The idea of employing ligand-receptor pairs in transgenic plants has been pursued most intensively with the goal of generating plants with durable disease resistance, although no commercial product has yet been generated by this approach (14). Plants successfully resist the attack of most potential pathogens in their environment through an efficient nonself recognition system that is similar to the innate immunity system of vertebrates and insects (15). Elicitors, originating from the pathogen or released from the plant cell wall during pathogen attack, are specifically recognized by receptors of the plant plasma membrane and thereby initiate a multicomponent defense response (15,16). Although several such elicitors have been purified and shown to bind specifically to binding sites of the plasma membrane (17), only two genes encoding components of the corresponding plant receptors have been cloned so far (18-20). One encodes the 75-kDa plasma membrane-associated binding protein of the hepta-/3-glucan elicitor from Phytophthora sojae that occurs in various Fabaceae (18,19). Transgenic tomato plants expressing the hepta-j3-glucan-binding protein from soybean display high-
affinity binding sites for this elicitor (19). It is unknown, however, whether these plants display increased resistance toward pathogens harboring the hepta-/3-glucan in their cell walls. A gene encoding a 129-kDa receptor-like kinase apparently involved in the recognition of bacterial flagellin was isolated from A. thaliana (20). Point mutations in different regions of this gene resulted in loss of ligand recognition and elicitor responsiveness (21). Although receptor function of the corresponding plasma membrane protein needs to be demonstrated, it represents an essential component in binding of a 22-amino-acid fragment of flagellin and may play an important role in the recognition of bacterial pathogens by plants (20-22). Overexpression of such receptors involved in nonhost recognition has the potential to increase basal pathogen resistance in many different crop plants.
In addition to the basal nonhost resistance, plants have developed a complex host defense system relying on receptor-mediated recognition of pathogen avirulence (Avr) gene products by plant resistance (/?) gene products (23). The existence of corresponding pairs of Avr and R genes results in an incompatible interaction between the pathogen and its host plant; i.e., disease development is efficiently stopped by the rapid activation of a mul-ticomponent plant defense response. Although evidence for direct ligand/ receptor-type interaction of Avr and R gene products is lacking in most cases, both may be components of larger signal perception complexes, whose formation is required for an incompatible interaction (24). The R genes introduced into crop plants by conventional breeding techniques did function in the expected way, but, with a few exceptions, the resulting resistance was found to lack durability in the field (25). Pathogens could rapidly break R gene-mediated resistance because conventional breeding allowed only the generation of R gene monocultures (23). The availability of a growing number of different cloned R genes directed against specific pathogen races would allow generating transgenic R gene polycultures of crop plants. Using a population of a given crop plant species consisting of individual plants expressing specific R gene patterns would significantly reduce the speed of adaptation of the pathogen and thereby result in an overall reduction of disease development. Interestingly, increasing the level of a specific R gene product by overexpression can activate defense responses in the absence of pathogens and thereby result in broad resistance of the transgenic plants as shown for the Pto gene in tomato (26,27).
A different strategy has been suggested by de Wit involving the coex-pression of pairs of Avr and R genes in one plant (28). This approach requires constitutive expression of a plant R gene and tightly regulated coexpression of a pathogen-derived Avr gene under control of a broadly pathogen-responsive promoter. Transformation of tomato plants carrying the Cf9 resistance gene against Cladosporium fulvum with the Avr9 gene from this fungal pathogen under control of a pathogen-responsive promoter rendered the transgenic plants resistant to a broad spectrum of pathogens (14,29). Although the application of this approach appears to be limited by the lack of functional expression of Cf9 and Avr9 genes in certain crop species, different pairs of matching R and Avr genes may function in different crop species (30-32).
Interestingly, this strategy to generate broad-spectrum disease resistance (28) appears not to be limited to R/Avr gene-mediated plant-pathogen recognition. All plant pathogenic Phytophthora species analyzed so far secrete elicitins, homologous proteinaceous elicitors (33) that induce an efficient resistance response in tobacco and a few other plant species (34). Tobacco plasma membranes harbor high-affinity binding sites for elicitins that appear to function as elicitin receptors (35,36). Phytophthora species pathogenic on tobacco, such as the causal agent of black shank disease, Phytophthora parasitica var. nicotiana, do not produce elicitins and thereby escape recognition (37). Expression of the elicitin cryptogein from Phytophthora cryptogea under control of a strictly pathogen-responsive promoter in tobacco resulted in broad-spectrum resistance of the transgenic plants against P. parasitica var. nicotiana, Thielaviopsis basicola, Erysiphe cichoracearum, and Botrytis cinerea (38).
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