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Vegetative Hyphal Fusion in Filamentous Fungi

* and .

* Corresponding Author: Nick D. Read—Fungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Rutherford Building, Edinburgh EH9 3JH, U.K. Email: Nick@fungalcell.org

The formation of channels between fungal hyphae by self fusion is a defining feature of filamentous fungi, and results in the fungal colony being a complex interconnected network of hyphae. During the vegetative phase hyphal fusions are commonly formed during colony establishment by specialized conidial anastomosis tubes (CATs), and then later by specialized fusion hyphae in the mature colony. CAT induction, homing and fusion in Neurospora crassa provides an excellent model in which to study the process of vegetative hyphal fusion because it is simple and experimentally very amenable. Various mutants compromised in hyphal fusion have been isolated and characterized. Although the self-signalling ligand(s) involved in CAT induction and homing has/have not been identified, MAP kinase signalling is downstream of the initial ligand-receptor interaction(s), and has features in common with MAP kinase signalling during mating cell interactions in the budding yeast and during fungal infection structure (appressorium) formation. Hyphal fusion also resembles yeast cell mating and appressorium formation in other ways. Vegetative hyphal fusion between hyphae of different genotypes (nonself fusion) usually results in a form of programmed cell death which normally prevents heterokaryons from developing further. This process in N. crassa is controlled by heterokaryon incompatibility (het) loci. Understanding hyphal fusion in the model fungus, N. crassa, provides a paradigm for self-signalling mechanisms in eukaryotic microbes and might also provide a model for understanding somatic cell fusion in other eukaryotic species.

Introduction

Cell fusion occurs at various stages and serves numerous functions during the vegetative and sexual phases of the filamentous fungal life cycle.1 This review is concerned with vegetative cell fusion which can occur between hyphae of the same genotype (i.e., self fusion) or different genotypes (i.e., nonself fusion). The latter normally results in an incompatible response and a form of programmed cell death.2-3

Buller was the first to provide a detailed description of the process of vegetative hyphal fusion in 1931,4-5 and show how it gives rise to the fungal colony as a complex interconnected hyphal network (Fig. 1).6 Remarkably, it is only recently that a systematic analysis of the cell biology and genetics of vegetative hyphal fusion has been initiated,1,7-8 and most of this work has been done with the model filamentous fungus, Neurospora crassa.9-10 Here we review: (1) the different types of vegetative hyphal fusion that occur in filamentous fungi, (2) their possible roles, (3) features that vegetative hyphal fusion has in common with yeast cell mating and infection structure differentiation in fungal pathogens, and (4) the heterokaryon incompatibility response that results from nonself fusions. Particular attention is given to recent work on N. crassa.

Figure 1. Buller's classic figure showing that hyphal fusion produces a fungal colony (in this case a colony of Coprinus sterquilinus) with an interconnected network of hyphae.

Figure 1

Buller's classic figure showing that hyphal fusion produces a fungal colony (in this case a colony of Coprinus sterquilinus) with an interconnected network of hyphae. a) a basidiospore which has germinated; b) and c) leading hyphae at the colony periphery (more...)

Fusion between Spores and Spore Germlings

During the early stages of colony establishment, fungal spores (or the germ tubes which arise from them) commonly fuse. This process has been best described between conidia and conidial germlings in ascomycete and mitosporic fungi (Fig. 2A).7,11-12 However, fusions between ascospore and urediospore germlings have also been shown (Fig. 2B).4,13-15

Figure 2. A) Germinated macroconidia of Neurospora crassa with long germ germ tubes avoiding each other and conidial anastomosis tubes which have homed and fused (asterisks).

Figure 2

A) Germinated macroconidia of Neurospora crassa with long germ germ tubes avoiding each other and conidial anastomosis tubes which have homed and fused (asterisks). (Reproduced from ref. 11 with permission.) B) Germinated ascospores of Sordaria macrospora (more...)

Fusion between conidia or conidial germlings involves the formation and interaction of specialized hyphae called conidial anastomosis tubes (CATs) which are morphologically and physiologically distinct from germ tubes,7,11-12 and under separate genetic control.11 CATs are short, thin, usually unbranched hyphae that arise from conidia or conidial germ tubes.7,11-12 What had not been appreciated until recently is that CAT fusion is an extremely common process that has been described in at least 73 species of 21 genera, including many plant pathogens, and thus is probably a common feature of colony establishment in ascomycete and mitosporic fungi.7 How widespread fusion is between other types of spores and spore germlings remains to be determined.

