Tissue Dependence and Differential Cordycepin Sensitivity of Race-Specific Resistance Responses in the Barley—Powdery Mildew Interaction

Abstract

Epidermal cell monolayers prepared from partially dissected barley (Hordeum vulgare) coleoptiles were used for in vivo analysis of race-specific resistance to powdery mildew (Erysiphe graminis f. sp. hordei) specified by host genes Mla-1, Mla-12, and Mlg. Complete resistance governed by each of these genes is closely associated with hypersensitive cell death (hypersensitive response, HR) in primary leaf tissue. In contrast, Mla-12 coleoptile tissue reveals a fully compatible, Mla-1 coleoptile tissue a partially compatible, and Mlg coleoptile tissue an incompatible interaction upon challenge with pathogen races carrying corresponding avirulence functions. Quantitative recording of single plant-fungus interaction sites showed arrest of fungal development in papillae on Mlg coleoptiles. On Mla-1 and Mla-12 coleoptiles, attacked cells become predominantly penetrated by the fungus. Approximately one third of penetrated cells on Mla-1 coleoptiles subsequently undergo an HR. These sites reveal no further fungal development. Both Mlg and Mla-12 coleoptiles fail to mount an HR. The effect of cordycepin (3′-deoxyadenosine), an inhibitor of mRNA synthesis, was studied in planta on primary leaf tissue of Mla-12 and Mlg genotypes. Host cell death triggered by either gene is reduced to background levels observed in the near-isogenic compatible interaction and exhibits the same dose-dependent cordycepin sensitivity. Inhibition of Mlg-triggered, single-cell HR is not accompanied by release of fungal growth arrest, indicating cordycepin insensitivity of a papillae-associated resistance component. The data suggest that host cell death is a requisite component for expression of Mla-type but not Mlg-type resistance.

Multiple Avirulence Paralogues in Cereal Powdery Mildew Fungi May Contribute to Parasite Fitness and Defeat of Plant Resistance

“…This indicated that cell death does not always occur in cells expressing the AVR gene and that other changes have prevented the establishment of a successful infection. Race-specific resistance that does not result in cell death has been reported previously in both wheat and barley powdery mildew (Schiffer et al, 1997;Li et al, 2005).…”

Programmed cell death in the plant immune system

“…Since then, several natural examples of plant-pathogen interactions resulting in resistance without cell death have been reported, in particular the potato Rx and barley Rrs1 disease resistance genes. [117][118][119][120][121][122][123][124] Additionally, suppressing caspase-like activities (unrelated to metacaspases) in plants inhibits pathogen-induced cell death without affecting disease resistance. 89,125 As described above, elimination of the metacaspase AtMC1 results in drastically reduced HR after infection with incompatible pathogens, but bacterial growth restriction remains unaffected in this mutant.…”

RAR1 Positively Controls Steady State Levels of Barley MLA Resistance Proteins and Enables Sufficient MLA6 Accumulation for Effective Resistance

“…Because epidermal cell monolayers prepared from partially dissected coleoptiles of Mla1 genotypes were shown to mount a race-specific resistance response (including single cell HR; Bushnell and Liu, 1994;Schiffer et al, 1997), epidermal cells must be competent to detect the cognate fungal effector and thus contain presumably very low levels of MLA1.…”