Host Specificity of Sporisorium reilianum Is Tightly Linked to Generation of the Phytoalexin Luteolinidin by Sorghum bicolor

The smut fungus Sporisorium reilianum occurs in two varieties (S. reilianum f. sp. reilianum and S. reilianum f. sp. zeae) that cause head smut disease on sorghum and maize, respectively. Prior to plant infection, compatible haploid sporidia of S. reilianum fuse to form infectious dikaryotic hyphae that penetrate the leaf surface, spread throughout the plant, and reach the inflorescences, in which spore formation occurs. To elucidate the basis of host specificity of the two S. reilianum varieties, we compared disease etiology of S. reilianum f. sp. reilianum and S. reilianum f. sp. zeae on sorghum and maize. Both varieties could penetrate and multiply in both hosts. However, red spots appeared on inoculated leaves after sorghum infection with S. reilianum f. sp. zeae. Using matrix-assisted laser desorption-ionization time of flight analysis of leaf extracts, we show that sorghum reacts with the production of the red and orange phytoalexins luteolinidin and apigeninidin upon colonization by S. reilianum f. sp. zeae but not by S. reilianum f. sp. reilianum. Using in vitro growth assays, we demonstrate that luteolinidin but not apigeninidin slows vegetative growth of both S. reilianum f. sp. zeae and S. reilianum f. sp. reilianum. However, the phytoalexin biosynthesis gene SbDFR3 is only induced in sorghum after infection with S. reilianum f. sp. zeae, as shown by quantitative real-time polymerase chain reaction. This suggests that regulation of luteolinidin biosynthesis determines infection success of S. reilianum on sorghum.