Fungi have three tetraspanin families with distinct functions

Lambou, Karine; Tharreau, Didier; Kohler, Annegret; Sirven, Catherine; Marguerettaz, Mélanie; Barbisan, Crystel; Sexton, Adrienne; Kellner, Ellen M.; Martin, Francis; Howlett, Barbara J.; Orbach, Marc J.; Lebrun, Marc

doi:10.1186/1471-2164-9-63

Cited by 44 publications

(37 citation statements)

References 31 publications

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“…1A]) to the conserved C-terminal tail sequence of Pls1 tetraspanins (20). This analysis shows that PaPls1 has all the structural hallmarks of Pls1 tetraspanins (20,31,50), suggesting that it corresponds to a functional protein.…”

Section: Resultsmentioning

confidence: 89%

“…Animal tetraspanins are involved in different biological processes including sperm-egg fusion, entry of parasites or viruses into host cells, cell-cell interactions in central nervous system or immune system (B-cell-T-cell immunological synapse), cell adhesion, motility, polarity, and trafficking of membrane proteins (23,33). Surprisingly, additional Pls1 orthologues were identified in saprobic fungi devoid of appressorium such as Neurospora crassa (20), Coprinopsis cinerea (26), Chaetomium globosum, Podospora anserina, Trichoderma reesei, and Phanerochete chrysosporium (31). To date, the role of Pls1 tetraspanins in these nonpathogenic fungi is unknown.…”

mentioning

confidence: 99%

“…At least 33 distinct tetraspanins were identified in humans, 37 in Drosophila melanogaster, and 20 in Caenorhabditis elegans, but only 3 in fungi: Pls1 and Tps2 in basidiomycetes and Pls1 and Tps3 in ascomycetes (26,31). In M. grisea, Pls1 is expressed in the appressoria and localizes either at the plasma membrane or in vacuoles (11), while it is expressed in both appressoria and vegetative mycelium in C. lindemuthianum (51) and in conidia, germ tubes, and appressoria during host penetration in B. cinerea (19).…”

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confidence: 99%

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The Crucial Role of the Pls1 Tetraspanin during Ascospore Germination in Podospora anserina Provides an Example of the Convergent Evolution of Morphogenetic Processes in Fungal Plant Pathogens and Saprobes

et al. 2008

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Pls1 tetraspanins were shown for some pathogenic fungi to be essential for appressorium-mediated penetration into their host plants. We show here that Podospora anserina, a saprobic fungus lacking appressorium, contains PaPls1, a gene orthologous to known PLS1 genes. Inactivation of PaPls1 demonstrates that this gene is specifically required for the germination of ascospores in P. anserina. These ascospores are heavily melanized cells that germinate under inducing conditions through a specific pore. On the contrary, MgPLS1, which fully complements a ⌬PaPls1 ascospore germination defect, has no role in the germination of Magnaporthe grisea nonmelanized ascospores but is required for the formation of the penetration peg at the pore of its melanized appressorium. P. anserina mutants with mutation of PaNox2, which encodes the NADPH oxidase of the NOX2 family, display the same ascospore-specific germination defect as the ⌬PaPls1 mutant. Both mutant phenotypes are suppressed by the inhibition of melanin biosynthesis, suggesting that they are involved in the same cellular process required for the germination of P. anserina melanized ascospores. The analysis of the distribution of PLS1 and NOX2 genes in fungal genomes shows that they are either both present or both absent. These results indicate that the germination of P. anserina ascospores and the formation of the M. grisea appressorium penetration peg use the same molecular machinery that includes Pls1 and Nox2. This machinery is specifically required for the emergence of polarized hyphae from reinforced structures such as appressoria and ascospores. Its recurrent recruitment during fungal evolution may account for some of the morphogenetic convergence observed in fungi.Convergent evolution of trophic strategies and morphogenetic processes is a hallmark of fungi (27). For example, many fungi belonging to different fungal clades are phytopathogenic, whereas their close relatives are saprobic. These plant parasitic fungi may penetrate into their host plants using a specialized structure called the appressorium. Appressoria are attached to the surface of plants and redirect fungal growth into the host tissues underneath through the formation of a penetration peg. Due to their importance in pathogenicity, appressoria are studied in fungi such as Magnaporthe grisea, a devastating pathogen of rice (25, 54), Botrytis cinerea, a wide-host-range plant pathogen (19), and Colletotrichum lindemuthianum, an important pathogen of beans (13). These three fungi belong to two different clades of ascomycetes. M. grisea and C. lindemuthianum are in the Sordariomycetes and B. cinerea in Leotiomycetes. A significant number of species related to these three fungi are saprobic. Which of the parasitic or saprobic lifestyles displayed by these organisms arise by convergent evolution is thus crucial to understand their evolution. An answer to this question is to establish whether appressoria are homoplasious or homologous in Sordariomycetes and Leotiomycetes and whether appressorium-specific ...

