Ustilago maydis Nit2 Regulates Nitrate Utilisation During Biotrophy and Affects Amino Acid Metabolism of Galls Under Nitrogen Depletion
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Wiley
Abstract
In previous work, we have shown that the transcription factor Nit2 plays a major role in the utilisation of non-favoured
nitrogen
sources like nitrate, minor amino acids or nucleobases in saprotrophic sporidia of the basidiomycete corn smut fungus Ustilago
maydis. Addressing the knowledge gap regarding how filamentous phytopathogens adapt to nitrogen limitation in the host plant,
we employed Δnit2 mutants in the natural FB1 × FB2 background to identify Nit2-regulated
genes during biotrophy. We further
investigated the impact of Nit2 on the physiology of leaf galls in nitrogen-replete
versus nitrogen-limited
host plants by comparative
RNA-Seq
and metabolic steady state analysis. About one third of the fungal genes affected by Nit2 during biotrophy were
involved in nitrogen metabolism and transport, only showing minor overlap to saprotrophic sporidia. Induction of the nitrate
assimilation cluster was completely dependent on Nit2 during biotrophy. In nitrogen-limited
host plants, Δnit2 leaf galls accumulated
nitrate and showed reduced accumulation of the nitrogen-rich
phloem transport amino acids asparagine and glutamine
compared to wild-type
galls. However, total protein content in galls and pathogenicity were comparable between fungal genotypes
in both nitrogen regimes. The findings of our physiological and transcriptomic analysis demonstrate that nitrate utilisation
is dispensable for U. maydis during biotrophy and can likely be actively compensated by increased utilisation of abundant organic
nitrogen sources, like asparagine, GABA and glutamine in a partially Nit2-dependent
fashion.
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