis accessions, Cvi and Ler where monitored throughout the plants' life cycle. Denaturing gradient gel electrophoresis (DGGE) fingerprints revealed that bacterial communities respond to plant derived factors immediately upon germination in an accession-specific manner. Rhizobacterial succession progresses differently in the two accessions in a reproducible manner. However, as plants age, rhizobacterial and control bulk soil communities converge, indicative of an attenuated rhizosphere effect, which coincides with the expected slow down in the active release of root exudates as plants reach the end of their life cycle. These data strongly suggest that exudation changes during plant development are highly genotype-specific, possibly reflecting the unique, local co-evolutionary communication processes that developed between Arabidopsis accessions and their indigenous microbiota. IntroductionPlant roots are an active component of soil, creating the rhizosphere by physically changing soil characteristics as they elongate and branch out, and dramatically altering the chemical milieu through exudation of hundreds of phytochemicals and sloughedoff cells. 1,2 Root-derived compounds mediate a plethora of biological processes. The plant-bacterial relationships that occur at the root-soil interface are probably a combination of opportunistic interactions, as ubiquitous organisms exploit the nutrients present, and highly regulated communication events. The latter interactions are mediated by root-exuded signalling molecules that elicit specific responses. The type and amounts of the various exudate compounds synthesized and released by roots are under the plant's genetic control, making plant genetic make-up one of the most significant determinants of rhizobacterial selection. Even opportunistic use of root exudates as metabolic fuel will attract only those bacteria equipped to make use of the nutrients that are extant and at the same time capable of adapting to the rhizosphere environment. The unique exudate cocktails released by different plant species therefore signal to and attract a specific bacterial assemblage in a reproducible manner, explaining the well established role of plant species in rhizobacterial community selection. 3,4 Using various Arabidopsis thaliana accessions, we have previously shown that the plant genetic control of rhizobacterial recruitment is so tightly regulated that even genetic variants of the same plant species se...

Rhizosphere microbiome assemblage is affected by plant development

“…While these studies demonstrated that plant microbial communities change in response to plant development they were not able to distinguish how or which microbes contribute to the changes observed. For example, Micallef et al (2009a) through denaturing gradient gel electrophoresis analysis observed that Arabidopsis rhizosphere microbial communities varied with plant development and that microbial communities in early plant development were more distinct to the bulk soil and that this difference decreased with plant age. Similarly, an assessment of the potato rhizosphere demonstrated that young potato plants showed cultivar-dependent rhizosphere microbial communities but these differences in the microbiomes disappeared as the plants aged (Inceoglu et al, 2011).…”

“…Here, we tested this hypothesis by analyzing the rhizosphere microbial composition of Arabidopsis by 454 pyrosequencing at four distinct physiological stages of development: seedling (four-five leaf stage), vegetative (rosette), bolting and flowering. We did not include samples past the flowering stage because previous studies have determined that rhizosphere microbial communities converge past the flowering stage (Micallef et al, 2009a;Lundberg et al, 2012). Further, a metatranscriptomics analysis of the rhizomicrobiome was also conducted to ascertain a relationship between plant growth and microbiome functioning.…”

“…Studies have shown that rhizospheric fungal and bacterial communities of a wide range of plants (i.e., Arabidopsis, Medicago, maize, pea, wheat and sugar beet) change according to a plant developmental gradient (Baudoin et al, 2002;Mougel et al, 2006;Houlden et al, 2008;Micallef et al, 2009a). In these studies the microbial communities were assessed through automated ribosomal intergenic spacer analysis or denaturing gradient gel electrophoresis techniques that produce a fingerprint of the community structure but not of its members' identity.…”

Spatio Temporal Influence of Isoflavonoids on Bacterial Diversity in the Soybean Rhizosphere

“…Rhizodeposits are composed of sugars, amino acids, organic acids, fatty acids, proteins, ions, secondary metabolites, mucilage, water, and miscellaneous carbon-containing compounds (Bais et al 2006;Dennis et al 2010). Significant evidence accumulated over the years indicates that the composition of root microbial communities is influenced, in large part, by the plant species and its developmental stage (Micallef et al 2009;Mougel et al 2006;Weisskopf et al 2006). Indeed, an intricate coevolution of plants and rhizosphere microbial communities was suggested by the observation that resident plants or their root exudates are capable of maintaining the biomass and diversity of soil fungal communities to a much greater extent than nonresident or introduced plants ).…”

Early Changes in Soil Metabolic Diversity and Bacterial Community Structure in Sugarcane under Two Harvest Management Systems

“…Differences in morphological and physiological features of roots among sugarcane cultivars may exist, as reported for the uptake capacity per unit of dry matter and for root branching, suggesting differences in the efficiency of C allocation and in acquisition of water and nutrients among sugarcane genotypes . Additionally, other studies have shown differences in the soil microbiota due to the plant genotype and its rhizospheric effect (Marschner et al, 2006;Schweitzer et al, 2008;Micallef et al, 2009). Changes in the structure of the microbial community and functional diversity due to plant genotype were also observed by Dunfield and Germida (2001) analyzing fatty acid profiles and C-substrate utilization in the rhizosphere of brassica spp.…”