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Heterokaryon Incompatibility in Fungi More Than Just Another Way to Die

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Heterokaryon Incompatibility in Fungi More Than Just Another Way to Die J. Goner., Vol. 75, Number 3, December 1996, pp. 415-424. $]) Indian Academy of Sciences Heterokaryon incompatibility in fungi more than just another way to die JOHN F. LESLIE* and KURT A. ZELLER Department of Plant Pathology, Throckmorton Plant Sciences Center, Kansas State University, Manhattan, Kansas 66506-5502, USA Abstract. In filamentous fungi heterokaryon (vegetative) compatibility is regulated by a number of different loci. Vegetative incompatibili~:yis most often detected as the inability to form a prototrophic heterokaryon under forcing conditions, or as the formation of a barrage when two incompatible strains interact. Vegetative compatibility has been used as a multi- locus phenotype in analysis of fungal populations. In some highly clonal populations the vegetative-compatibility phenotype is correlated with pathogenicity. The molecular basis for vegetative compatibility is not well understood. Four he~ loci have been cloned from Neurospora crassa or Podospora anserina, but no two are alike and it is clear that the her genes themselves do not encode the gone products that are directly responsible for cell death. We suggest that a broader view of vegetative compatibility would include genes that are responsible for profusion, fusion, and posffusion activities. Postfusion activities could include the fungal apoptotie apparatus since microscopic observations of cell death resemble those in higher plants and animals. Keywords. Apoptosis; fungi;vegetative compatibility. 1. Introduction The ready formation of a heterokaryon involving hyphal fusion and nuclear mixing is common in fungi and is an integral part of their life cycle. To the inexperienced it may appear that any pair of strains are capable of forming a heterokaryon. Upon closer inspection, however, it quickly becomes obvious that heterokaryon formation is a complex process, and that not all pairs of strains are capable of forming hetero- karyons. Heterokaryons may form vegetatively or as a part of the sexual repro- duction process. In some species a difference at a single gone, determining mating type, simultaneously precludes formation of a vegetative heterokaryon between two strains and is essential for formation of a sexual heterokaryon between the same two strains. Although the phenomenology of this process is well understood, its molecular basis remains obscure. Linking the molecular basis of compatibility to its corresponding phenomenology should provide new insights into basic cellular mechanisms and identify relationships between compatibility and previously described processes. Neurospora crassa has played a major role in the study of vegetative (heterokaryon) compatibility. A genetic basis for the vegetative-compatibility phenomenon was first described by Beadle and Coonradt (1944), who determined that differences at the mating-type locus were sufficient to prevent formation of a vegetative heterokaryon. Efforts to separate the sexual and the vegetative compatibility functions of the mating-type locus by recombination were unsuccessful (Newmeyer and Taylor 1967; *For correspondence 415 416 John F. Leslie and Kurt A. Zeller Newrneyer et aI. 1973), although these functions can be inactivated independently by mutation (Griffiths and Delange 1978; Griffiths 1982). At least one allele at the tot locus can suppress the vegetative-corapatibility interaction at the mating-type locus (New- meyer 1970) even though tol neither reduces sexual fertility nor affects interactions between alleles at any of the other known her loci (Newmeyer 1970; Perkins 1975; Johnson 1979; Leslie and Yamashiro 1997). In N. tetrasperma, tol plays a crucial role in establishment and maintenance of the pseudohomothallic life style (Jacobson 1992). Three loci involved exclusively in vegetative compatibility were identified by Garnjobst (1953, 1955) and Wilson and Garnjobst (1966). One of these loci, her-C, has recently been cloned (Saupe et al. 1996). Mylyk (1975) expanded the number of her loci to ten by identifying regions that contained one, or more, heterozygous het loci through phenotypic differences in partial aneuploids. Genetic evidence consistent with existence of multiple alleles at individual bet loci has been reported (Howlett et al. 1993), but final confirmation of these results will require cloning the putative alleles and testing their fhnctional relatedness. The involvement of loci other than her loci in the vegetative- compatibility phenomenon has been recently described (Arganoza et at. 1994). Studies of vegetative compatibility in filamentous fungi have expanded to numerous other species, including species of Aspergiltus, Colletotrichum, Cryphonectria, Fusarium, Ophiostoma and Podospora. Three primary areas of study are: (i) descriptions of phenomenology, (ii) identification of population and evolutionary implications of heterokaryon formation, and (iii) elucidation of molecular mechanisms. Readers who want greater depth than is presented here should consult recent review articles by B6gueret et al. (1994), Glass and Kuldau (1992), and Leslie (1993, 1996). 