A two‐domain protein triggers heat shock pathway and necrosis pathway both in model plant and nematode

Abstract

The entomopathogen Bacillus thuringiensis is equipped with multiple virulent factors. The genome sequence of B. thuringiensis YBT1520 revealed the presence of a two-domain protein named Nel which is composed of a necrosis-inducing phytophthora protein 1-like domain found in phytopathogens and a ricin B-like lectin domain. The merging of two distantly related domains is relatively rare. Nel induced necrosis and pathogen-triggered immunity (PTI) on model plants. The Nel also exhibited inhibition activity to nematode. Microscopic observation showed that the toxicity of Nel to nematodes targets the intestine. Quantitative proteomics revealed that Nel stimulated the host defence. The Nel thus possesses dual roles, as both toxin and elicitor. Remarkably, the Nel protein triggered a similar response, induction of the heat shock pathway and the necrosis pathway, in both model plants and nematodes. The unusual ability of Nel to function across kingdom suggests a highly conserved mechanism in eukaryotes that predates the divergence of plants and animal. It is also speculated that the two-domain protein is the result of horizontal gene transfer (HGT) between phytopathogens and entomopathogens. Our results provide an example that HGT occurs between members of different species or even genera with lower frequency are particularly important for evolution of new bacterial pathogen lineages with new virulence. Bacillus thuringiensis occupies the same ecological niches, plant and soil, as phytopathogens, providing the opportunity for gene exchange.

The CRISPR-Cas systems were selectively inactivated during evolution of Bacillus cereus group for adaptation to diverse environments

“…As pathogens for insects and nematodes, B. thuringiensis produces diverse virulence factors [39,[61][62][63][64][65]. Production of multiple virulence factors benefits the populations by facilitating host infection, that represent more resources.…”

Bacillus thuringiensis Crystal Protein Cry6Aa Triggers Caenorhabditis elegans Necrosis Pathway Mediated by Aspartic Protease (ASP-1)

“…elegans mediated by ASP-4 [ 43 ]. We recently found a two-domain protein named Nel, which is composed of a necrosis-inducing phytophthora protein 1-like domain found in phytopathogens and a ricin B-like lectin domain, induced necrosis mediated by ASP-4 [ 54 ]. Therefore, we speculate that different aspartyl proteases in the necrosis pathway respond to different death-inducing stimuli.…”

Genetic and Biochemical Characterization of a Gene Operon for trans-Aconitic Acid, a Novel Nematicide from Bacillus thuringiensis

“…Crystallized proteins, such as Cry5, Cry6, Cry13, Cry14, Cry21, and Cry55, are the predominant nematicidal toxins (8 -15), and the application of Cry6A (16) or truncated Cry5B (17) in transgenic plants conferred significantly improved resistance to plant-parasitic nematodes. Meanwhile, chitinases (18), metalloproteinases (1,4), lantibiotics (19), and a two-domain Nel protein (20) of B. thuringiensis are also active against nematodes. In addition to the most studied protein or peptide toxins, B. thuringiensis also secretes small active compounds to intoxicate nematodes.…”