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Eukaryotic Cell, October 2008, p. 1809-1818, Vol. 7, No. 10
1535-9778/08/$08.00+0     doi:10.1128/EC.00149-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

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{triangledown} ,{dagger}

Karine Lambou,1 Fabienne Malagnac,2,3 Crystel Barbisan,1 Didier Tharreau,4 Marc-Henri Lebrun,1* and Philippe Silar2,3*

UMR 5240 CNRS-UCB-INSA-Bayer CropScience, Microbiologie Adaptation et Pathogénie, 14-20 Rue Pierre Baizet, 69263 Lyon Cedex 09 France,1 UFR des Sciences du Vivant, Université de Paris 7—Denis Diderot, 75205 Paris Cedex 13 France,2 Université Paris-Sud 11, CNRS, UMR8621, Institut de Génétique et Microbiologie, 91405 Orsay Cedex, France,3 CIRAD, UMR BGPI (CIRAD-INRA-SupAgro.M), TA A 54/K, Campus International de Baillarguet, 34398 Montpellier Cedex 5, France4

Received 29 April 2008/ Accepted 19 August 2008

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 {Delta}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 {Delta}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.


* Corresponding author. Mailing address for M.-H. Lebrun: UMR 5240 CNRS UCB INSA Bayer CropScience, Microbiologie Adaptation et Pathogénie, Bayercropscience, 14-20 Rue Pierre Baizet, 69263 Lyon Cedex 09, France. Phone: (33) 4 72 85 24 81. Fax: (33) 4 72 85 22 97. E-mail: marc-henri.lebrun{at}bayercropscience.com. Mailing address for P. Silar: Institut de Génétique et Microbiologie, Bat.400 Univ. Paris-Sud 11, 91405 Orsay, France. Phone: (33)1 69 15 45 58. Fax: (33)1 69 15 70 06. E-mail: philippe.silar{at}igmors.u-psud.fr

{triangledown} Published ahead of print on 29 August 2008.

{dagger} Supplemental material for this article may be found at http://ec.asm.org/.


Eukaryotic Cell, October 2008, p. 1809-1818, Vol. 7, No. 10
1535-9778/08/$08.00+0     doi:10.1128/EC.00149-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.