Here, we identified a new member of the Fizzy-related family of APC activators, Cru1, which is required for virulence in the corn smut fungus Ustilago maydis. We show that Cru1 promotes the degradation of B-type cyclins in U. maydis. Cells deficient in the Cru1 protein show defects in cell size, adaptation to nutritional conditions and cell separation. We propose that the phenotypes observed are a consequence of the inability of cru1Δ cells to keep under control the levels of mitotic cyclins during G1. The levels of cru1 mRNA are controlled by nutritional conditions and cAMP levels, implicating the cAMP/protein kinase A pathway in the transmission of environmental conditions to the cell cycle. Cells deficient in Cru1 function are severely impaired in their ability to infect corn plants. This low rate of plant infection is caused by several defects. First, a low level of expression of the pheromone-encoding gene, mfa1, resulted in a low frequency of dikaryotic infective filament formation. Second, proliferation of fungal cells inside the plant is also affected, resulting in the inability to induce tumors in plants. Finally, the formation and germination of teliospores is also impaired. Our results support the hypothesis that virulence and cell cycle are connected in U. maydis. We propose that along the infection process, Cru1 is required to keep the appropriate G1 length necessary for the adaptation of fungal cells to host environment through the different stages of the plant infection.