Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Drought-Induced Plant Physiology Drives Altered Microbe-Metabolite Interactions Along the Plant Rhizosphere Column

Authors:

Winston Anthony1* (winston.anthony@pnnl.gov), Sumit Purohit2, Anil Battu3, Chaevien Clendinen3, Citlali Garcia-Fonseca4, Kylee Tate3, Yuliya Farris1, Tamas Varga3, Devin Coleman-Derr4, Robert Egbert1, Pubudu Handakumbura3

Institutions:

1Biological Sciences Division, Pacific Northwest National Laboratory; 2Advanced Computing, Mathematics, and Data Division, Pacific Northwest National Laboratory; 3Environmental Molecular Sciences Division, Pacific Northwest National Laboratory; 4Plant Gene Expression Center, USDA-ARS, University of California–Berkeley

URLs:

Goals

The Persistence Control Science Focus Area (PerCon SFA) at Pacific Northwest National Laboratory (PNNL) seeks to understand plant-microbiome interactions in bioenergy crops to establish plant growth–promoting microbiomes that are contained to the rhizosphere of a target plant. This vision requires the discovery of exudate catabolism pathways from plant roots, the elimination of genes that support fitness in bulk soil environments without decreasing rhizosphere fitness, and the engineering of rhizosphere-niche occupation traits in phylogenetically distant bacteria. The team anticipates the impacts of these efforts will be to increase understanding of plant-microbe interactions and to extend high-throughput systems and synthetic biology tools to nonmodel microbes.

Abstract

The rhizosphere represents a critical zone of interaction between plant roots and soil microbiota, harboring complex biotic interactions that are essential for plant and soil health. The intricate nature of these interactions becomes particularly evident under environmental stress conditions such as drought. Though scientists know the soil microbiome changes as soil depth increases, previous research identifying drought-induced shifts in microbial abundance and root exudate composition used homogenized rhizosphere samples, losing spatial resolution.

With the increasing prevalence of drought conditions due to climate change, it is imperative to understand its impact on the rhizosphere. This study aims to elucidate the changes in microbe-metabolite interactions along the rhizosphere column of the bioenergy crop sorghum under drought stress.

The RhizoGrid, a spatial root cartography experimental system, was deployed to monitor variations in root physiology, microbial community assembly, and interactions with root exudates using planar and axial spatial sampling under drought and control conditions.

Investigation reveals a significant spatial organization within the healthy rhizosphere (Figure 1.A). Largely influenced by the enrichment of multiple microbial taxa at shallow depths, Flavisolibacter, Lysobacter, and Ramlibacter genera exhibited noticeable spatial variation, decreasing in abundance in the lower half of the rhizosphere soil column (Figure 1.B). Comprehensive analysis highlighted drought-induced shifts in rhizosphere community composition (Figure 1.C), with a marked decrease in taxa diversity, root exudate complexity, and an increase in intraplanar beta diversity across depth. Alterations in plant root physiology, characterized by reduced root mass and number along the RhizoGrid soil column, and machine learning network analysis of spatial microbe-metabolite patterns (Figure 1.D) define the assembly of a drought-distinct microbiome state in the lower half of the soil column marked by a depletion of various Proteobacteria and a reduction in classes of benzenoid metabolites (Figure 1.E).

These findings underscore the importance of spatial resolution in assessing the rhizosphere’s response to drought, providing valuable insights into the resilience of soil ecosystems and recontextualizing previous work. The team believes this approach will be a model for high-resolution investigation of plant-microbe interactions subjected to environmental stress or the introduction of beneficial or pathogenic agents.

Image

Figure 1. Drought Reshapes the Rhizosphere and Alters Microbe-Metabolite Interactions Along the Plant Rhizosphere Column. (A) Generalized additive model regression fit of microbial abundance data for taxa significantly increasing or decreasing over depth in the rhizosphere. (B) Volcano plot identifying genera with the largest fold-change across depth and colored by their phylum designation. (C) Taxa tree of linear regression analysis identifying cross-sectional differential abundance in taxa between drought and control plants. (D) A spatial mutual-information network of samples with high model importance divides the rhizosphere, with a subnetwork belonging to depths 5 to 10 characterized by the decrease in abundance of Proteobacteria and Benzenoid metabolites.

Funding Information

This research was supported by the U.S. DOE BER program as part of BER’s GSP and is a contribution of the PNNL Secure Biosystems Design SFA “Persistence Control of Engineered Functions in Complex Soil Microbiomes.” PNNL is a multiprogram national laboratory operated by Battelle for DOE under Contract DE-AC05-76RL01830.