THE TOMATO CF-9 DISEASE RESISTANCE GENE FUNCTIONS IN TOBACCO AND POTATO TO CONFER RESPONSIVENESS TO THE FUNGAL AVIRULENCE GENE-PRODUCT AVR9

The Cf-9 gene encodes an extracytoplasmic leucine-rich repeat protein that confers resistance in tomato to races of the fungus Cladosporium fulvum that express the corresponding avirulence gene Avr9. We investi gated whether the genomic Cf-9 gene functions in potato and tobacco. T ransgenic tobacco and potato plants carrying Cf-9 exhibit a rapid hype rsensitive cell death response (HR) to Avr9 peptide injection. Cf9 tob acco plants were reciprocally crossed to Avr9-producing tobacco. A dev elopmentally regulated seedling lethal phenotype occurred in F-1 proge ny when Cf9 was used as the male parent and Avr9 as the female parent. However, when Cf9 was inherited in the maternal tissue and a heterozy gous Avr9 plant was used as the pollen donor, a much earlier reaction was caused, leading to no germination of any F-1 seed. Detailed analys is of the Avr9-induced responses in Cf9 tobacco leaves revealed that ( 1) most mesophyll cells died within 3 hr (compared with 12 to 16 hr in tomato); (2) the macroscopic HR was visible at an Avr9 titer five tim es lower than that which caused visible symptoms in tomato; (3) the HR invariably extended into noninjected panels of the tobacco leaf; (4) no HR occurred in leaves of young tobacco plants; (5) in older plants, the HR was dramatically enhanced by sequential Avr9 challenges; and ( 6) coexpression of a salicylate hydroxylase transgene (nahG) from Pseu domonas putida reduced the severity of the macroscopic leaf HR and als o restored germination to Cf9 x 35S:Avr9 F-1 seedlings. Simultaneous i ntroduction of Cf-9 homologs (Hcr9-9 genes A and B or D) along with th e native Cf-9 gene did not alter the responses that were specifically induced by Avr9. Various ways to use the Cf-9-Avr9 gene combination to engineer broad-spectrum disease resistance in several solanaceous spe cies are discussed.