Cytoplasmic Continuity Revisited: Closure of Septa of the Filamentous Fungus Schizophyllum commune in Response to Environmental Conditions

PLOS ONE, Jun 2009

Background Mycelia of higher fungi consist of interconnected hyphae that are compartmentalized by septa. These septa contain large pores that allow streaming of cytoplasm and even organelles. The cytoplasm of such mycelia is therefore considered to be continuous. Methodology/Principal Findings Here, we show by laser dissection that septa of Schizophyllum commune can be closed depending on the environmental conditions. The most apical septum of growing hyphae was open when this basidiomycete was grown in minimal medium with glucose as a carbon source. In contrast, the second and the third septum were closed in more than 50% and 90% of the cases, respectively. Interestingly, only 24 and 37% of these septa were closed when hyphae were growing in the absence of glucose. Whether a septum was open or closed also depended on physical conditions of the environment or the presence of toxic agents. The first septum closed when hyphae were exposed to high temperature, to hypertonic conditions, or to the antibiotic nourseothricin. In the case of high temperature, septa opened again when the mycelium was placed back to the normal growth temperature. Conclusions/Significance Taken together, it is concluded that the septal pores of S. commune are dynamic structures that open or close depending on the environmental conditions. Our findings imply that the cytoplasm in the mycelium of a higher fungus is not continuous perse.

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Cytoplasmic Continuity Revisited: Closure of Septa of the Filamentous Fungus Schizophyllum commune in Response to Environmental Conditions

Wo sten HAB (2009) Cytoplasmic Continuity Revisited: Closure of Septa of the Filamentous Fungus Schizophyllum commune in Response to Environmental Conditions. PLoS ONE 4(6): e5977. doi:10.1371/journal.pone.0005977 Cytoplasmic Continuity Revisited: Closure of Septa of the Filamentous Fungus Schizophyllum commune in Response to Environmental Conditions Arend F. van Peer 0 Wally H. Mu ller 0 Teun Boekhout 0 Luis G. Lugones 0 Han A. B. Wo sten 0 Alexander Idnurm, University of Missouri-Kansas City, United States of America 0 1 Department of Microbiology, Institute of Biomembranes, Utrecht University , Utrecht , The Netherlands , 2 Department of Cellular Architecture and Dynamics, Institute of Biomembranes, Utrecht University , Utrecht , The Netherlands, 3 CBS Fungal Biodiversity Centre, Utrecht , The Netherlands Background: Mycelia of higher fungi consist of interconnected hyphae that are compartmentalized by septa. These septa contain large pores that allow streaming of cytoplasm and even organelles. The cytoplasm of such mycelia is therefore considered to be continuous. Methodology/Principal Findings: Here, we show by laser dissection that septa of Schizophyllum commune can be closed depending on the environmental conditions. The most apical septum of growing hyphae was open when this basidiomycete was grown in minimal medium with glucose as a carbon source. In contrast, the second and the third septum were closed in more than 50% and 90% of the cases, respectively. Interestingly, only 24 and 37% of these septa were closed when hyphae were growing in the absence of glucose. Whether a septum was open or closed also depended on physical conditions of the environment or the presence of toxic agents. The first septum closed when hyphae were exposed to high temperature, to hypertonic conditions, or to the antibiotic nourseothricin. In the case of high temperature, septa opened again when the mycelium was placed back to the normal growth temperature. Conclusions/Significance: Taken together, it is concluded that the septal pores of S. commune are dynamic structures that open or close depending on the environmental conditions. Our findings imply that the cytoplasm in the mycelium of a higher fungus is not continuous perse. - Funding: The work was supported by Utrecht University. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. A fungal mycelium is the result of fusing hyphae that grow at their apices and that branch subapically. In general, hyphae of the lower fungi, i.e. the Glomeromycota, Zygomycota, and Chytridiomycota are sparsely, if at all, septated [13]. Therefore, the cytoplasm within mycelia of these fungi is continuous. Hyphae of the higher fungi, i.e. the Ascomycota and Basidiomycota, are compartmentalized by septa. These septa contain central pores of up to 500 nm that allow streaming of cytoplasm and translocation of organelles like mitochondria and nuclei [13]. Therefore, the cytoplasm within these mycelia is also considered to be continuous. This discriminates the filamentous fungi from plants and animals. In these latter two kingdoms there are also intercellular cytoplasmic connections but they are much smaller. Gap junctions in animals and plasmodesmata in plants have pores with a diameter of about 1.5 to 3.0 nm. These pores allow streaming of inorganic ions and small water-soluble organic molecules [810]. It should be noted that the diameter of the pores of plasmodesmata and gap junctions is dynamic. For instance, the channels in plasmodesmata can be closed or their width increased to 5 to 9 nm. The major groups of fungi within the Basidiomycota contain different types of septa. The Pucciniomycotina and the Ustilaginomycotina have relatively simple septa [1,11,12]. In contrast, septa of the Agaricomycotina are relatively complex. They consist of a barrel-shaped swelling around the pore, the dolipore, which is associated with a septal pore cap (SPC) [6]. This septal pore cap, which restricts organelle translocation, can be of the vesiculate type, the perforate type or the imperforate type [13] and is assumed to be derived from the endoplasmic reticulum [1416]. The SPC of Schizophyllum commune is of the perforate type. Its base, i.e. the part closest to the septum, has a diameter of 450600 nm and the whole structure is regularly perforated by openings of approximately 100 nm [15,17]. Septa of Ascomycota and the Basidiomycetes become plugged in response to hyphal damage to prevent loss of cytoplasm [18 20]. Peroxisome-like organelles, called Woronin bodies, plug the septa of the ascomycetes [2123], whereas in basidiomycetes septa are closed by electron dense, plugging material [19]. It has been proposed that the SPC is involved in the plugging process [15,20,24,25]. Here, it is shown by laser dissection that septa of growing hyphae o (...truncated)


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Arend F. van Peer, Wally H. Müller, Teun Boekhout, Luis G. Lugones, Han A. B. Wösten. Cytoplasmic Continuity Revisited: Closure of Septa of the Filamentous Fungus Schizophyllum commune in Response to Environmental Conditions, PLOS ONE, 2009, Volume 4, Issue 6, DOI: 10.1371/journal.pone.0005977