
Article, November 20, 2024,
Nature Communications, [Impact Factor = 14.7]
DOI: https://doi.org/10.1038/s41467-024-54417-5
First Authors: Wang Zhenghong, Li Zewen
Corresponding Author: Song Yi
Co-authors: Zhang Yujie; Liao Jingye; Guan Kaixiang; Zhai Jingxuan; Meng Pengfei; Tang Xianli; Dong Tao
Affiliation: School of Life Sciences, Southern University of Science and Technology, Institute of Plant and Food Research
This study references the Jiupo Plant Growth Chamber BPC500H and aims to analyze the impact of root hair development regulatory factors on the composition and assembly patterns of root-associated microbial communities under drought conditions through microbiome sequencing. It further identifies key microbial groups or taxa affected by root hair regulatory factors under drought. Additionally, the study validates the drought-protective effects (phenotypic) of key microbes and their plant protection mechanisms (transcriptional responses) through microbiological cultivation-based genomics. Combining metagenomics, the research identifies key functional genes in microbes and verifies them through genetic manipulation. The overall goal is to explore the interaction and regulatory mechanisms between plants and microbes mediated by root hair development factors under drought stress.

As root hairs are essential for plant root water absorption and interactions with microbes, Song Yi’s research group at Southern University of Science and Technology used multiple root hair development (root hair density decrease and increase) mutants to discover that the gl2 multi-root hair mutant can induce specific assembly of the root microbial community under drought and specifically enrich beneficial rhizobia. Through high-throughput strain isolation, PEG plate, and soil system-based microbial verification, the study confirms that rhizobia strains affected by root hair-related mutants enhance plant drought resistance, revealing the underlying transcriptomic mechanisms. Furthermore, metagenomic studies show that under drought, key functional genes involved in microbial arginine and proline metabolism pathways (such as the ocd gene encoding ornithine cyclodeaminase) are significantly enriched in the gl2 root microbiome. Bacterial knockout experiments demonstrate that this gene significantly affects the drought tolerance of rhizobia under oxidative stress and significantly reduces its plant drought alleviation effects. This research integrates genetics and multi-omics methods to confirm the role of host genetic effects in the dynamic interactions between plants and microbes under drought and reveals the non-biological stress protection mechanisms mediated by rhizobia. It expands understanding of the physiological and ecological mechanisms of beneficial interactions between non-leguminous plants and rhizobia under stress conditions.

Figure 1: Root Hair Development Regulatory Factors Significantly Affect Root-Associated Microbial Community Composition Under Drought and Induce Specific Root Microbial Assembly in gl2 Mutants.
a-b. Alpha and beta diversity of root-associated microbiomes across genotypes.
c-d. Root microbial assembly patterns and relative contributions of different driving factors across genotypes.

Figure 2: Multi-Omics Analysis Reveals Drought-Protective Function of Rhizobial Strains and Their Dependence on the Key Gene ocd in Proline Metabolism Pathway for Growth, Oxidative Stress Adaptation, and Plant Drought Protection Effects.
a. Schematic diagram of the ocd gene in the Rhizobium sp. 4F10 genome.
b. ocd gene-mediated conversion of L-Ornithine to L-Proline.
c-e. Phenotypic analysis of Rhizobium sp. 4F10 and its mutant △ocd for root growth and fresh weight under inoculation.
f. Growth rate differences between Rhizobium sp. 4F10 and △ocd.
g-h. Differences in oxidative stress adaptation between Rhizobium sp. 4F10 and △ocd.

Figure 3: Model of Root-Rhizobium Interaction Under Drought Conditions.
a. Mutants with different root hair regulatory factors impact root metabolites (such as amino acids and flavonoids) under drought. The gl2 mutant induces deterministic root microbial assembly under drought and specifically enriches rhizobial species, increasing their importance in the microbial network. Additionally, the gl2 root microbiome enriches microbial pathways involved in amino acid metabolism and transport.
b. Drought-protective rhizobia induce the biosynthesis of protective sugars (such as trehalose) and enhance the expression of drought-responsive transcription factors (TFs), improving plant drought adaptation. Moreover, rhizobia key genes affect their own growth rate and oxidative stress adaptation under drought, thereby influencing their plant drought protection effects.