In Neurospora crassa, CAT formation is conidium density dependent and thus may involve quorum sensing.11 The nature of the CAT inducer is unknown but it activates a mitogen-activated protein (MAP) kinase cascade which has orthologs in the MAP kinase pathway involved in: (1) pheromone signalling in Saccharomyces cerevisiae,16-17 and (2) appressorium formation in fungal plant pathogens.17-20 Mutations in the genes encoding the MAP kinase kinase kinase, NRC-1, and the MAP kinase, MAK-2, are unable to form CATs (Fig. 3).11 Increased phosphorylation of MAK-2 was shown to correlate with the onset of fusion between conidial germlings during colony establishment.17 The downstream target of these MAP kinases seems to be the transcription factor, pp-1 which is an ortholog of the budding yeast ste-12.7-8,21 HAM-2, a putative transmembrane protein of unknown function,22 has also been implicated in CAT induction because it is unable to form CATs.11

Figure 3. Conidial anastomosis tube induction, homing and fusion in Neurospora crassa, and signalling which occurs during CAT induction and homing.

Figure 3

Conidial anastomosis tube induction, homing and fusion in Neurospora crassa, and signalling which occurs during CAT induction and homing. A) Mutants blocked in CAT induction and homing. B) Model of the signalling pathways involved in CAT induction and (more...)

CATs home towards each other. CAT homing has been shown to involve the secretion and reception of a chemoattractant at CAT tips of Neurospora by using optical tweezers as a novel experimental tool to move spores or germlings relative to each other.11

The identities of the CAT inducer and CAT chemoattractant are unknown, but conceivably could be the same self-signalling ligand. However, it is known that neither signalling molecule is cAMP in Neurospora because CATs form and home in a mutant that lacks cAMP.11

Another Neurospora gene, so encodes a protein which plays a role in the biochemical machinery involved in the synthesis and/or secretion of the CAT chemoattractant, or in the signalling apparatus involved in the perception and/or transduction of the chemoattractant signal. This mutant forms CATs but they are unable to home towards or fuse with other CATs of the so mutant or wild type (Fig. 3).23

Once two CAT tips make contact, they adhere, a fusion pore forms between them, and organelle and cytoplasmic mixing occurs. The movement of organelles between fusion partners is very slow.7

Fusion between Hyphae in the Mature Colony

A detailed description of vegetative hyphal fusion in mature colonies of N. crassa has been provided by Hickey et al using confocal microscopy to perform time lapse imaging of living hyphae.24 Three basic phases in the process leading up to hyphal fusion have been defined: (1) pre-contact, (2) post-contact, and (3) post-fusion.1,3,24 The different stages involved in these three phases are summarized in Figure 4. Hickey et al24 demonstrated that during the precontact phase specialized fusion hyphae that are fusion-competent exhibit positive tropisms by growing (homing) towards each other, and their close vicinity to other hyphae can induce the formation of further fusion hyphae (Fig. 5). During the post-contact phase, these hyphae make contact, adhere, commonly swell at their tips, and their intervening cell walls break down. Finally, during the post-fusion phase the plasma membranes of the two hyphae fuse providing cytoplasmic continuity and allowing the movement of organelles between them. The bulk flow of organelles and cytoplasm from one hypha to another through the connecting channel can often be very rapid resulting in their immediate mixing. The fusion pore usually increases in size following fusion (Fig. 5) and septa often form in the vicinity of the site of fusion.24

Figure 4. Diagram showing the precontact, post-contact and post-fusion stages involved in vegetative hyphal fusion in the mature colony (diagram modified from that shown in ref.

Figure 4

Diagram showing the precontact, post-contact and post-fusion stages involved in vegetative hyphal fusion in the mature colony (diagram modified from that shown in ref. ). Two types of precontact behaviour are shown: (a) a tip of a fusion hypha induces (more...)

Figure 5. Confocal microscopy showing the induction, homing and fusion of fusion hyphae in the mature colony of Neurospora crassa after staining with FM1-43.

Figure 5

Confocal microscopy showing the induction, homing and fusion of fusion hyphae in the mature colony of Neurospora crassa after staining with FM1-43. Note the growth of three branches (1-3) from one hypha towards two short branches on the opposite hypha (more...)

