Giving back to the community: microbial mechanisms of plant–soil interactions

Abstract

Summary1. The role of both plants and soil microbes on ecosystem functioning has been long recognized, but the precise feedback mechanisms between them are more elusive. Definition of these interactions is critical if we aim to achieve an integral understanding of ecosystem functioning, and ultimately explain natural, agricultural and synthetic systems. 2. Advances in genomic technologies and the development of more appropriate statistical, mathematical and computational frameworks enable researchers to almost fully describe and measure the diversity of microbial communities in soil, rhizosphere and plant tissues. Under the scaffold of community ecology, we integrate the observed patterns of microbial diversity with current mechanistic understanding of plant-microbe mutualistic and pathogenic interactions, and propose a model in which plant microbial communities are shaped by different ecological forces differentially through the plant life cycle. 3. The same genomic technologies, applied on natural and reconstructed systems, establish that plant genotype has a small, but significant, effect on the microbial community composition in, on and around plant organs. Despite these advances, technical limitations are still important and only a handful of studies exist where a precise genetic element definitively participates in these interactions. 4. Studies at the field or ecosystem level are dominated by agricultural settings, examining microbial species and communities effects on plant productivity; and conversely, that plant genetics and agricultural practices can potentially impose selective pressures on specific microbes and microbial communities. 5. Revitalized interest in plant-soil microbial feedbacks requires researchers to systematically pose and evaluate more complex hypotheses with increasingly more realistic microbial settings. Despite the advances reviewed here, most studies focus on one aspect of plant, microbe and soil interactions. Experiments that simultaneously and methodically manipulate multiple components are necessary to establish the ecological principles, and molecular mechanisms, which drive microbially mediated plant-soil interactions. This knowledge will be critical to predict how environmental changes affect microbial and plant diversity, and will guide efforts to improve agricultural and conservation practices.

Eco‐evolutionary dynamics in plant–soil feedbacks

“…Changes in the strength or direction of PSF affect species dominance and drive community assembly and successional trajectories (Kardol et al . , Herrera Paredes & Lebeis ).…”

Understanding and exploiting plant beneficial microbes

“…The advent of culture-independent microbial ecology, powered by development of high-throughput analytic technologies, has enabled increasingly systematic study of the plant-associated ecological context in which microbial inoculants could be applied; and of mechanisms of plant control over colonization by beneficial microbes. Novel approaches also offer opportunities to bridge current gaps between plant-productivity phenotypes and understanding of the underlying mechanisms [7–9]. …”

Plant–soil feedbacks: connecting ecosystem ecology and evolution

“…Root exudates structure rhizosphere communities by providing carbohydrate sources and functioning as signalling molecules (Chaparro et al . ; Dighton ; Herrera Paredes & Lebeis ). Plant control on soil and root microbiota has been observed under highly controlled greenhouse, common garden and agricultural settings (Marschner et al .…”

“…While several studies have shown the effects of plant phenotypic variation on soil communities and emergent ecosystem properties over the last decade, far fewer have shown how soil communities may shape plant phenotypes, although that is beginning to change (Friesen et al . ; Revillini, Gehring & Johnson ; Herrera Paredes & Lebeis ; Table ). For example, using an invasive tree Ailanthus altissima , Felker‐Quinn, Bailey & Schweitzer () found that genetic variation and among‐population variation for plant biomass was only expressed when the soil microbial community was living (relative to sterilized controls).…”

“…Topics in this special feature include the evolutionary role of PSF in biodiversity and ecosystem function (Evans et al . ; terHorst & Zee ), local adaptation of soil microbial communities and their reciprocal effects on plant phenotypes (Herrera Paredes & Lebeis ; Revillini, Gehring & Johnson ), phylogenetic responses of plants to soil N, demonstrating large‐scale evolutionary effects of plant–soil linkages (Wooliver et al . ), and finally, the applications and frontiers of PSF under land use and environmental change (de la Pena et al .…”