Hungry for Sex: Differential Roles for Ustilago maydisb Locus Components in Haploid Cells vis à vis Nutritional Availability

Abstract

Mating-types allow single-celled eukaryotic organisms to distinguish self from non-self in preparation for sexual reproduction. The components of mating-type loci provide initial self/non-self-recognition through pheromone and receptor interactions that control early cell fusion events. However, they may also provide a second level of scrutiny that requires differences in alleles leading to production of a transcription factor required for successful downstream developmental pathways after initial cell fusion. Interestingly, the protein subunits of these transcription factors have not been thoroughly examined for their roles, if any, in the haploid cells themselves. In Ustilago maydis, the causative agent of galls in maize plants, the b locus, encoding bEast (bE) and bWest (bW), components of the eventual requisite transcription factor, has been extensively studied for its role in formation of the stable dikaryon after mating and subsequent pathogenic program. Little is known, however, about any roles for bE or bW in haploid cells. Since mating in fungi is often induced under conditions of nitrogen starvation, we have explored connections between the b locus and the nitrogen-sensing and response pathways in U. maydis. We previously identified a connection in haploid cells between the b locus and Ump2, the high-affinity transceptor, a protein that both transports ammonium and triggers filamentous growth as a response to nitrogen starvation. Deletion of the entire b locus abrogates the filamentous response to low ammonium, a phenotype that is rescued by overexpression of Ump2. Here we further investigated the individual roles of bE and bW in haploid cells. We show that bE and bW are expressed differentially in haploid cells starved for ammonium. Their respective deletion elicits different effects on transcription of mating and pathogenic-related genes and, importantly, on the degree of pathogenic development in host plants. This is the first demonstration of a role for these mating locus components on haploid development and the first to demonstrate a connection to the ammonium transceptors.

Smuts to the Power of Three: Biotechnology, Biotrophy, and Basic Biology

“…Wallen and coworkers investigated the gene–gene interaction between the b mating type genes and ump2 encoding an ammonium transporter of U. maydis . They found that bE and bW were expressed to different levels in different haploid strains starved of ammonium, and that bE and bW had different effects on the expression of genes needed for mating and pathogenicity [ 18 ]. Finally, T. Kijpornyongpan and M.C.…”

Vacuolar proteases and autophagy in phytopathogenic fungi: A review

“… The role of autophagy and vacuolar proteases PrA and PrB in the pathosystem of U. maydis , M. oryzae , and A alternata. (A) In the course of an infection by U. maydis , nitrogen scarcity promotes filamentation of haploid sporidia mediated by the bE and bW genes (in an independent and nonredundant manner) and the Ump2 transporter, probably preparing the cells for mating ( Wallen et al, 2021 ). After the mating of two compatible basidiospores, Rbf1 and bE/bW induce cell cycle arrest and dikaryotic filaments extend apically over the host tissue.…”

“…For U. maydis and other fungi, carbon stress conditions existing at distinct stages of the fungal life cycle are able to cause cellular reprogramming, which can be provoked by a number of conditions. For example, the mating process involving the conjugation and fusion of two complementary sporidia of U. maydis is preferably carried out under conditions of starvation or a low nitrogen concentration ( Wallen et al., 2021 ). Apart from its participation in the fungal response to stress conditions, autophagy might play a relevant role in the uniparental inheritance of a2 mitochondria in U. maydis .…”