Diffusible signal factor primes plant immunity against Xanthomonas campestris pv. campestris (Xcc) via JA signaling in Arabidopsis and Brassica oleracea

Qian Zhao; Fang Liu; Cong Song; Tingting Zhai; Ziwei He; Limei Ma; Xuemeng Zhao; Zhenhua Jia; Shuishan Song

doi:10.3389/fcimb.2023.1203582

Diffusible signal factor primes plant immunity against Xanthomonas campestris pv. campestris (Xcc) via JA signaling in Arabidopsis and Brassica oleracea

Front Cell Infect Microbiol. 2023 Jun 19:13:1203582. doi: 10.3389/fcimb.2023.1203582. eCollection 2023.

Authors

Qian Zhao^{1

2}, Fang Liu³, Cong Song^{1

2}, Tingting Zhai¹, Ziwei He¹, Limei Ma^{1

2}, Xuemeng Zhao¹, Zhenhua Jia^{1

2}, Shuishan Song^{1

2}

Affiliations

¹ Biology Institute, Hebei Academy of Sciences, Shijiazhuang, China.
² Hebei Technology Innovation Center of Microbiological Control on Main Crop Disease, Shijiazhuang, China.
³ Shijiazhuang Academy of Agricultural and Forestry Sciences, Shijiazhuang, China.

Abstract

Background: Many Gram-negative bacteria use quorum sensing (QS) signal molecules to monitor their local population density and to coordinate their collective behaviors. The diffusible signal factor (DSF) family represents an intriguing type of QS signal to mediate intraspecies and interspecies communication. Recently, accumulating evidence demonstrates the role of DSF in mediating inter-kingdom communication between DSF-producing bacteria and plants. However, the regulatory mechanism of DSF during the Xanthomonas-plant interactions remain unclear.

Methods: Plants were pretreated with different concentration of DSF and subsequent inoculated with pathogen Xanthomonas campestris pv. campestris (Xcc). Pathogenicity, phynotypic analysis, transcriptome combined with metabolome analysis, genetic analysis and gene expression analysis were used to evaluate the priming effects of DSF on plant disease resistance.

Results: We found that the low concentration of DSF could prime plant immunity against Xcc in both Brassica oleracea and Arabidopsis thaliana. Pretreatment with DSF and subsequent pathogen invasion triggered an augmented burst of ROS by DCFH-DA and DAB staining. CAT application could attenuate the level of ROS induced by DSF. The expression of RBOHD and RBOHF were up-regulated and the activities of antioxidases POD increased after DSF treatment followed by Xcc inoculation. Transcriptome combined with metabolome analysis showed that plant hormone jasmonic acid (JA) signaling involved in DSF-primed resistance to Xcc in Arabidopsis. The expression of JA synthesis genes (AOC2, AOS, LOX2, OPR3 and JAR1), transportor gene (JAT1), regulator genes (JAZ1 and MYC2) and responsive genes (VSP2, PDF1.2 and Thi2.1) were up-regulated significantly by DSF upon Xcc challenge. The primed effects were not observed in JA relevant mutant coi1-1 and jar1-1.

Conclusion: These results indicated that DSF-primed resistance against Xcc was dependent on the JA pathway. Our findings advanced the understanding of QS signal-mediated communication and provide a new strategy for the control of black rot in Brassica oleracea.

Keywords: DSF; Jasmonic acid; Xanthomonas campestris pv. campestris; plant immunity; priming; quorum sensing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arabidopsis* / genetics
Arabidopsis* / metabolism
Bacterial Proteins / genetics
Brassica* / metabolism
Plant Diseases / microbiology
Plant Immunity
Reactive Oxygen Species / metabolism
Xanthomonas campestris* / genetics
Xanthomonas campestris* / metabolism

Substances

jasmonic acid
Reactive Oxygen Species
Bacterial Proteins

Grants and funding

This work was financially supported by a project from the Central Guidance on Local Science and Technology Development Fund of Hebei Province (226Z6501G), the National Natural Science Foundation of China (No. 31601144), the National Basic Research Program of China (No. 2015CB150604), and the Science and Technology project of Hebei Academy of Sciences (22304).