The Tin2 effector of U. maydis has been neofunctionalized

The Tin2 effector of U. maydis is one of the few effectors whose molecular function has been elucidated. Tin2 stabilizes the maize protein kinase TTK1 which regulates anthocyanin biosynthesis. The induction of anthocyanin biosynthesis is considered to deplete the levels of p-coumarate which is also a precursor for lignin biosynthesis. A reduction in lignification is important for fungal spreading in the infected tissue. We now functionally compared Tin2 effectors of U. maydis and the related smut fungus Sporisorium reilianumS. reilianum also infects maize but causes symptoms only in the inflorescences and fails to induce anthocyanin (Figure 7). S. reilianum harbors a gene related to tin2 of U. maydis at a syntenic position in the genome. The S. reilianum tin2 gene also contributed to virulence. We showed that Tin2 effectors from both fungi target distinct paralogues of the maize protein kinase TTK1, leading to stabilization and inhibition, respectively. We also reconstructed an ancestral Tin2 effector and demonstrated that it could functionally replace 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 the ability of U. maydis Tin2 to induce anthocyanin is an acquired specialized function. We consider it likely that this specialized function is connected to the distinct pathogenic lifestyle of this fungus and the ability to induce tumors in leaves, a phenotype not shared by S. reilianum.

Figure 7: U. maydis and S. reilianum disease symptoms in maize. A) Symptoms of both smut fungi in cobs. U. maydis induces large tumors containing spores while S. reilianum converts kernel tissue to spore masses without prior induction of tumors. B) Symptoms of both smut fungi in leaves. U. maydis induces tumors and anthocyanin while S. reilianum infected leaves lack visible disease symptoms, although they are colonized.
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