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 maize¹. 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 neofunctionalized. 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.

中文翻译：

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真菌病原体Ustilago maydis中分泌的Tin2效应子的新功能化。

植物病原性真菌通过分泌效应蛋白劫持了它们的宿主。效应子可抑制植物的免疫反应并调节宿主的新陈代谢，从而使病原体受益。黑穗病真菌是生物营养型病原体，也寄生了重要的谷物，包括玉米¹。症状的发展通常仅限于植物的花序。玉米粉虱是一个例外，它能够在玉米的花序和叶片中引起肿瘤，并通过分泌的锡2效应子诱导花青素的生物合成[ ^2,3]。。U. maydis独特生活方式的演变方式还有待阐明。在这里，我们显示了U. maydis中的Tin2已被新功能化。我们在功能上比较了美利坚合众国锡和相关的黑穗病菌（Sporusorium reilianum）的Tin2效应子，后者仅在玉米的花序中导致症状，而不能诱导花色苷。我们显示，来自两种真菌的Tin2效应子均靶向玉米蛋白激酶的不同旁系同源物，分别导致稳定和抑制。祖先的Tin2效应器在功能上替代了S. reilianum Tin2的毒力功能，但未能诱导花青素，并且无法替代美第斯菌中的Tin2。这表明美利坚合众国的Tin2具有特殊的功能，可能与这种真菌的独特致病生活方式有关。