Legacy of land use history determines reprogramming of plant physiology by soil microbiome

Abstract Microorganisms associated with roots are thought to be part of the so-called extended plant phenotypes with roles in the acquisition of nutrients, production of growth hormones, and defense against diseases. Since the crops selectively enrich most rhizosphere microbes out of the bulk soil, we hypothesized that changes in the composition of bulk soil communities caused by agricultural management affect the extended plant phenotype. In the current study, we performed shotgun metagenome sequencing of the rhizosphere microbiome of the peanut (Arachis hypogaea) and metatranscriptome analysis of the roots of peanut plants grown in the soil with different management histories, peanut monocropping and crop rotation. We found that the past planting record had a significant effect on the assembly of the microbial community in the peanut rhizosphere, indicating a soil memory effect. Monocropping resulted in a reduction of the rhizosphere microbial diversity, an enrichment of several rare species, and a reduced representation of traits related to plant performance, such as nutrients metabolism and phytohormone biosynthesis. Furthermore, peanut plants in monocropped soil exhibited a significant reduction in growth coinciding with a down-regulation of genes related to hormone production, mainly auxin and cytokinin, and up-regulation of genes related to the abscisic acid, salicylic acid, jasmonic acid, and ethylene pathways. These findings suggest that land use history affects crop rhizosphere microbiomes and plant physiology.