The formation and homing of fusion hyphae were shown to be intimately associated with the dynamic behaviour of the Spitzenkörper, a cluster of secretory vesicles, cytoskeletal elements, and other proteins which plays a crucial role in hyphal extension.25 However, in contrast to vegetative hyphae, the Spitzenkörper in fusion hyphae persists after they have made contact with each other, stopped growing and a fusion pore formed. This suggests that the Spitzenkörper in fusion hyphae continues to provide secretory vesicles for wall synthesis during cell swelling, adhesive molecules for adhesion, and lytic enzymes to allow dissolution of cell wall material.24

All of the mutants (nrc-1, mak-2, ham-2 and so) which are compromised in CAT induction and homing (Fig. 3) are also unable to undergo hyphal fusion in mature colonies. However, we do not know the precise stages at which the fusion process is blocked in mature colonies.

Nematophagous fungi undergo a specialized type of self-fusion which results in the formation of simple rings (Fig. 6A), complex rings that can form net-like structures (Fig. 6B), or constricting rings. These structures are all designed to trap nematodes either by ensnaring them passively (with simple and complex rings), or actively (with constricting rings).26 The development of these structures can be elicited by the presence of nematodes. Pramer and Stoll27 coined the term nemin to describe the inducer. Nordbring-Hertz28 later showed that di- and tri-peptides containing valine were very effective in inducing traps under nutrient poor conditions.

Figure 6. Low-temperature scanning electron microscopy of ring traps produced by the nematophagous fungus Arthrobotrys oligospora.

Figure 6

Low-temperature scanning electron microscopy of ring traps produced by the nematophagous fungus Arthrobotrys oligospora. A) Simple ring trap. B) Net-like ring traps. Bars = 10 μm.

CAT Fusion as a Model for Studying Vegetative Hyphal Fusion

Initial studies to systematically analyse the cell biology and genetics of vegetative hyphal fusion in N. crassa have concentrated on fusion between hyphae in mature colonies.17,23-24 Research is now shifting to focusing more on fusion between conidia and conidial germlings7,11,17,23 because they provide a much simpler and more experimentally amenable system in which to study the process of vegetative hyphal fusion.7 CAT fusion is thus being used as a model to study basic fundamental aspects of vegetative hyphal fusion. However, although there are many features of CAT fusion which are common to the fusion of hyphae in the mature colony, there are also some differences. Firstly, CATs are short (Fig. 2)7,11 whilst fusion hyphae vary from being short peg-like structures (Fig. 5) to being reasonably long (Fig. 5), and often dichotomously branched hyphae.24 The isolation and characterization of mutants which form fusion hyphae but not CATs (or vica versa) should be useful to understand the significance of the morphological variation between these different types of hyphae. The second difference relates to fusion hyphae and CATs being in a different physiological state. Cytoplasmic and organelle mixing is usually very rapid between hyphae in the mature colony but is very slow between fused CATs. We have speculated that there might be slight differences in the turgor pressures of fusion hyphae which results in the rapid bulk flow of cytoplasm and organelles.24 It may be that the turgor pressure differential between fusing CATs is much less or nonexistent.

Functions of Vegetative Hyphal Fusion

We have suggested that CAT fusion may have two roles.7 Firstly, CAT fusion may function in improving the chances of colony establishment by allowing heterogeneously distributed nutrients or water within the environment to be shared between different conidial germlings. Secondly, CAT fusion may play an important role in providing a mechanism for gene transfer as a prelude to nonmeiotic gene recombination following nonself fusion.7,29-30 Our preliminary results indicate that the incompatible response following heterokaryon formation, that normally results in a form of programmed cell death (see below), is suppressed for an extended period during the early stages of colony establishment. 7 CAT fusion during this period may provide a ‘window of opportunity’ for nonmeiotic recombination to occur. If true, then this may provide a mechanism to explain how much of the genetic variation arises in species in which sexual forms are rare or nonexistent in nature.7

Within the mature colony, vegetative hyphal fusion seems to serve a number of different functions. By interconnecting hyphae within the fungal colony (Fig. 1), hyphal fusion significantly contributes to its supracellular state.31 The supracellular fungal colony is a combination of being a syncytium (in which hyphae have fused together) and a coenocyte (in which individual mitoses are not associated with individual cell divisions). Indeed, adjacent hyphal compartments are separated by septa possessing pores which are commonly open and allow movement of cytoplasm and organelles between hyphal compartments. The supracellular nature of the colony of a filamentous fungus allows it to act as a cooperative, and confers novel yet little understood mechanisms for long distance communication, translocation of water, and transport of nutrients within the typically heterogeneous environments in which they reside.31 This can be particularly important for the flow of nutrients and water to fruitbodies and other multicellular structures.5 Furthermore, self fusion between multiple colonies can allow them to act cooperatively in supporting one or more large fruitbodies such as toadstools.4 In general terms, hyphal fusion must contribute significantly to the overall homeostasis of a fungal colony.

