Mechanisms of unisexual mating in Cryptococcus neoformans

Wang, Linqi; Lin, Xiaorong

doi:10.1016/j.fgb.2011.02.001

Cited by 41 publications

(68 citation statements)

References 142 publications

(170 reference statements)

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“…Unisexual mating and opposite-sex mating share similar inducing stimuli and elements of the pheromone response pathway (Hsueh et al 2009;Lin et al 2010;Wang and Lin 2011). However, a key difference is that the homeodomain cell identity determinants Sxi1a and Sxi2a are only required for postfusion steps during opposite-sex mating and are dispensable for unisexual reproduction .…”

Section: Resultsmentioning

confidence: 99%

“…Unisexual and opposite-sex mating involve many shared components, including the Cpk1 MAPK signal transduction cascade that responds to pheromones and governs the dimorphic transition in C. neoformans (Wang and Lin 2011;Hsueh et al 2009;Lin et al 2010). However, the homeodomain cell identity protein Sxi2a encoded by the a mating type locus is present and functions only during a-a mating but not a-a mating.…”

Section: Discussionmentioning

confidence: 99%

“…Because a isolates predominate (.95%) in most naturally occurring C. neoformans populations, and the a mating type is linked to virulence (Kwon-Chung and Bennett 1978;Nielsen et al 2005;Lin et al 2006;Lin 2009), the discovery of a-a unisexual reproduction (samesex mating) suggests how infectious spores can be produced by this almost unisexual pathogen. Although many similarities are shared between opposite-sex and same-sex mating, ongoing studies comparing the underlying mechanisms provide insight into how same-sex mating can contribute in unique ways to the fitness of these pathogenic fungi (Lee et al 2010;Wang and Lin 2011).SIS was first identified during the a-a opposite-sex mating cycle (Wang et al 2010). In this study, we found that a transgene-induced RNAi-dependent sex-induced silencing pathway also operates during a-a unisexual reproduction and that the silencing frequency during opposite-sex mating and same-sex mating is comparable.…”

mentioning

confidence: 99%

“…This observation is similar to our finding with respect to SIS in opposite-sex mating (Wang et al 2010). These findings lead us to propose that the potential high mutational burden due to hyperactive transposons during mating necessitates a mechanism like SIS, which is much more robust than silencing occurring during vegetative mitotic growth, to defend against transposition and thereby guard genomic integrity of the progeny.Unisexual and opposite-sex mating involve many shared components, including the Cpk1 MAPK signal transduction cascade that responds to pheromones and governs the dimorphic transition in C. neoformans (Wang and Lin 2011;Hsueh et al 2009;Lin et al 2010). However, the homeodomain cell identity protein Sxi2a encoded by the a mating type locus is present and functions only during a-a mating but not a-a mating.…”

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confidence: 99%

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Sex-Induced Silencing Operates During Opposite-Sex and Unisexual Reproduction in Cryptococcus neoformans

2013

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Cryptococcus neoformans is a human fungal pathogen that undergoes a dimorphic transition from yeast to hyphae during a-a opposite-sex mating and a-a unisexual reproduction (same-sex mating). Infectious spores are generated during both processes. We previously identified a sex-induced silencing (SIS) pathway in the C. neoformans serotype A var. grubii lineage, in which tandem transgene arrays trigger RNAi-dependent gene silencing at a high frequency during a-a opposite-sex mating, but at an 250-fold lower frequency during asexual mitotic vegetative growth. Here we report that SIS also operates during a-a unisexual reproduction. A self-fertile strain containing either SXI2a-URA5 or NEO-URA5 transgene arrays exhibited an elevated silencing frequency during solo and unisexual mating compared with mitotic vegetative growth. We also found that SIS operates at a similar efficiency on transgene arrays of the same copy number during either a-a unisexual reproduction or a-a opposite-sex mating. URA5-derived small RNAs were detected in the silenced progeny of a-a unisexual reproduction and RNAi core components were required, providing evidence that SIS induced by same-sex mating is also mediated by RNAi via sequence-specific small RNAs. In addition, our data show that the SIS RNAi pathway also operates to defend the genome via squelching transposon activity during same-sex mating as it does during opposite-sex mating. Taken together, our results confirm that SIS is conserved between the divergent C. neoformans serotype A and serotype D cryptic sibling species. COMPLEX genomes have evolved sophisticated mechanisms to sense the presence, and to control the behavior of genomic invaders such as transposable elements and viruses. Among a panoply of diverse strategies, homologydependent gene silencing (HDGS) is a ubiquitous phenomenon among fungi, plants, and animals (Cogoni 2001). HDGS, also known as cosuppression, was first found to be triggered by transgenes, viruses, or unusual duplications of endogenous genes in both plants and fungi (Cogoni et al. 1996;English et al. 1996;Bingham 1997;Cogoni and Macino 1999a). Although a broad variety of HDGS phenomena are known, all of these gene silencing processes are based on the recognition of nucleic acid sequence homology, followed by inactivation of homologous sequences. Gene silencing can occur at a transcriptional or post-transcriptional level involving sequence-specific mRNA degradation. The most studied and best-characterized HDGS phenomenon in fungi is a process known as quelling, which occurs in Neurospora crassa vegetative tissue (Cogoni et al. 1996). Quelling is an RNAi-mediated silencing mechanism that post-transcriptionally inactivates duplicated sequences, in many cases resulting from introduction of transgenes. In quelling, the silenced loci can act in trans, leading to silencing of all homologous genes throughout the genome. The core RNAi components, including Argonaute, Dicer-like proteins, and RNA-dependent RNA polymerase (RdRP), are all required for quellin...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Sex-Induced Silencing Operates During Opposite-Sex and Unisexual Reproduction in Cryptococcus neoformans

