A prophage-encoded nonclassical secretory protein of “Candidatus Liberibacter asiaticus” induces a strong immune response in Nicotiana benthamiana and citrus

Abstract

Huanglongbing (HLB), associated with “Candidatus Liberibacter asiaticus” (CLas), is a globally devastating plant disease. The highly reduced genome of CLas encodes a number of secretory proteins. The conserved prophage-encoded protein AGH17470 is herein identified as a nonclassical secretory protein. We confirmed that the N-terminal and C-terminal sequences jointly determine the secretion of AGH17470. The transient expression of AGH17470 protein in Nicotiana benthamiana caused hypersensitive response (HR) cell death in infiltrated leaves and systemically infected leaves as well as the dwarfing of the entire plant, suggesting that AGH17470 is involved in the plant immune response, growth, and development. Overexpression of AGH17470 in N. benthamiana and citrus plants up-regulated the transcription of pathogenesis-related and salicylic acid (SA)-signalling pathway genes and promoted SA accumulation. Furthermore, transient expression of AGH17470 enhanced the resistance of sweet orange to Xanthomonas citri subsp. citri. To our knowledge, AGH17470 is the first prophage-encoded secretory protein demonstrated to elicit an HR and induce a strong plant immune response. The findings have increased our understanding of prophage-encoded secretory protein genes, and the results provide clues as to the plant defence response against CLas.