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In this study, Lanz et al. investigated how the Mec1/ATR kinase functions in genome maintenance and replication and, using a novel genetic system to spatially manipulate Mec1 activation and action, show that the ability of Mec1 to suppress genomic instabilities is separate from a novel role in promoting DNA replication. These findings establish that the Mec1/ATR kinase initiates checkpoint signaling, promotes DNA replication, and maintains genetic stability through distinct modes of action.