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Chapter 18 : Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead

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Abstract:

This chapter describes the progress that has been achieved by combining recent molecular studies with older, classical investigations for understanding pheromone signaling. There are approximately 75-100 pheromones and at least 18 pheromone receptors involved in the mating system, complicating initial pheromone recognition in in comparison with . The currently characterized collection of pheromones can be divided into five groups, based on the amino acid sequence similarity of their predicted mature pheromone peptides, and their receptoractivation spectra in transgene experiment. It seems likely that there is an additional purpose for the aromatic amino acids in the carboxy-terminal position in pheromones, because there are only three aromatic residues, and these would not be sufficient to distinguish among all of the pheromones. Recombinant receptor chimeras and site-directed mutagenesis have been used to understand how pheromone receptors specifically recognize pheromones. Pheromone transformants were paired with other transformed strains that were expressing compatible or incompatible receptors and then assayed for diploid formation. This experiment confirmed that pheromone receptors and pheromones function in yeast, each expressing its expected specificity and inducing diploidization in compatible pairings. Two mating processes are known to depend on activation of the B-regulated developmental pathway: nuclear migration and hook cell fusion. Phylogenetic relationships of pheromone receptors of several mushroom species, including , indicate that the subtypes of pheromone receptors that we can recognize today in mushroom fungi diverged in common ancestors of the modern homobasidiomycetes.

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Figures

Image of Figure 18.1
Figure 18.1

The mating process in . Hyphal anastomosis is not regulated by the mating-type genes. Nuclear migration and hook-cell fusion are controlled by the locus, and all the other steps in the process of dikaryon formation are controlled by .

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Image of Figure 18.2
Figure 18.2

The flat phenotype. (a) Hyphae of an unmated homokaryon. (b through d) Hyphae of the common- heterokaryon exhibiting a strong flat phenotype. Abundant short branches and hyphal wall distortions are typical hyphal features. Micrographs by T. Fowler.

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Image of Figure 18.3
Figure 18.3

Arrangement of the locus in . (a) The generalized arrangement of the two subloci and , separated by a region of variable length, is shown. There are nine different haplotypes of and nine different haplotypes of that can associate in most pairwise combinations. (b) The - combination has been completely sequenced and tested in biological activity assays ( ). Squares represent pheromone genes, and rectangles represent receptor genes.

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Image of Figure 18.4
Figure 18.4

Precursors of two related pheromones. The pheromones Bbp2( ) and Bbp2( ) activate the same two receptors, Bbr3 and Bbr9, and have very similar mature sequences (predicted), shown in boldface type. These two pheromone precursors are typical of the pheromones. Amino acid pairs (DK and DS) are thought to mark the sites of protease processing for the N termini (arrow) of the mature pheromone and can be identified readily in most of the known pheromone sequences. The amino acid sequences of the N termini of these two precursors are very different although their C termini (the presumed mature pheromones) are not, also suggesting that the conserved, functional portions (bold) and the nonconserved, nonfunctional portions (italics) are separated at the predicted protease recognition sites. Underlined at the C termini is the CaaX-box motif that is processed to remove the final three amino acids. Following aaX cleavage, the new terminal cysteine is likely carboxymethylated and farnesylated.

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Image of Figure 18.5
Figure 18.5

Some predicted mature pheromones and their biological activities. Predicted pheromones are grouped by sequence similarity ( ), and the receptors activated by each pheromone are indicated by a plus sign (+). Only the peptide portion is shown; each pheromone is presumed to be carboxymethylated and farnesylated on the C-terminal cysteine. The asterisks above two group III amino acid positions were tested in site-directed mutagenesis studies (see the text for details).

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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Image of Figure 18.6
Figure 18.6

Bar1 and Bar2 pheromone receptor chimeras. Bar1 and Bar2 were engineered to produce hybrid receptors that exhibited a variety of phenotypes when exposed to wild-type pheromones in matings (redrawn based on references and ). Some receptor chimeras displayed the selectivity of a wild-type receptor, while other receptor chimeras had the ability to be activated by pheromones from all wild-type haplotypes (“promiscuous”). Still others, including a site-directed mutant, were “super-specific” and excluded more pheromones than the wild-type receptors. One receptor chimera was constitutively activated and required no pheromone for signaling. In these drawings, the dotted lines represent the boundaries of the plasma membrane in which the receptors are anchored. Above the upper dotted line is the extracellular space, and below the lower dotted line is the cytoplasm. The N termini of these receptors are extracellular, and the C termini are intracellular. The intracellular C-terminal portion of each receptor is not drawn representatively but is shortened for convenience.

Citation: Fowler T, Vaillancourt L. 2007. Pheromones and Pheromone Receptors in Mate Recognition: Retrospective of a Half-Century of Progress and a Look Ahead, p 301-315. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555815837.ch18
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