Features of Hyphal Fusion in Common with Yeast Cell Mating and Appressorium Formation

Our initial studies on the intracellular signal transduction pathways involved in vegetative hyphal fusion indicate that this process of self fusion exhibits similarities (e.g., with regard to MAP kinase signalling) to that of the nonself fusion involved in mating cell fusion in the budding yeast. The latter involves cells of each mating type producing a different peptide pheromone (α- or a-factor).32 However, it seems likely that the process of hyphal self fusion involves the production of the same self-signalling ligand by the CATs or fusion hyphae which are going to fuse. How a self-signalling ligand can provide recognition between two hyphae of the same genotype to orchestrate their induction and homing prior to fusion, is at present a mystery. However, it seems probable that this CAT inducer/CAT chemoattractant, which may or may not be the same molecular species, is a peptide because this would provide specificity11 (the homing and fusion of CATs has been shown to be strongly species specific).33 Other features which hyphal fusion and yeast cell mating have in common are that they both involve chemotropic growth of cells towards each other, cell adhesion and cell wall digestion.34

Hyphal fusion also exhibits a number of similarities with the formation of an appresorium (a type of infection structure) and its penetration of a plant host cell. Firstly, mutations in mak-2 homologues in various plant pathogens inhibit appressorium induction indicating that MAP kinase signalling of the type involved CAT induction and in hyphal fusion in the mature colony, is involved in this process too.17-20 Secondly, both hyphal fusion and appressorium formation typically involve cell adhesion, swelling, and cell wall digestion.24,35

It will be interesting to determine how much of the genetic and biochemical machinery involved in hyphal fusion is also involved in yeast cell mating and in appressorium formation.

Vegetative Hyphal Fusion and Heterokaryon Incompatibility

Vegetative hyphal fusion between different colonies carries risks of transmitting infectious cytoplasmic elements such as mycoviruses36 and senescence plasmids,37 as well as risks of nuclear parasitism. 38 As a cellular defence mechanism, filamentous fungi have evolved means for recognizing fusions between hyphae of different genotypes and this typically results in an incompatible reaction which prevents heterokaryons from developing further.2,3,39

In N. crassa, heterokaryon incompatibility results from allelic differences at heterokaryon incompatibility (het) loci. Fusion between het-incompatible hyphae typically results in rapid hyphal compartmentation and death of the hyphal fusion cell (Fig. 7). This involves the plugging of septal pores to compartmentalize and physically isolate hyphal segments, increased vacuolarisation of the cytoplasm, increased permeability of the plasma membrane and organelle membranes, the release of hydrolytic enzymes into the cytoplasm, and organelle degradation.2-3 The destruction of the heterokaryotic cell (and often some surrounding cells) can be complete within 30 min following hyphal fusion.40

Figure 7. Heterokaryon incompatibility in a mature colony of Neurospora crassa resulting from the fusion of het-cOR and het-cPA strains.

Figure 7

Heterokaryon incompatibility in a mature colony of Neurospora crassa resulting from the fusion of het-cOR and het-cPA strains. Both strains are stained with the membrane-selective dye FM4-64 and the nuclei in the het-cOR strain are labelled with H1-GFP. (more...)

In N. crassa there are 11 het loci with two or three alleles at each locus.41 Five of these het genes (mat A-1, mat a-1, het-c, het-6 and un-24) have been cloned and the products of these genes have been found to be very diverse indicating that each het locus involves a different mechanism of nonself recognition.2 Nonself recognition at the het-c locus has been shown to be mediated by a heterocomplex of polypeptides encoded by het-c alleles of alternative specificity and to be localized at the plasma membrane.42

tol and vib-1 have been found to be downstream effectors of heterokaryon incompatibility in N. crassa: tol suppresses mat heterokaryon incompatibility43-46 whilst vib-1 (which encodes a putative transcription factor) suppresses both mat and het-c incompatibility.47-48

Concluding Comments

Although much is known about nonself fusion between nonidentical cells (e.g., sperm and egg in animals; mating cells in yeast), little is known about self fusion between genetically identical cells (e.g., between myoblasts during muscle formation), and particularly with regard to the mechanistic basis of self-signalling. Self fusion, in the form of hyphal fusion, is a defining feature of colony morphogenesis in filamentous fungi. Understanding hyphal fusion in the model genetic system N. crassa, provides a paradigm for self-signalling mechanisms in eukaryotic microbes and might also provide a model for understanding somatic cell fusion in other eukaryotic species.1

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