A common toxin fold mediates microbial attack and plant defense

Abstract

Many plant pathogens secrete toxins that enhance microbial virulence by killing host cells. Usually, these toxins are produced by particular microbial taxa, such as bacteria or fungi. In contrast, many bacterial, fungal and oomycete species produce necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) that trigger leaf necrosis and immunity-associated responses in various plants. We have determined the crystal structure of an NLP from the phytopathogenic oomycete Pythium aphanidermatum to 1.35Å resolution. The protein fold exhibits structural similarities to cytolytic toxins produced by marine organisms (actinoporins). Computational modeling of the 3-dimensional structure of NLPs from another oomycete, Phytophthora parasitica, and from the phytopathogenic bacterium, Pectobacterium carotovorum, revealed a high extent of fold conservation. Expression of the 2 oomycete NLPs in an nlp-deficient P. carotovorum strain restored bacterial virulence, suggesting that NLPs of prokaryotic and eukaryotic origins are orthologous proteins. NLP mutant protein analyses revealed that identical structural properties were required to cause plasma membrane permeabilization and cytolysis in plant cells, as well as to restore bacterial virulence. In sum, NLPs are conserved virulence factors whose taxonomic distribution is exceptional for microbial phytotoxins, and that contribute to host infection by plasma membrane destruction and cytolysis. We further show that NLP-mediated phytotoxicity and plant defense gene expression share identical fold requirements, suggesting that toxin-mediated interference with host integrity triggers plant immunity-associated responses. Phytotoxin-induced cellular damage-associated activation of plant defenses is reminiscent of microbial toxin-induced inflammasome activation in vertebrates and may thus constitute another conserved element in animal and plant innate immunity.crystal structure ͉ immunity ͉ pathogen ͉ plant immunity ͉ phytotoxin

Rhamnolipids Elicit Defense Responses and Induce Disease Resistance against Biotrophic, Hemibiotrophic, and Necrotrophic Pathogens That Require Different Signaling Pathways in Arabidopsis and Highlight a Central Role for Salicylic Acid

“…Such a sensor role of the lipid bilayer is quite uncommon considering that plant basal immunity is usually triggered upon recognition of microbial molecular patterns by high-affinity proteic receptors. It is yet unclear whether the induction of the defense response by RLs requires a specific pattern recognition receptor in the plant plasma membrane, as it is the case for flg22 and oligogalacturonides (Gómez-Gómez and Boller, 2000;Brutus et al, 2010) or whether they interfere directly with the plant plasma membrane as it has been postulated for surfactin or Nep1-like proteins (Qutob et al, 2006;Ottmann et al, 2009;Raaijmakers et al, 2010;Henry et al, 2011). However, the similarities in physical and chemical properties of lipopeptides and RLs suggest that RLs could be perceived in the same manner.…”

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

“…They promote the accumulation of reactive oxygen species, pathogenesis-related proteins, and the production of ethylene, as well as callose deposition and localized cell death (1284). Interestingly, these proteins seem to elicit necrosis and ethylene production only in dicotyledonous plants and are inactive in monocots (1285)(1286)(1287)(1288). NPL-encoding genes, however, are also present in pathogens of monocots that do not elicit necrosis, suggesting additional roles (1289).…”

“…NPL-encoding genes, however, are also present in pathogens of monocots that do not elicit necrosis, suggesting additional roles (1289). Despite their diverse distribution across taxa, most of the NPLs share a fold characterized by a heptapeptide (GHRHDWE) motif (1285)(1286)(1287)(1288), although it was shown that only 36% (12 of 33 proteins) of NLPs from Phytophthora possessed a full complement of the amino acids from this domain (1290). T. reesei, T. atroviride, and T. virens have four genes for a putative NEP-like protein domain (IPR008701) (see Fig.…”

Methodology Identification of 18 genes encoding necrosis-inducing proteins from the plant pathogen Phytophthora capsici (Pythiaceae: Oomycetes)

“…Additionally PsojNIP was linked to the transition from biotrophic to the saprotrophic phase in P. sojea (Qutob et al, 2002). Remarkably, it was observed that the crystal structure of an NLP from Pythium aphanidermatum exhibited structural similarities to cytolytic toxins produced by marine organisms, suggesting that this protein contributed to host infection by plasma membrane destruction and cytolysis (Ottmann et al, 2009). However, the reason why Phytophthora species have a large NPP gene family and the roles these genes play during infection process are still unclear.…”