Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)

Hubiao Jiang; Changxin Li; Xuefang Huang; Temoor Ahmed; Solabomi Olaitan Ogunyemi; Shanhong Yu; Xiao Wang; Hayssam M Ali; Fahad Khan; Chengqi Yan; Jianping Chen; Bin Li

doi:10.3389/fpls.2023.1147351

Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)

Front Plant Sci. 2023 Apr 19:14:1147351. doi: 10.3389/fpls.2023.1147351. eCollection 2023.

Authors

Affiliations

¹ State Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, Zhejiang University, Hangzhou, China.
² Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, China.
³ Taizhou Academy of Agricultural Sciences, Taizhou, China.
⁴ Ningbo Jiangbei District Agricultural Technology Extension Service Station, Ningbo, China.
⁵ Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia.
⁶ Tasmanian Institute of Agriculture, University of Tasmania, Launceston, TAS, Australia.
⁷ Institute of Biotechnology, Ningbo Academy of Agricultural Sciences, Ningbo, China.
⁸ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, China.

Abstract

Rice bacterial leaf blight (BLB) is the most destructive bacterial diseases caused by Xanthomonas oryzae pv. oryzae (Xoo). Phages have been proposed as a green and efficient strategy to kill bacterial pathogens in crops, however, the mechanism of action of phages in the control of phyllosphere bacterial diseases remain unclear. Here, the glasshouse pot experiment results showed that phage combination could reduce the disease index by up to 64.3%. High-throughput sequencing technology was used to analyze the characteristics of phyllosphere microbiome changes and the results showed that phage combinations restored the impact of pathogen invasion on phyllosphere communities to a certain extent, and increased the diversity of bacterial communities. In addition, the phage combination reduced the relative abundance of epiphytic and endophytic Xoo by 58.9% and 33.9%, respectively. In particular, Sphingomonas and Stenotrophomonas were more abundant. According to structural equation modeling, phage combination directly and indirectly affected the disease index by affecting pathogen Xoo biomass and phage resistance. In summary, phage combination could better decrease the disease index. These findings provide new insights into phage biological control of phyllosphere bacterial diseases, theoretical data support, and new ideas for agricultural green prevention and control of phyllosphere diseases.

Keywords: Xanthomonas oryzae pv. oryzae; bacterial leaf blight; biocontrol mechanism; phage; phyllosphere microbiome.

Grants and funding

This work is financially supported by the National Natural Science Foundation of China (32072472, 31872017), Key Research and Development Program of Zhejiang Province, China (2019C02006), National Key Research and Development Program of Ningbo (2022Z175), Zhejiang Provincial Natural Science Foundation of China (LZ19C140002), Shanghai Agriculture Applied Technology Development Program (2021-02-08-00-12-F00771), Zhejiang Basic Public Welfare Research Plan Project (LGN19C140001), Agricultural and social development project of Jiangbei District, Ningbo in 2021 (2021B01), State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products (grant number 2010DS700124-ZZ2014;-KF202101;-KF202205) and Researchers Supporting Project number (RSP2023R123), King Saud University, Riyadh, Saudi Arabia.