2013

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“…On the other hand, the hyphal morphotype assists the fungus in resisting predation from soil amoebae (8), increases its ability to explore the environment (11), and is linked to its unisexual and bisexual reproduction (3,(12)(13)(14). Thus, it is important to understand the factors that promote cryptococcal hyphal growth.Many environmental stimuli and a few cryptococcal factors that promote hyphal growth in C. neoformans have been identified (12,(15)(16)(17)(18). Pheromones are the most prominent cryptococcal molecules that stimulate mating and filamentation.…”

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confidence: 99%

Secreted Acb1 Contributes to the Yeast-to-Hypha Transition in Cryptococcus neoformans

Zhao

Kirkman

et al. 2016

Appl Environ Microbiol

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Adaptation to stress by eukaryotic pathogens is often accompanied by a transition in cellular morphology. The human fungal pathogen Cryptococcus neoformans is known to switch between the yeast and the filamentous form in response to amoebic predation or during mating. As in the classic dimorphic fungal pathogens, the morphotype is associated with the ability of cryptococci to infect various hosts. Many cryptococcal factors and environmental stimuli, including pheromones (small peptides) and nutrient limitation, are known to induce the yeast-to-hypha transition. We recently discovered that secreted matricellular proteins could also act as intercellular signals to promote the yeast-to-hypha transition. Here we show that the secreted acyl coenzyme A (acyl-CoA)-binding protein Acb1 plays an important role in enhancing this morphotype transition. Acb1 does not possess a signal peptide. Its extracellular secretion and, consequently, its function in filamentation are dependent on an unconventional GRASP (Golgi reassembly stacking protein)-dependent secretion pathway. Surprisingly, intracellular recruitment of Acb1 to the secretory vesicles is independent of Grasp. In addition to Acb1, Grasp possibly controls the secretion of other cargos, because the grasp⌬ mutant, but not the acb1⌬ mutant, is defective in capsule production and macrophage phagocytosis. Nonetheless, Acb1 is likely the major or the sole effector of Grasp in terms of filamentation. Furthermore, we found that the key residue of Acb1 for acyl binding, Y80, is critical for the proper subcellular localization and secretion of Acb1 and for cryptococcal morphogenesis.A daptation to a changing environment by eukaryotic microbes is often accompanied by a transition in cellular morphology. The human fungal pathogen Cryptococcus neoformans causes devastating cryptococcal meningitis, which claims the lives of hundreds of thousands of people each year (1). Late diagnosis, limited options for antifungals, and the lack of vaccines to prevent cryptococcosis all contribute to the high mortality rate of this disease (2). C. neoformans typically grows as yeasts but can switch from yeasts to filaments (hyphae or pseudohyphae) in response to predation (e.g., by amoebae) or during sexual reproduction (3-7). As with many other fungal pathogens, the morphotype of C. neoformans shapes its interactions with various hosts (8). As we demonstrated recently, the hyphal form is associated with the attenuation of virulence in mouse models of cryptococcosis, because the hyphal morphotype elicits strong and protective host immune responses (9, 10). On the other hand, the hyphal morphotype assists the fungus in resisting predation from soil amoebae (8), increases its ability to explore the environment (11), and is linked to its unisexual and bisexual reproduction (3,(12)(13)(14). Thus, it is important to understand the factors that promote cryptococcal hyphal growth.Many environmental stimuli and a few cryptococcal factors that promote hyphal growth in C. neoformans have been identified ...

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14 Mating-Type Structure, Function, Regulation and Evolution in the Pezizomycotina

2016

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Mechanisms of unisexual mating in Cryptococcus neoformans

Cited by 41 publications

References 142 publications

Sex-Induced Silencing Operates During Opposite-Sex and Unisexual Reproduction in Cryptococcus neoformans

Sex-Induced Silencing Operates During Opposite-Sex and Unisexual Reproduction in Cryptococcus neoformans

Secreted Acb1 Contributes to the Yeast-to-Hypha Transition in Cryptococcus neoformans

14 Mating-Type Structure, Function, Regulation and Evolution in the Pezizomycotina

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