2. Phenomenology The phenotypes of vegetative-incompatibility interactions and the methods used to detect them are critical to the understanding of vegetative compatibility. The most common phenotypes are (i) inability to form a prototrophic heterokaryon under forcing conditions, and (ii) formation of a barrage when two incompatible strains interact. The intensity of the interaction is known to vary depending on the locus, the alleles, and the number of gene differences involved (Mylyk 1975; Anagnostakis and Waggoner 1981). Most studies focus only on allelic interactions, i.e. incompatibility resulting fron~ interactions of different alleles at the same locus. However, nonallelic interactions, in which two alleles at different loci interact to give a vegetative- incompatibilityinteraction, are known in P. anserina (see Glass and Kuldau E1992] and B6gueret et al. [19941 for recent reviews). Existence of nonallelic interactions in other fungi has not been demonstrated. Heterokaryons resulting from protoplast fusion of otherwise vegetatively incompatible strains are often quite different from similar heterokaryons formed following hyphal anastomosis (Adams et al. 1987; Stasz et aI. 1989). The killing reaction seen in heterokaryons formed via hyphal fusion may be lacking in those formed following protoplast fusion (Dales and Croft 1977; Ferenczy et al. 1977; Peberdy and Ferenczy 1985; Moln~tr et al. 1990). These data, when combined with information on some of the cloned her loci, suggest that cell-wall or cell-lnembrane components are responsible for triggering the kitling reaction associated with vegetative incompatibil- ity. Such an explanation could also be used to explain the survival of heterozygous Heterokaryon incompatibility in Jhngi 417 partial diploids in Neurospora that carry both het alleles in the same nucleus (Mylyk 1975). If the vegetative-incompatibility reaction requires an interaction between two different cell walls (or cell membranes), the partial-duplication method of identifying het loci may miss some loci. An additional difficulty in characterizing hot genes is in cloning of the loci. Direct selection for transformants is possible in systems where barrages can be observed if a transformation results in a change fi'om one vegetative-compatibility group to another. Transformants would produce a barrage with neighbouring colonies of a different compatibility group and should be relatively easy to pick out. Cloning het genes in other systems is more difficult since the only obvious phenotype of hetero- karyons for alleles at a her locus is cell death. With individual clones it may be possible to transform strains that differ at a single hot locus, e.g. het-x ~ and het-xtL If the transforming DNA carries the het-x" allele, then a hot-x" recipient should grow normally, while a het-x u recipient should have at best the inhibited growth seen in a heterozygous partial duplication of the same composition. Successful cloning at- tempts have usually relied on a chrornosonae-walking technique to identify the initial library clones that are then subcloned to identify the hot allele. 3. Population considerations Under laboratory conditions, stable heterokaryons form only when the stratus are genotypically identical at all of the her loci. Under field conditions these different genotypes are called vegetative-compatibility groups (VCGs), and strains in one VCG are genetically isolated from strains in other VCGs during asexual reproduction. VCGs serve as a natural means to subdivide populations of fungi that spend a large fraction of their life cycle reproducing asexually (Leslie and Klein 1996). If selection acts to maintain a la'ge number of VCGs within a population, perhaps due to values of individualism (Rayner 1991) or to reduce the spread of infectious agents (Caten 1972; Hartl et at. 1975), then frequency- dependent selection may play an important :role in maintaining the array of VCGs and in keeping a large number of het loci heterozygous within the population. Population studies rely heavily on the ease with which strains can be assigned to a VCG. Barrage reactions are the fastest and easiest to assess since all that is required is to place two wild-type strains adjacent to one another on an appropriate medium and then score their interaction at a later date. Heterokaryon forcing techniques are somewhat more laborious than the simple assessment of barrage interactions. If heterokaryons are to be
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