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Architecture and Development of the Neurospora Crassa Hypha E a Model Cell for Polarized Growth

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Architecture and Development of the Neurospora Crassa Hypha E a Model Cell for Polarized Growth fungal biology 115 (2011) 446e474 journal homepage: www.elsevier.com/locate/funbio Architecture and development of the Neurospora crassa hypha e a model cell for polarized growth Meritxell RIQUELMEa,*, Oded YARDENb,*, Salomon BARTNICKI-GARCIAa, Barry BOWMANc, Ernestina CASTRO-LONGORIAa, Stephen J. FREEd, Andre FLEIßNERe, f g ~ a h Michael FREITAG , Roger R. LEW , Rosa MOURINO-PEREZ , Michael PLAMANN , Carolyn RASMUSSENi, Corinna RICHTHAMMERj, Robert W. ROBERSONk, Eddy SANCHEZ-LEONa, Stephan SEILERj, Michael K. WATTERSl aCenter for Scientific Research and Higher Education of Ensenada e CICESE, Ensenada Baja California 22860, Mexico bDepartment of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel cDepartment of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, CA 95064, USA dDepartment of Biological Sciences, University at Buffalo, Buffalo, NY 14260, USA eInstitut fur€ Genetik, Technische Universitat€ Braunschweig, 38106 Braunschweig, Germany fDepartment of Biochemistry and Biophysics, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331-7305, USA gYork University, Toronto, Ontario M3J 1P3, Canada hSchool of Biological Sciences, University of Missouri-Kansas City, Kansas City, MO 64110, USA iUniversity of California, San Diego, Cell and Developmental Biology, 9500 Gilman Dr., La Jolla, CA 92093-0116, USA jDepartment of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, Georg-August-Universitat,€ D-37077 Gottingen,€ Germany kSchool of Life Sciences, Arizona State University, Tempe, AZ 85287, USA lDepartment of Biology, Valparaiso University, Valparaiso, IN 46383-4543, USA article info abstract Article history: Neurospora crassa has been at the forefront of biological research from the early days of bio- Received 17 December 2010 chemical genetics to current progress being made in understanding gene and genetic network Received in revised form function. Here, we discuss recent developments in analysis of the fundamental form of fungal 8 February 2011 growth, development and proliferation e the hypha. Understanding the establishment and Accepted 9 February 2011 maintenance of polarity, hyphal elongation, septation, branching and differentiation are at Available online 19 February 2011 the coreof current research. The advances in the identification and functional dissection of reg- Corresponding Editor: ulatory as well as structural components of the hypha provide an expanding basis for elucida- Brian Douglas Shaw tion of fundamental attributes of the fungal cell. The availability and continuous development of various molecular and microscopic tools, as utilized by an active and co-supportive research Keywords: community, promises to yield additional important new discoveries on the biology of fungi. Branching ª 2011 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. Cell wall Hyphal growth Septation Spitzenkorper€ * Corresponding authors. E-mail address: [email protected] 1878-6146/$ e see front matter ª 2011 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.funbio.2011.02.008 Neurospora crassa hyphae 447 Herrmann 2007; Jinhu & Yi 2010; Chen et al. 2010; Vitalini Introduction et al. 2006; Smith et al. 2010; Chen et al. 2009; Borkovich et al. 2004). Neurospora crassa - a model going strong The entire community of fungal biologists has benefited from useful resources derived from the Functional Genomics Our understanding of the morphogenesis of filamentous fungi and Systems Biology Project, a project promoted by members is progressing rapidly (with >15 000 publications in just the of the Neurospora community that culminated in the publica- last 5 y). The wealth of genetic information, availability of mu- tion of the N. crassa genome draft sequence (Galagan et al. tants and the progress made in live imaging techniques, cou- 2003; Borkovich et al. 2004; Dunlap et al. 2007). Some valuable pled with biochemical analysis, have significantly contributed tools include a collection of single-gene deletion mutants to the progress made in understanding one of the most char- (Colot et al. 2006), as well as expression and tiling microarrays acteristic and fundamental forms of fungal growth, develop- (Greenwald et al. 2010; Hutchison et al. 2009; Kasuga & Glass ment and proliferation e the hypha. Along with neurons 2008), and single nucleotide polymorphism data for widely and pollen tubes, hyphae are the most highly polarized cell used strains (Lambreghts et al. 2009). The publication of the first forms known (Palanivelu & Preuss 2000; Borkovich et al. high-quality draft