The Barley MLO Modulator of Defense and Cell Death Is Responsive to Biotic and Abiotic Stress Stimuli

Abstract

Lack of the barley (Hordeum vulgare) seven-transmembrane domain MLO protein confers resistance against the fungal pathogen Blumeria graminis f. sp. hordei (Bgh). To broaden the basis for MLO structure/function studies, we sequenced additional mlo resistance alleles, two of which confer only partial resistance. Wild-type MLO dampens the cell wall-restricted hydrogen peroxide burst at points of attempted fungal penetration of the epidermal cell wall, and in subtending mesophyll cells, it suppresses a second oxidative burst and cell death. Although the Bgh-induced cell death in mlo plants is spatially and temporally separated from resistance, we show that the two processes are linked. Uninoculated mutant mlo plants exhibit spontaneous mesophyll cell death that appears to be part of accelerated leaf senescence. Mlo transcript abundance increases in response to Bgh, rice (Oryza sativa) blast, wounding, paraquat treatment, a wheat powdery mildew-derived carbohydrate elicitor, and during leaf senescence. This suggests a broad involvement of Mlo in cell death protection and in responses to biotic and abiotic stresses.Homozygous mutant (mlo) alleles of the Mlo gene confer broad spectrum disease resistance to the biotrophic powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh; Jørgensen, 1992). The resistance is manifested in the failure of the fungus to penetrate the epidermal cell wall, and at these sites, cell wall remodeling and oxidative cross-linking processes fortify the cell wall (Thordal-Christensen et al., 1997; von Rö penack et al., 1998; Hü ckelhoven et al., 1999). Although cell wall reinforcement is likely to contribute to the resistant phenotype, other yet unknown molecular events may lead to abortion of fungal attack. Although the wild-type Mlo gene in effect acts as a negative regulator of a defense response, wildtype Ror1 and Ror2 are two genes that are required for full expression of mlo resistance to Bgh, but not race-specific resistance (Freialdenhoven et al., 1996; Peterhänsel et al., 1997). It is curious that powdery mildew-resistant mlo plants exhibit enhanced susceptibility to the fungal pathogens Magnaporthe grisea and Bipolaris sorokiniana (Jarosch et al., 1999; Kumar et al., 2001).Mutant mlo plants exhibit a spontaneous mesophyll cell death phenotype that is compromised by ror1 and ror2 mutations (Wolter et al., 1993; Peterhänsel et al., 1997). In this respect, mlo mutations resemble other mutations known to enhance host cell death processes along with disease resistance (Shirasu and SchulzeLefert, 2000). Many of these mutants constitutively express pathogen-related (PR) genes, but in barley (Hordeum vulgare) mlo, maize (Zea mays) lls1, and Arabidopsis lsd1 and edr1 plants, pathogen inoculation is required to trigger an enhanced defense response (Jabs et al., 1996; Frye and Innes, 1998; Simmons et al., 1998). These four genes have been isolated (Bü schges et al., 1997; Dietrich et al., 1997; Gray et al., 1997; Frye et al., 2001), and encode dissimilar proteins.Barley MLO is the pro...

Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain

“…This finding is surprising because apoplastic oxidative microbursts (revealed by hydrogen peroxide accumulation) are known to take place underneath both primary and AGTs, demonstrating that each germ tube is capable of eliciting a subcellular defense response at the cell periphery of attacked host cells (17,23). Although the enzyme(s) generating these oxidative microbursts have not been conclusively identified in barley (24,25), it is interesting that treatment of tobacco BY2 cells with cryptogein, a 10-kDa protein secreted by the phytoparasitic oomycete Phytophthora cryptogea, resulted in the accumulation of the NADPH oxidase NtrbohD and its presumed negative regulator, NtRac5, components of the oxi- dative burst machinery, in PM lipid rafts (22).…”

Overexpression of barley BAX inhibitor 1 induces breakdown of mlo -mediated penetration resistance to Blumeria graminis

“…This is most prominently demonstrated by the fact that loss of MLO function leads to both Bgh resistance and spontaneous cell death (14). The functional Mlo gene is expressed in response to pathogens, wounding, reactive oxygen intermediates, and during leaf aging (27). A similar expression profile was found for BI-1 (refs.…”

“…These findings question a physical interaction of MLO and BI-1. We speculate that BI-1 is a mesophyll teammate of epidermis-expressed MLO (27). Interestingly, although MLO is epidermis-specific, mlo mutants show spontaneous cell death especially in the mesophyll (30).…”

Blufensin1Negatively Impacts Basal Defense in Response to Barley Powdery Mildew

“…MLO, as a negative regulator of penetration resistance, but not Mla-mediated hypersensitive response, is essential for compatibility to all known Bgh isolates (Bü schges et al, 1997;Piffanelli et al, 2002). Hypothesized to be a host susceptibility factor, it is believed that MLO is recruited by Bgh to diminish the plant defense response (Bü schges et al, 1997;Devoto et al, 1999).…”