TY - JOUR
T1 - Phage Resistance Reduced the Pathogenicity of Xanthomonas oryzae pv. oryzae on Rice
AU - Liu, Mengju
AU - Tian, Ye
AU - Zaki, Haitham E.M.
AU - Ahmed, Temoor
AU - Yao, Rong
AU - Yan, Chengqi
AU - Leptihn, Sebastian
AU - Loh, Belinda
AU - Shahid, Muhammad Shafiq
AU - Wang, Fang
AU - Chen, Jianping
AU - Li, Bin
N1 - Funding Information:
The work is partially supported by National Key Research and Development Program of Ningbo (2022Z175), National Natural Science Foundation of China (31872017, 32072472), Zhejiang Provincial Natural Science Foundation of China (LZ19C140002), Shanghai Agriculture Applied Technology Development Program (2021-02-08-00-12-F00771), Zhejiang Provincial Project (2019C02006, 2020C02006), State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products (grant number 2010DS700124-ZZ2014;-KF202101;-KF202205). Ministry of Higher Education, Research and Innovation–Oman, The Research Council (TRC), Block Funding Program (BFP), Research Grant (RG), UTAS-Sur, TRC-RG/2022/02.
Publisher Copyright:
© 2022 by the authors.
PY - 2022/8
Y1 - 2022/8
N2 - Plants grow together with microbes that have both negative and positive impacts on the host, while prokaryotes are in turn also hosts for viruses, co-evolving together in a complex interrelationship. Most research focuses on the interaction of either bacterial pathogens interacting with the plant host, or the impact on viruses on their pathogenic bacterial hosts. Few studies have investigated the co-evolution of bacterial pathogens with their host plants as well as with their bacterial viruses. In this work, we aimed to identify the genes that were associated with both phage sensitivity and host pathogenicity of the bacterium Xanthomonas oryzae pv. oryzae (Xoo), which is the most important bacterial rice pathogen. Using the Tn5 transposon mutation technology, we created a library of Xoo strain C2 comprising 4524 mutants, which were subsequently tested for phage infectability. The phage infection tests showed that less than 1% of the mutants (n = 36) were resistant to phage infection, which was attributed to the Tn5 insertion in 19 genes. Interestingly, three out of 19 genes that conveyed resistance to the phage resulted in reduced pathogenicity to rice seedlings compared to the wild type. We identified three genes involved in both phage infection and bacterial virulence, which were studied by knockout mutants and complementation experiments. All of the three knockout mutants were resistant to infection by phage X2, while the complemented strains restored the susceptibility to the bacterial virus. Surprisingly, the genes are also essential for pathogenicity, which we confirmed by single knockout mutants corresponding to the Tn5 mutants. All three genes are involved in lipopolysaccharide synthesis, thus changing the cell envelope surface molecule composition. Our work shows a possible balance in terms of the connection between bacterial virulence and phage resistance, supporting the deployment of phages for the biocontrol of plant pathogens.
AB - Plants grow together with microbes that have both negative and positive impacts on the host, while prokaryotes are in turn also hosts for viruses, co-evolving together in a complex interrelationship. Most research focuses on the interaction of either bacterial pathogens interacting with the plant host, or the impact on viruses on their pathogenic bacterial hosts. Few studies have investigated the co-evolution of bacterial pathogens with their host plants as well as with their bacterial viruses. In this work, we aimed to identify the genes that were associated with both phage sensitivity and host pathogenicity of the bacterium Xanthomonas oryzae pv. oryzae (Xoo), which is the most important bacterial rice pathogen. Using the Tn5 transposon mutation technology, we created a library of Xoo strain C2 comprising 4524 mutants, which were subsequently tested for phage infectability. The phage infection tests showed that less than 1% of the mutants (n = 36) were resistant to phage infection, which was attributed to the Tn5 insertion in 19 genes. Interestingly, three out of 19 genes that conveyed resistance to the phage resulted in reduced pathogenicity to rice seedlings compared to the wild type. We identified three genes involved in both phage infection and bacterial virulence, which were studied by knockout mutants and complementation experiments. All of the three knockout mutants were resistant to infection by phage X2, while the complemented strains restored the susceptibility to the bacterial virus. Surprisingly, the genes are also essential for pathogenicity, which we confirmed by single knockout mutants corresponding to the Tn5 mutants. All three genes are involved in lipopolysaccharide synthesis, thus changing the cell envelope surface molecule composition. Our work shows a possible balance in terms of the connection between bacterial virulence and phage resistance, supporting the deployment of phages for the biocontrol of plant pathogens.
KW - Xanthomonas oryzae pv. oryzae
KW - gene
KW - lipopolysaccharide
KW - pathogenicity
KW - phage
UR - http://www.scopus.com/inward/record.url?scp=85136670739&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85136670739&partnerID=8YFLogxK
U2 - 10.3390/v14081770
DO - 10.3390/v14081770
M3 - Article
C2 - 36016392
AN - SCOPUS:85136670739
SN - 1999-4915
VL - 14
JO - Viruses
JF - Viruses
IS - 8
M1 - 1770
ER -