New Vista in the Elucidation of Mechanisms for Powdery Mildew Resistance

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In a review article, “Closing the ranks to attack by powdery mildew” published in the August, 2000 issue of Trends in Plant Science  (5(8):343-8.), Drs. Paul Schulze-Lefert and J. Vogel of the Sainsbury Lab, John Innes Centre, begin by explaining the phenomenon of host ‘compatibility’ and ‘incompatibility’ to powdery mildew. The discussion focuses on two representative interactions, barley representing a monocot andArabidopsis representing a dicot species. Turns out that resistance to powdery mildew is variety specific i.e., a variety of barley or Arabidopsis may be resistant to a particular race of mildew but susceptible to others. The resistance is conditioned by a pair of genes: one is race-specific resistance (R) in the host and the other, a corresponding fungal avirulence (Avr) gene. This gene-for-gene mechanism has evolved to enable the host plant to recognize invading pathogens.

One of the alleles of the R-gene locus conferring resistance to barley cultivars is Mla contributed by Hordeum spontaneum - a wild relative of barley. This 240 kb long locus contains 11 genes and they are grouped into three distinct families. Their gene products are similar in that they consist of an N-terminal nucleotide-binding (NB) site and C-terminal leucine-rich repeats (LRRs). In fact, the proteins of this class confer resistance to many plant pathogens. The Mla-1 is one of the 11 genes and has been located within the cytoplasm. The fact that this gene is resident within the cytoplasm indicates that the fungus transports Avr proteins across its own plasma membrane and that of the host before the host recognizes the invading pathogen. (The normal alleles of the latter two, Rar1 and ]Rar2, are required for the functioning of Mla)

Within 24 h of inoculation, epidermal cells of a resistant variety containing Mla, show degeneration resulting in their death. In the mutants, mla, rar1 and ra2 cell-death does not occur, indicating that none of the three mutant genes can activate the host’s suicide response. Cell-death occurs as a result of the accumulation of H2O2 in two phases; first, directly below a fungal appressorium, and in the second wave, filling the infected epidermal cell. It has been shown that H2O2 acts as a signaling molecule in cell-death programs. In the mutants, there is no H2O2 accumulation in the second phase and as a result epidermal and mesophyll cells do not perish. Recent studies have shown that Rar1 resides in the cytoplasm and belongs to a novel family of genes producing Zn 2+ binding proteins.

The authors then descibe two outstanding barley samples collected from German Expeditions to Ethiopia in 1937-38. These two samples were found to be resistant to all tested powdery mildew strains caused by inoculation with Blumeria graminis f. sp. hordei isolates. Unlike the dominant R genes, a single recessive gene, designated mlo was found to confer this broad-spectrum resistance. When its wild-type allele Mlo present in susceptible varieties was mutated, several individuals were obtained with a similar broad-spectrum resistance. These mutant strains were found to be free from mildew attacks for more than 20 years. Analysis of the dominant gene Mlo , present in susceptible varieties revealed that it is a plasma membrane protein anchored by seven transmembranes. The wild-type allele does not activate the suicide process as in mutant individuals. Interestingly, 25 genes, similar to the Mlo gene family with almost identical structure and protein properties, have been found in Arabidopsis.

Studies on the mechanisms for an mlo-controlled defense have revealed that concentric rings of new cell walls are formed directly under fungal penetration pegs, creating a structural barrier and at the same time stopping the supply of nutrition to the invading fungus causing its death. In susceptible plants containing the dominant allele Mlo, the invading pathogen penetrates cell walls successfully in the absence of an obstruction.

Unlike barley, the resistance to Erisiphe chicoracearum and E. cruciferarum in Arabidopsis has proved to be polygenic as was revealed by a study of 360 accessions. The nature of resistance in Arabidopsis is less known. However, recent studies have shown that salicylic acid (SA) plays a significant role in limiting powdery mildew growth. Confirmation of the role of SA comes from the results of experiments in which disabling of the SA pathway has increased the growth of the pathogen. In contrast, the compatibility interactions were enhanced following the activation of the SA pathway concomitant with the activation of defense genes such as PR1, PR5, BGL2.

The authors are confident that with the advancement of knowledge in genetic and molecular research in barley and Arabidopsis, it will be possible to determine key components for compatibility and incompatibility to powdery mildews across plant species. For instance, the discovery of a functional homologue of Mlo in Arabidopsis will help elucidate whether the defense response in mlo plants functions only in close relatives of barely such as wheat or it applies to plants of other species too. In this connection the authors describe a recently discovered wheat Mlo ortholog that complements barley mlo null mutants

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