Abstract
Harpins are produced by Gram-negative phytopathogenic bacteria and typically elicit hypersensitive response (HR) in non-host plants. The characterization of harpins in Xanthomonas species is largely unexplored. Here we demonstrate that Xanthomonas produce a highly conserved single-stranded DNA-binding protein (SSBX) that elicits HR in tobacco as by harpin Hpa1. SSBX, like Hpa1, is an acidic, glycine-rich, heat-stable protein that lacks cysteine residues. SSBX-triggered HR in tobacco, as by Hpa1, is characterized by the oxidative burst, the expression of HR markers (HIN1, HSR203J), pathogenesis-related genes, and callose deposition. Both SSBX- and Hpa1-induced HRs can be inhibited by general metabolism inhibitors actinomycin D, cycloheximide, and lanthanum chloride. Furthermore, those HRs activate the expression of BAK1 and BIK1 genes that are essential for induction of mitogen-activated protein kinase (MAPK) and salicylic acid pathways. Once applied to plants, SSBX induces resistance to the fungal pathogen Alternaria alternata and enhances plant growth. When ssbX was deleted in X. oryzae pv. oryzicola, the causal agent of bacterial leaf streak in rice, the resulting ssbXoc mutant was reduced in virulence and bacterial growth in planta, but retained its ability to trigger HR in tobacco. Interestingly, ssbXoc contains an imperfect PIP-box (plant-inducible promoter) and the expression of ssbXoc is regulated by HrpX, which belongs to the AraC family of transcriptional activators. Immunoblotting evidence showed that SSBx secretion requires a functional type-III secretion system as Hpa1 does. This is the first report demonstrating that Xanthomonas produce a highly-conserved SSBX that functions as a harpin-like protein for plant immunity.
Highlights
Plants employ innate immune systems to overcome microbial pathogen infections [1,2]
We demonstrate that single-stranded DNAbinding proteins from Xanthomonas elicit hypersensitive response (HR) in tobacco
This activity was not demonstrated with SSB proteins obtained from other prokayrotes, so it may be a unique feature of Xanthomonas
Summary
Plants employ innate immune systems to overcome microbial pathogen infections [1,2]. Pathogen-associated molecular patterns (PAMPs) comprise a diverse group of molecules such as flagellin [3], EF-Tu [4], chitin [5] and harpins [6,7,8]. Examples of RLKs include flagellin-sensitive 2 (FLS2) [12], the EF-Tu receptor EFR [13], and the chitin elicitor receptor kinase 1 (CERK1) [14] These RLKs take similar roles to proteins encoded by plant resistance (R) genes for pathogen recognition [9,10,15,16]. Signal transduction pathways associated with PTI and ETI include mitogen-activated protein kinase (MAPK) cascades, calcium fluxes, and the activation of reactive oxygen species (ROS). The FLS2/ BAK1 complex phosphorylates BIK1 (Botrytis-induced kinase 1) for signal transduction to the MAPK cascade [21] The latter may activate the expression of WRKY transcription factors that regulate SA-, JA- or Eth-dependent genes by binding the W-box [22]. It is unclear whether the proteins mentioned above are involved in harpin-triggered immunity
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