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Chapter 39 : Ustilago maydis and Maize: a Delightful Interaction
Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis
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Understanding the molecular mechanisms of the interaction of Ustilago maydis with maize entails understanding the molecular mechanisms that regulate its life cycle. This chapter presents an overview of the current knowledge regarding the interaction of Ustilago maydis with maize. First, useful features that have facilitated analysis of the life cycle are described, followed by a brief synopsis of the morphological transitions that characterize the life cycle and their control by the mating-type loci and the mitogen-activated protein kinase (MAPK) and cyclic AMP (cAMP) signal transduction pathways. Lastly, specific genes known to be required or to be expressed at different stages of the infectious cycle are described. Infection of anthers at various developmental stages not only induces tumors but can also cause aberrant development of different parts of the anther. Thus, infections with U. maydis may provide important insights about floral development in maize. Hyphal fragmentation occurs within the tumors, though it has been reported that this process can occur between cells. Studies that utilized different maize lines suggested that the host can modulate the course of infection. Analysis of mutants in combination with sophisticated imaging techniques and the application of expression profiling of individual infected versus noninfected cells will allow a more precise dissection of the infectious process and identification of the genes that are differentially regulated in the partners of this “apparent” harmonious interaction.
Life cycle of U. maydis. Modified with permission from Kenaga et al., 1971 .
Life cycle transitions in U. maydis. Three basic forms characterize the life cycle of U. maydis: a yeast-like cell, a filamentous form, and a spore (teliospore). The transition from one form to the other is accompanied by changes in ploidy, growth habit, and ability to induce tumors and entails three processes: meiosis, conjugation, and karyogamy, respectively. The fungus undergoes additional morphological changes in the host that are not observed in culture, suggesting that host signals play an important role in fungal differentiation.
Fungal differentiation in the plant. (A) Fungal hyphae develop appressorium-like structures prior to penetration (not shown; see the text for details). Clamp-like structures (1 and 2) (short branches with Y-shaped septum) are necessary for nuclear partitioning and proliferation (see the text for details). The fungus branches profusely prior to tumor induction. Once tumors are formed, fungal hyphae undergo fragmentation, releasing cylindrical fragments containing a single nucleus (3). These fragments then undergo cell rounding (4) and deposit a specialized cell wall resulting in formation of mature diploid teliospores (5). Arrows point to likely sites of cell wall-remodeling events prior to fragmentation. (B) The teliospore germinates by formation of a short filament, the promycelium. The diploid nucleus migrates into the promycelium to complete meiosis resulting in a four-cell septate promycelium. These four haploid cells are the primary meiotic products. They give rise, by budding, to basidiospores, which in turn produce chains of yeast-like cells by budding. The progeny cells can be isolated by micromanipulation and used for segregation analysis.
Formation of filaments on charcoal agar. Saturated cultures of haploid strains (top four horizontal lines) and Fuz– diploids (bottom four horizontal lines) were costreaked against haploid testers a1 b1, a2 b2, a1 b2, and a2 b1 on charcoal medium and incubated overnight at room temperature. Strains in the horizontal lines are (from top to bottom) a2 b2, a1 b1, a2 b1, a1 b2, a1/a2 b1/b1, a1/a2 b2/b2, a1/a1 b1/b2, and a2/a2 b1/b2. The fuzzy reaction observed is due to formation of filaments. Haploid strains that carry different a and b alleles form dikaryotic filaments when costreaked on this medium (top four reactions). Diploid strains heterozygous at a and homozygous at b or homozygous at a and heterozygous at b form filaments when costreaked with haploid strains that carry a different b allele (regardless of the a allele) or a different a allele (regardless of the b allele), respectively (bottom four reactions). Diploids heterozygous at both a and b form mycelial colonies (not shown). Reproduced from Banuett and Herskowitz, 1989 .
Signal transduction in U. maydis. The MAPK and cAMP signal transduction pathways regulate formation of the infectious filamentous dikaryon and also interaction with the host plant. (A) Pheromones activate a MAPK module consisting of Kpp4/Ubc4, Fuz7/Ubc5, Kpp2/Ubc3, and Crk1. Both Kpp2 and Crk1 activate Prf1, which in turn binds to pheromone response element sites present in the upstream regions of genes in the a locus (mfa1, mfa2, pra1, pra2, and lga2) and the b locus (bW and bE). Activation of the b genes in the haploid ensures that upon fusion of haploid cells containing different b alleles, the active b protein is readily formed and activates the filamentous program and pathogenic development. In addition, Kpp2/Ubc3 acts via an unknown transcriptional activator to control formation of conjugation tubes, which mediate cell fusion. Ubc2, an adaptor protein, interacts with Kpp4/Ubc4. Smu1 (Ste20) is likely upstream of the MAPK module, though this remains to be determined. Ras2 is proposed to act upstream of the MAPK module (see the text). (B) Once the filamentous dikaryon is formed in the plant, the same MAPK module and another MAPK (Kpp6) in response to putative plant signals activate appressorium formation (Kpp2/Ubc3), cuticle penetration (Kpp6), and filamentous growth and pathogenicity. (C) The signals that activate the cAMP and pheromone response MAPK pathways converge on Prf1. Prf1 is phosphorylated by the MAPKs Kpp2/Ubc3 and Crk1 and by Adr1, the catalytic subunit of PKA. Gpa3 activates the cAMP pathway in response to pheromones and to nutritional inputs, including lipids and phosphate (see the text). Components of the cAMP pathway play roles at various stages of the infectious cycle (see the text).
Genes required for pathogenicity