An Investigation into the Involvement of Defense Signaling Pathways in Components of the Nonhost Resistance of Arabidopsis thaliana to Rust Fungi Also Reveals a Model System for Studying Rust Fungal Compatibility

Abstract

Seventeen accessions of Arabidopsis thaliana inoculated with the cowpea rust fungus Uromyces vignae exhibited a variety of expressions of nonhost resistance, although infection hypha growth typically ceased before the formation of the first haustorium, except in Ws-0. Compared with wild-type plants, there was no increased fungal growth in ndr1 or eds1 mutants defective in two of the signal cascades regulated by the major class of Arabidopsis host resistance genes. However, in the Col-0 background, infection hyphae of U. vignae and two other rust fungi were longer in sid2 mutants defective in an enzyme that synthesizes salicylic acid (SA), in npr1 mutants deficient in a regulator of the expression of SA-dependent pathogenesis related (PR) genes, and in NahG plants containing a bacterial salicylate hydroxylase. Infection hyphae of U. vignae and U. appendiculatus but not of Puccinia helianthi were also longer in jar1 mutants, which are defective in the jasmonic acid defense signaling pathway. Nevertheless, haustorium formation increased only for the Uromyces spp. and only in sid2 mutants or NahG plants. Rather than the hypersensitive cell death that usually accompanies haustorium formation in nonhost plants, Arabidopsis typically encased haustoria in calloselike material. Growing fungal colonies of both Uromyces spp., indicative of a successful biotrophic relationship between plant and fungus, formed in NahG plants, but only U. vignae formed growing colonies in the sid2 mutants and cycloheximide-treated wild-type plants. Growing colonies did not develop in NahG tobacco or tomato plants. These data suggest that nonhost resistance of Arabidopsis to rust fungi primarily involves the restriction of infection hypha growth as a result of defense gene expression. However, there is a subsequent involvement of SA but not SA-dependent PR genes in preventing the Uromyces spp. from forming the first haustorium and establishing a sufficient biotrophic relationship to support further fungal growth. The U. vignae-Arabidopsis combination could allow the application of the powerful genetic capabilities of this model plant to the study of compatibility as well as nonhost resistance to rust fungi.

Specific Targeting of theArabidopsisResistance Protein RPW8.2 to the Interfacial Membrane Encasing the Fungal Haustorium Renders Broad-Spectrum Resistance to Powdery Mildew

“…However, there may exist a mechanistic connection between H 2 O 2 accumulation in the cytoplasm of the invaded cells due to structural perturbation of the EHC (and papillae) and upregulation of SA signaling. Subcellular callosic structures similar to the EHC have long been observed in other host-pathogen interactions (Heath and Heath, 1971;Bushnell, 1972;Donofrio and Delaney, 2001;Mellersh and Heath, 2003;Soylu et al, 2003), suggesting that EHC formation may be a general basal defense mechanism against haustorial invasion and a target for suppression by the pathogens for pathogenesis. Based on the correlation between RPW8.2 expression and H 2 O 2 accumulation in the HC along with EHC formation, one can envision an exquisite postinvasion defense mechanism in Arabidopsis that involves targeting RPW8.2 to the host-pathogen interface to enhance H 2 O 2 accumulation and EHC formation for constraining the haustorium while protecting the host cell itself.…”

ArabidopsisPEN3/PDR8, an ATP Binding Cassette Transporter, Contributes to Nonhost Resistance to Inappropriate Pathogens That Enter by Direct Penetration

“…Although until recently little was known about the biochemical defenses that contribute to nonhost resistance, cytological descriptions suggested that a majority of inappropriate fungal pathogens were unable to breach the plant cell wall and infiltrate host cells (Yun et al, 2003;Zimmerli et al, 2004). However, some variation in penetration efficiency exists among different host and fungal pathogen combinations (Mellersh and Heath, 2003). These studies also showed that plants respond actively to attack by inappropriate pathogens and do not rely solely on preformed and constitutive barriers for protection against inappropriate pathogens (Meyer and Heath, 1988;Zimmerli et al, 2004).…”

“…These studies also showed that plants respond actively to attack by inappropriate pathogens and do not rely solely on preformed and constitutive barriers for protection against inappropriate pathogens (Meyer and Heath, 1988;Zimmerli et al, 2004). Furthermore, it appears that operationally, nonhost resistance can be divided into penetration resistance, barriers limiting entry of the pathogen into cells, and postpenetration resistance, mechanisms that act intracellularly if penetration resistance is overcome (Fernandez and Heath, 1991;Huitema et al, 2003;Mellersh and Heath, 2003;Yun et al, 2003;Zimmerli et al, 2004;Lipka et al, 2005).…”

“…Among the mutants with defects in the salicylic acid (SA) signal transduction pathway, nonhost resistance was diminished in eds1 mutants and transgenic plants with the bacterial NahG gene relative to wild-type plants (Parker et al, 1996;Mellersh and Heath, 2003;Yun et al, 2003;Zimmerli et al, 2004). Using virus-induced gene silencing, the chaperone and chaperone-like proteins HSP70, HSP90, and SGT1, which are thought to stabilize resistance (R) proteins and act upstream of EDS1, were shown to contribute to nonhost resistance in Nicotiana benthamiana (Peart et al, 2002;Kanzaki et al, 2003).…”

Cladosporium fulvum CfHNNI1 induces hypersensitive necrosis, defence gene expression and disease resistance in both host and nonhost plants

“…Preformed defence mechanisms include formation of plant cytoskeleton and barriers against pathogenic invasion (Kobayashi et al 1997;Yun et al 2003), and constitutive accumulation of a variety of secondary metabolites, especially those with antimicrobial activity (Osbourn 1996). Induced defence mechanisms comprise of accumulation of components involved in preformed defence mechanisms, activation of plant defence signalling, accumulation of reactive oxygen species and initiation of hypersensitive response (HR) in some cases (Kamoun et al 1999;Heath 2000;Lauge et al 2000;Mellersh et al 2002;Mellersh and Heath 2003;Christopher-Kozjan and Heath 2003;Shimizu et al 2003;Mysore and Ryu 2004). Some essential nonhost resistance genes have recently been cloned from Arabidopsis.…”