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John succeeded his father as elector in 1486, while the Franconian possessions of the Hohenzollern dynasty passed to his younger brothers Frederick I and Siegmund. He decreed that the Stadtschloss in Berlin, erected at the behest of his uncle Frederick II, should serve as the permanent residence of the Brandenburg electors, the beginning of the city's history as a state capital. He also implemented an excise tax on beer in 1488, which sparked several disturbances, mainly in the towns of the Altmark region.
In 1490 John was able to purchase the former Lusatian territory around Zossen, acknowledged by the Bohemian king Vladislaus II, and maintained the succession claims of the Hohenzollern dynasty to the Pomeranian lands held by the House of Griffins. He died in 1499 from pleural effusion at Arneburg Castle and was succeeded by his eldest son Joachim I. John was the first of the Hohenzollern electors to be buried in Brandenburg, first at Lehnin Abbey, later transferred to Berlin Cathedral by order of his grandson Joachim II.