Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco

Front Microbiol. 2024 Mar 1:15:1361883. doi: 10.3389/fmicb.2024.1361883. eCollection 2024.

Abstract

The plant microbiota is believed to be an accessory genome that extends plant functions, forming holobionts together with the host plant. Plant disease resistance, therefore, is inextricably linked with plant microbiota, which play important roles in plant growth and health. To explore the relationship between plant microbiota and disease resistance, we investigated the tobacco microbiome of two varieties with contrasting disease-resistance levels to bacterial wilt and black shank diseases. Comparative microbiome analysis indicated that the resistant variety assembled a distinct microbiota with higher network complexity and diversity. While Pseudomonas and Ensifer, which contain biocontrol and beneficial members, were enriched in the rhizosphere of the resistant variety, Ralstonia, a genus including the known causative pathogen, was enriched in the susceptible variety. Metagenome sequencing revealed that biocontrol functions, such as hydrogen cyanide synthase, pyochelin biosynthesis, and arthrofactin-type cyclic lipopeptide synthetase, were more abundant in the resistant variety. Further analysis indicated that contigs encoding the corresponding genes were mostly assigned to Pseudomonas. Among all the metagenome-assembled genomes, positive selection was suggested in the genome assigned to Pseudomonas only in the rhizosphere of the resistant variety. The search of biosynthetic gene clusters in the Pseudomonas genome revealed a non-ribosomal peptide synthetase, the compound of which was brabantamide A, with known antimicrobial activity. Collectively, our study suggests that the plant microbiota might be involved in microbe-mediated disease resistance. Particularly, our results highlight Pseudomonas in the rhizosphere of the disease-resistant variety as a promising biocontrol candidate. Our study may facilitate further screening of bacterial isolates and the targeted design of microbial communities.

Keywords: biocontrol; disease resistance; plant microbiota; positive selection; tobacco microbiome.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the Guizhou Provincial Department of Science and Technology (E2DF028), the Startup Funding of the Chinese Academy of Sciences (2017-020), the National Natural Science Foundation of China (41877400), the National Key Research and Development Project of China (2018YFC1802601), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB40020300), and the State Key Laboratory of Environmental Geochemistry (SKLEG2018911).