genome of a filamentous fungus was just the 2004; Harris 2006; Ischebeck et al. 2010). On the one hand, beginning. In fact, w200 fungal genome sequences will soon be much has been discovered about the role and function of hy- available (for details see http://fungalgenomes.org/wiki/Fun- phal elements that are shared with many other eukaryotic cell gal_Genome_Links). This number will greatly increase in the types, albeit in the context of a syncytium. On the other hand, near future as high-throughput sequencing allows affordable many structures and functions unique to filamentous fungi sequencing and de novo assembly of fungal genomes have now been identified and analyzed. Thus, the accumulat- (Nowrousian 2010). In addition to genetics-based developments ing information, along with the technological advances en- and tools, techniques that have progressed our abilities to hancing our capabilities of probing and analyzing both study the cell biology of N. crassa have also evolved. Fluorescent existing and new directions, make the compilation of this re- protein (FP) labelling was successfully developed for N. crassa view timely. Featuring N. crassa, we intend this review to serve separately by two different labs in 2001 and 2002 (Freitag et al. as an updated resource and a source of ideas for future studies 2001; Fuchs et al. 2002), and made widely available to the Neu- on the fungal filament. Furthermore, the increased interest in rospora community in 2004 (Freitag et al. 2004). Currently, an fungal pathogens of humans, animals and plants, along with ever-increasing number of strains with fluorescently labelled the use of filamentous fungi in biotechnology and biopro- proteins (Table 1) are readily available from the Fungal Genetics specting warrants the in-depth understanding of the hyphal Stock Center (http://www.fgsc.net/). filament as the fundamental unit in these organisms. By providing a critical and current evaluation of research Neurospora crassa has been an excellent model organism for on one of the most advanced model systems useful to all re- eukaryotic genetics and biochemistry and one of the work- searchers studying filamentous fungi, we hope to stress op- horses for fungal cell biology research. While Saccharomyces portunities for future research directions and identify cerevisiae is often referred to as a good representative of the important challenges. Fifth Kingdom, it has become increasingly apparent that - de- spite its virtues - the yeast cell represents only a minor frac- The hyphal lifestyle encompasses multiple morphological tion of the fungal kingdom in many morphological and structures biochemical aspects. Most fungi have a highly branched fila- mentous morphology and occupy a much broader spectrum The ability to form polarized cell types is not only a fundamen- À of habitats. The rapid (w4mmhr 1) filamentous growth habit tal property of filamentous fungi, but is also one of the key at- of N. crassa is the result of a strongly polarized mechanism tributes that contributes to their success in inhabiting culminating in the biogenesis of the tubular cell wall. Seven beneficial niches and/or avoiding detrimental ones. As such, decades of pioneering research on the biology of the hypha the development of hyphae is one of the bases for fungal pro- performed with this model organism (Beadle & Tatum 1945; liferation. In many cases, hyphal development can be a prereq- Garnjobst & Tatum 1967; Collinge & Trinci 1974; Vollmer & uisite for the formation of additional cell types that, along Yanofsky 1986; Metzenberg & Glass 1990; Yarden et al. 1992; with hyphae, are involved in growth, development and Plamann et al. 1994; Steinberg & Schliwa 1995; Seiler et al. propagation. 1997; Riquelme et al. 1998; Davis 2000; Perkins et al. 2001; Amongst at least 28 distinct morphological cell types de- Seiler & Plamann 2003; Gavric & Griffiths 2003), have proven scribed in Neurospora crassa (Bistis et al. 2003), more than six N. crassa to be a rewarding model fungus for experimental can be designated as hyphae. These forms of hyphae encom- work e work that continues today in more than 30 laborato- pass both asexual and sexual development of this fungus. The ries around the world. Extensive work has been performed, hyphal cell types described include (for more details see Bistis utilizing N. crassa, on genome defence, DNA repair and recom- et al. 2003): Leading hypha (wide, fast growing with subapical bination, on light and circadian regulation as well as on mito- branching; Robertson 1965); Trunk hypha (in the colony inte- chondrial protein import and biogenesis, but because of the rior); Fusion hypha and conidial anastomosis tubes hypha scope of this article we refer readers interested in this subject (bridge between
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