The Sporangiophore of Phycomyces Blakesleeanus: a Tool to Investigate Fungal Gravireception and Graviresponses P

Plant Biology ISSN 1435-8603 REVIEW ARTICLE The sporangiophore of Phycomyces blakesleeanus: a tool to investigate fungal gravireception and graviresponses P. Galland Fachbereich Biologie, Philipps-Universitat€ Marburg, Marburg, Germany Keywords ABSTRACT Exponential law; gravisusceptors; gravitropism; gravitropism mutants; The giant sporangiophore of the single-celled fungus, Phycomyces blakesleeanus, uti- light-gravity interaction; Phycomyces lises light, gravity and gases (water and ethylene) as environmental cues for spatial blakesleeanus; resultant law; sine law; orientation. Even though gravitropism is ubiquitous in fungi (Naturwissenschaftliche sporangiophore. Rundschau, 1996, 49, 174), the underlying mechanisms of gravireception are far less understood than those operating in plants. The amenability of Phycomyces to classical Correspondence genetics and the availability of its genome sequence makes it essential to fill this P. Galland, Fachbereich Biologie, Philipps- knowledge gap and serve as a paradigm for fungal gravireception. The physiological Universitat€ Marburg, Karl-von-Frisch Str. 8, phenomena describing the gravitropism of plants, foremost adherence to the D-35032 Marburg, Germany. so-called sine law, hold even for Phycomyces. Additional phenomena pertaining to E-mail: [email protected] gravireception, specifically adherence to the novel exponential law and non-adherence to the classical resultant law of gravitropism, were for the first time investigated Editor for Phycomyces. Sporangiophores possess a novel type of gravisusceptor, i.e. lipid K. Palme globules that act by buoyancy rather than sedimentation and that are associated with a network of actin cables (Plant Biology, 2013). Gravitropic bending is associated Received: 4 January 2013; Accepted: 16 with ion currents generated by directed Ca2+ and H+ transport in the growing zone August 2013 (Annals of the New York Academy of Sciences, 2005, 1048, 487; Planta, 2012, 236, 1817). A set of behavioural mutants with specific defects in gravi- and/or photorecep- doi:10.1111/plb.12108 tion allowed dissection of the respective transduction chains. The complex pheno- types of these mutants led to abandoning the concept of simple linear transduction chains in favour of interacting networks with molecular modules of physically interacting proteins. 1992; Chaudhary et al. 2013) are available, all making it INTRODUCTION amenable to modern molecular approaches. In comparison to the classical plant objects of photo- and The Phycomyces literature has been reviewed at regular inter- gravitropism, such as grass coleoptiles and seedlings, the Phyc- vals during the past decades. Older literature, with major omyces sporangiophore is in several ways unique. The sporan- emphasis on blue light reception and the concomitant interac- giophore is a single coenocytic cell, which, for simplicity, can tion with gravitropism (Corrochano & Galland 2006), has been be regarded as a thin, water-filled tube elongating under a critically discussed in previous reviews (Bergman et al. 1969; turgor pressure of about 0.31 MPa at an astonishing rate of Galland & Lipson 1987a; Galland 2001). For physical principles À 2–3mmÁh 1. Light and gravity perception, growth modula- regarding optics, photoreceptor dichroism and excitation pro- tion and phototropism all occur in the small growing zone files, as well as for a critical discussion of problems pertaining extending 2–3 mm below the sporangium (Bergman et al. to adaptation and action spectroscopy, the reader is referred to 1969). The many complexities of signal transduction are thus the reviews of Fukshansky (1993), Galland (2001) and restricted to this fragile transparent cylinder of 2 mm length Corrochano (2007). and 100 lm diameter, whose growth and twist is modulated by unilateral light and gravity in a way that manifests as SPORANGIOPHORE GROWTH tropic bending. During the early decades of the last century it was not The local and time-dependent modulation of growth rate uncommon to investigate Phycomyces tropisms side by side represents a fundamental parameter underlying photo- and with those of higher plants (Banbury 1959, 1962). From gravitropism. Elongation growth and bending is restricted to such comparative investigations it became apparent that the the growing zone, which extends about 2–3 mm below the tip physiological principles underlying the light- and gravirecep- of stage 1 (Fig. 1, left) or below the sporangium in stage 4 tion of Phycomces and higher plants share a similar logical (Fig. 1, right). The growing zone represents the sensitive, and structure (Galland 1990). The many similarities which Phyc- at the same time, also the reactive zone of the sporangiophore. omyces tropisms share with those of plants and other fungi At its upper boundary it is continually formed anew, and at the justifies its use as a model organism, moreover, this organ- lower boundary it is converted into non-reactive material. The ism has been sequenced (http://genome.jgi-psf.org/Phybl2/ growth rate is largely determined by water uptake, transpira- Phybl2.home.html), and detailed genetic maps (Alvarez et al. tion and cell wall extension, which are brought about by the 58 Plant Biology 16 (Suppl. 