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

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 bacte...

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Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1147351/full
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author 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
author_facet 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
author_sort Hubiao Jiang
collection DOAJ
description 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.
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spelling doaj.art-48ae1420401a4e5a9e5076f0c36f61f92023-04-19T11:30:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-04-011410.3389/fpls.2023.11473511147351Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)Hubiao Jiang0Changxin Li1Xuefang Huang2Temoor Ahmed3Solabomi Olaitan Ogunyemi4Shanhong Yu5Xiao Wang6Hayssam M. Ali7Fahad Khan8Chengqi Yan9Jianping Chen10Bin Li11State 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, ChinaHunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, ChinaState 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, ChinaState 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, ChinaState 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, ChinaTaizhou Academy of Agricultural Sciences, Taizhou, ChinaNingbo Jiangbei District Agricultural Technology Extension Service Station, Ningbo, ChinaDepartment of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi ArabiaTasmanian Institute of Agriculture, University of Tasmania, Launceston, TAS, AustraliaInstitute of Biotechnology, Ningbo Academy of Agricultural Sciences, Ningbo, ChinaState 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, ChinaState 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, ChinaRice 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.https://www.frontiersin.org/articles/10.3389/fpls.2023.1147351/fullphagebacterial leaf blightXanthomonas oryzae pv. oryzaephyllosphere microbiomebiocontrol mechanism
spellingShingle 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
Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
Frontiers in Plant Science
phage
bacterial leaf blight
Xanthomonas oryzae pv. oryzae
phyllosphere microbiome
biocontrol mechanism
title Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
title_full Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
title_fullStr Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
title_full_unstemmed Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
title_short Phage combination alleviates bacterial leaf blight of rice (Oryza sativa L.)
title_sort phage combination alleviates bacterial leaf blight of rice oryza sativa l
topic phage
bacterial leaf blight
Xanthomonas oryzae pv. oryzae
phyllosphere microbiome
biocontrol mechanism
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1147351/full
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