A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in Arabidopsis

Abstract

Microbe- or host damage-derived patterns mediate activation of pattern-triggered immunity (PTI) in plants. Microbial virulence factor (effector)-triggered immunity (ETI) constitutes a second layer of plant protection against microbial attack. Various necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) produced by bacterial, oomycete and fungal microbes are phytotoxic virulence factors that exert immunogenic activities through phytotoxin-induced host cell damage. We here show that multiple cytotoxic NLPs also carry a pattern of 20 amino acid residues (nlp20) that triggers immunity-associated plant defenses and immunity to microbial infection in Arabidopsis thaliana and related plant species with similar characteristics as the prototype pattern, bacterial flagellin. Characteristic differences in flagellin and nlp20 plant responses exist however, as nlp20s fail to trigger extracellular alkalinization in Arabidopsis cell suspensions and seedling growth inhibition. Immunogenic nlp20 peptide motifs are frequently found in bacterial, oomycete and fungal NLPs. Such an unusually broad taxonomic distribution within three phylogenetic kingdoms is unprecedented among microbe-derived triggers of immune responses in either metazoans or plants. Our findings suggest that cytotoxic NLPs carrying immunogenic nlp20 motifs trigger PTI in two ways as typical patterns and by inflicting host cell damage. We further propose that conserved structures within a microbial virulence factor might have driven the emergence of a plant pattern recognition system mediating PTI. As this is reminiscent of the evolution of immune receptors mediating ETI, our findings support the idea that there is a continuum between PTI and ETI.

From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition

“…Noncytotoxic NLPs discovered from oomycete and fungal species also confer immune activation ability (3). This elicitor activity was further pinpointed to a conserved 20-aa region (nlp20) (13). XEG1, a glycoside hydrolase 12 protein from Phytophthora sojae , is an important virulence factor and also acts as a MAMP in soybean (106).…”

Understanding Plant Immunity as a Surveillance System to Detect Invasion

“…The necrosis and ethylene-inducing peptide 1 (Nep1) was originally identified in culture filtrates from Fusarium oxysporum (7), and numerous homologs, referred to as Nep1-like proteins (NLPs), are encoded by bacteria, fungi, and oomycetes where they can positively contribute to virulence (53,115). Recently, a conserved region of approximately 20-24 amino acids was identified on NLPs (termed nlp20 and nlp24, respectively) that serves as a potent inducer of plant immune responses (16,114). Thus, conserved NLP effectors contain a pattern that acts as a MAMP.…”

“…Also, nlp24 is recognized by some Brassicaceae and distantly related lettuce but not by the more closely related plants A. lyrata, Petroselinum crispum, N. benthamiana, or Solanum spp. (16).…”

Effector Mimics and Integrated Decoys, the Never-Ending Arms Race between Rice and Xanthomonas oryzae

“…As a consequence, Xa1 recognizes an entire effector family, and not as other NLRs, only individual effectors in a very specific manner. This is a new feature of NLR activity that has previously been rather associated with membrane bound receptor complexes which can in certain cases recognize entire, widely distributed effector families (Böhm et al, 2014). …”