1) (2014) 58–68 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands Galland Gravireception of Phycomyces blakesleeanus A B Fig. 1. Sporangiophores of Phycomyces blakesleeanus. Left: stage 1 sporangiophore. The open arrow points to the complex of lipid globules that con- tain yellow b-carotene. The central hyaline structure in the lower 360 lm represents the central vacuole. Bar: 100 lm. Photograph: Dr. Irmin Meyer. Middle: close up (interference-contrast micrograph) of the complex of lipid globules. Arrowhead: single lipid globule. Because of interference-contrast other globules appear dark. Small arrows: hyaline zone that houses the lipid globules. Bar: 10 lm. Photograph: Dr. Franz Grolig. Right: dark-field photograph of a stage 4 sporangiophore, i.e. with the spore-bearing sporangium. Bar: 100 lm. Photograph: Dr. Irmin Meyer. allocation of chitosomes (Herrea-Estrella et al. 1982). The tur- Fig. 2. Kinetics of gravitropic bending of stage 4 sporangiophores of Phyc- gor pressure amounts to 0.31 MPa and a growth rate of about omyces. A: Sporangiophores were placed horizontally. Filled circles: wild l Á À1 33 m min (Ortega et al. 1992). Because of transpiration, the type; open squares: mutant C202 (lacking vacuolar protein crystals); open water uptake of a sporangiophore can exceed seven times the triangles: hypergravitropic mutant C5 containing an excess of vacuolar volumetric growth rate (Ortega et al. 1992). The growth rate is protein crystals. Data from Schimek et al. (1999a). B: Gravitropic bending of not completely steady but rather fluctuates and displays a a single sporangiophore in response to step changes of the centrifugal accel- frequency spectrum with several minor peaks between 0.3 and eration (1.5 g ? 3 g ? 1.5 g; upper solid line). Modified from Dennison 10 mHz and a maximum at 10 mHz that can be altered in 1961. some of the phototropism mutants (Ensminger & Lipson 1992). A further complication derives from the fact that in gravitational acceleration (Dennison 1961; Dennison & Shrop- À stage 4, sporangiophores do not only elongate (2–3mmÁh 1) shire 1984; Horie et al. 1998; Schimek et al. 1999a), while but rather rotate clockwise, when viewed from above, at a rate mycelial hyphae and zygophores are agravitropic. Cultures of À of about 180°Áh 1 (Oort 1931). Elongation and rotation repre- Phycomyces cultivated for 19.5 days in microgravity in the Rus- sent two growth components that are not evenly distributed in sian biosatellite Cosmos-782 maintained normal vegetative and the growing zone (Cohen & Delbruck€ 1958). The rotation sexual development, but had completely disoriented sporangio- causes a slight complication in gravi- and phototropic bending, phores, forming twists and loops. The normal growth pattern because near the respective thresholds sporangiophores do not of sporangiophores could be recovered on a centrifuge operat- bend exactly in the plane of the stimulus but rather in a plane ing at an acceleration of 1 g (Parfyonov et al. 1979). The effec- that slightly deviates from it, leading to errors in direction tiveness of gravitropism depends to some extent on the (Bergman et al. 1969; Galland et al. 2004). developmental stage, as stage 1 sporangiophores, which lack a sporangium (Fig. 1, left), bend gravitropically more slowly than stage 4 sporangiophores with a sporangium (Schimek et al. GRAVITROPISM 1999a; Grolig et al. 2004). Gravireception is ubiquitous in the fungal kingdom and is It is important to distinguish between two different types of manifested as gravimorphogenesis and gravitropism (reviewed gravitropic response: (i) ‘normal’ gravitropism in response to a in Kern & Hock 1996; Kern 1999; Galland 2001; Corrochano & displacement of the sporangiophore from the vertical (Fig. 2A), Galland 2006). Fruiting bodies usually grow vertically and which persists for as long as the gravitropic stimulus persists, reorient a few hours after displacement from the vertical i.e. it is non-adaptive and slow; and (ii) gravitropism in (Fig. 2A). Sporangiophores of Phycomyces display negative response to sudden step-up or step-down changes of centrifu- gravitropism, i.e. they bend opposite to the Earth’s gal acceleration (Fig. 2B), which is transient and fast. Plant Biology 16 (Suppl. 1) (2014) 58–68 ©

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