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Section: Resultsmentioning

confidence: 89%

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confidence: 99%

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confidence: 99%

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The Crucial Role of the Pls1 Tetraspanin during Ascospore Germination in Podospora anserina Provides an Example of the Convergent Evolution of Morphogenetic Processes in Fungal Plant Pathogens and Saprobes

et al. 2008

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“…Here we describe one, LZM36, in which laccase is not inhibited by glucose. The mutated gene in LZM36 was identified as a tetraspanin-encoding gene, designated TSP2-1, which belongs to the fungal Tsp2 tetraspanin family (17,24). We prove here that TSP2-1 plays a key role in laccase repression by glucose.…”

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confidence: 63%

Requirement of a Tsp2-Type Tetraspanin for Laccase Repression and Stress Resistance in the Basidiomycete Cryptococcus neoformans

Yang

et al. 2012

Appl Environ Microbiol

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Fungal laccases have been widely used in industry. The expression of laccase often is repressible by the primary carbon source glucose in many fungi. The underlying basis is largely unclear. We demonstrate here that a gene, TSP2-1, was required for laccase repression by glucose in the basidiomycete Cryptococcus neoformans. TSP2-1 encodes a Tsp2-type tetraspanin. The disruption of TSP2-1 resulted in constant melanin formation and the expression of the laccase gene LAC1. This derepression phenotype was restorable by 10 mM exogenous cyclic AMP (cAMP). A capsule defect in the mutant tsp2-1⌬ also was restored by cAMP. The results indicate an interaction of Tsp2-1 with the cAMP-dependent protein kinase A (PKA) pathway that has been shown to modulate laccase repression and capsule biosynthesis in this fungus. Other roles of TSP2-1, e.g., in maintaining cell membrane integrity and stress resistance, also were defined. This work reveals a Tsp2-1-dependent glucose repression in C. neoformans. The function of Tsp2-type tetraspanin Tsp2-1 is described for the first time.

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“…Tetraspanin-like proteins have also been identifi ed in fungi, and their molecular mass (more than 200 kDa) is greater than those of tetraspanin identifi ed in animals and plants (20-30 kDa) (Lambou et al 2008 ). An appressorium is a specialized cell typical of many fungal plant pathogens that is used to infect host plants.…”

Section: Tetraspaninmentioning

confidence: 99%

Role of CD9 in Sperm–Egg Fusion and Virus-Induced Cell Fusion in Mammals

Yoshida

Kawano

Harada

et al. 2014

Sexual Reproduction in Animals and Plants

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In mammals, two integral membrane proteins, sperm IZUMO1 and egg CD9, regulate sperm-egg fusion, and their roles are critical but as yet unknown. In such situation, a recent study has shown that CD9-containing exosome-like vesicles, which are released from wild-type eggs, can induce the fusion between sperm and Cd9 -defi cient egg, even though Cd9 -defi cient eggs are highly refractory to the fusion with sperm. This result provides compelling evidence for the crucial involvement of CD9-containing, fusion-facilitating vesicles in sperm-egg fusion. On the other hand, similarities have been observed between the generation of retroviruses in host cells and the formation of small cellular vesicles, termed exosomes, in mammalian cells. The exosomes are thought to regulate intercellular communication through transfer of proteins and RNAs. These collective studies provide an insight into the molecular mechanisms of gamete fusion and other membrane fusion events.

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Fungi have three tetraspanin families with distinct functions

Cited by 44 publications

References 31 publications

The Crucial Role of the Pls1 Tetraspanin during Ascospore Germination in Podospora anserina Provides an Example of the Convergent Evolution of Morphogenetic Processes in Fungal Plant Pathogens and Saprobes

The Crucial Role of the Pls1 Tetraspanin during Ascospore Germination in Podospora anserina Provides an Example of the Convergent Evolution of Morphogenetic Processes in Fungal Plant Pathogens and Saprobes

Requirement of a Tsp2-Type Tetraspanin for Laccase Repression and Stress Resistance in the Basidiomycete Cryptococcus neoformans

Role of CD9 in Sperm–Egg Fusion and Virus-Induced Cell Fusion in Mammals

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