Rice bacterial leaf blight drives rhizosphere microbial assembly and function adaptation

Author:

Jiang Hubiao1ORCID,Luo Jinyan2,Liu Quanhong1,Ogunyemi Solabomi Olaitan1,Ahmed Temoor1,Li Bing1,Yu Shanhong3,Wang Xiao4,Yan Chenqi5,Chen Jianping6ORCID,Li Bin1ORCID

Affiliation:

1. State Key Laboratory of Rice Biology and Breeding, Institute of Biotechnology, Zhejiang University , Hangzhou , China

2. Department of Plant Quarantine, Shanghai Extension and Service Center of Agriculture Technology , Shanghai, China

3. Taizhou Academy of Agricultural Sciences , Taizhou, China

4. Ningbo Jiangbei District Agricultural Technology Extension Service Station , Ningbo , China

5. Institute of Biotechnology, Ningbo Academy of Agricultural Sciences , Ningbo, China

6. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology , Ningbo University, Ningbo, China

Abstract

ABSTRACT Rice bacterial leaf blight (BLB) is the most destructive phyllosphere bacterial disease caused by Xanthomonas oryzae pv. oryzae . The effect of soil-borne diseases on the rhizosphere microbiome has been extensively investigated. However, the regulatory role of the phyllosphere disease BLB on the rhizosphere microbiome remains unclear. Here, we observed that BLB significantly altered the composition of the bacterial-fungal community in the rhizosphere, decreasing bacterial diversity but not fungal diversity. The scale of inter-kingdom networks in the rhizosphere microbiome of BLB-infected plants was more complex and broader than in healthy plants, while the bacterial community was more vulnerable to BLB than the fungal community. Indeed, the relative abundance of Streptomyces , Chitinophaga , Sphingomonas , and Bacillus was higher in the BLB rhizosphere, which can be explained by their keystone hub taxa status in the rhizosphere co-occurrence network. Null model analysis showed that the deterministic assembly of bacterial communities increased while that of fungi decreased. Additionally, the assembly of bacterial and fungal communities was significantly related to variations in BLB and soil nutrients, especially pH and available phosphorus. Random forest model results showed that the bacterial community in the rhizosphere had a strong potential for predicting BLB. Metagenomic analysis revealed that BLB had a considerable impact on the functional adaptation of the rhizosphere microbiome. Interestingly, the abundance of some functional genes involved in carbon, phosphorus, and methane metabolism increased drastically. IMPORTANCE Our results suggest that rhizosphere bacteria are more sensitive to bacterial leaf blight (BLB) than fungi. BLB infection decreased the diversity of the rhizosphere bacterial community but increased the complexity and size of the rhizosphere microbial community co-occurrence networks. In addition, the relative abundance of the genera Streptomyces , Chitinophaga , Sphingomonas , and Bacillus increased significantly. Finally, these findings contribute to the understanding of plant-microbiome interactions by providing critical insight into the ecological mechanisms by which rhizosphere microbes respond to phyllosphere diseases. In addition, it also lays the foundation and provides data to support the use of plant microbes to promote plant health in sustainable agriculture, providing critical insight into ecological mechanisms.

Funder

National Natural Science Foundation of China

National Key Research and Development Program of Ningbo

Key Research and Development Program of Zhejiang Province, China

Shanghai Agriculture Applied Technology Development Program

Agricultural and Social Development Project of Jiangbei District, Ningbo in 2021

Zhejiang Provincial Natural Science Foundation of China

Zhejiang Basic Public Welfare Research Plan Project

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products

Publisher

American Society for Microbiology

Subject

Infectious Diseases,Cell Biology,Microbiology (medical),Genetics,General Immunology and Microbiology,Ecology,Physiology

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