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Abstract:
Plant-pathogenic fungi hijack their hosts by secreting effector
proteins. Effectors serve to suppress plant immune responses and
modulate the host metabolism to benefit the pathogen. Smut fungi are
biotrophic pathogens that also parasitize important cereals, including
maize(1). Symptom development is usually restricted to the plant
inflorescences. Ustilago maydis is an exception in its ability to cause
tumours in both inflorescences and leaves of maize, and in inducing
anthocyanin biosynthesis through the secreted Tin2 effector(2,3). How
the unique lifestyle of U. maydis has evolved remains to be elucidated.
Here we show that Tin2 in U. maydis has been neo-functionalized. We
functionally compared Tin2 effectors of U. maydis and the related smut
Sporisorium reilianum, which results in symptoms only in the
inflorescences of maize and fails to induce anthocyanin. We show that
Tin2 effectors from both fungi target distinct paralogues of a maize
protein kinase, leading to stabilization and inhibition, respectively.
An ancestral Tin2 effector functionally replaced the virulence function
of S. reilianum Tin2 but failed to induce anthocyanin, and was unable to
substitute for Tin2 in U. maydis. This shows that Tin2 in U. maydis has
acquired a specialized function, probably connected to the distinct
pathogenic lifestyle of this fungus.
