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Abstract

Ustilago maydis is a biotrophic fungus causing smut disease in corn. The
infectious forms are dikaryotic hyphae. Here we analyze mutants lacking
the nlt1 transcription factor and investigate why these mutants are
unable to induce leaf tumors.
The study involved reverse genetics, complementation, epistasis
analysis, microscopy, gene expression analysis by quantitative reverse
transcriptase PCR and virulence assays.
We show that nlt1 mutants colonize maize leaves efficiently but fail to
undergo karyogamy and are attenuated in late proliferation. Nlt1
activates transcription of ros1, a transcription factor controlling
karyogamy, and represses see1, an effector previously shown to
contribute to leaf tumor induction. In mononuclate solopathogenic
strains, nlt1 mutants cause attenuated leaf tumor formation. In actively
dividing maize organs, nlt1 mutants undergo karyogamy and induce tumor
formation. Sporisorium reilianum, a smut fungus unable to induce leaf
tumors, possesses an ortholog of nlt1 that controls the fusion of
dikaryotic nuclei late in infection during cob colonization.
Our results have established a regulatory connection between nlt1, ros1
and see1 and suggest the existence of two stages contributing to leaf
tumor formation, one before nuclear fusion and involving nlt1 and one
after karyogamy that is nlt1 independent.