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Home , Fungus

The Origin of in Fungi

Tatiana Giraud*, Pierre Gladieux fungal species, just like most and that many cryptic species exist in and Michael Hood , have been recognized using groups of fungi where morphological morphological characters. Since the last characteristics provide little or no *Corresponding author: century, experiments with crosses ability to distinguish them. For instance, Departement Genetique have also been used to assess which genealogies based upon DNA sequences et Ecologie Evolutives groups are reproductively compatible have discovered eight cryptic species Laboratoire Ecologie, Systématique with each other. These experiments within a single morphological species et revealed that crosses between some in the (Dettman et UMR 8079 CNRS-UPS-AgroParisTech fungal strains were impossible even al., 2003a). In contrast to the situation Bâtiment 360, Université de Paris-Sud though they were thought to belong in Ascomycetes, DNA analyses have 91405 Orsay cedex France [email protected]

The problem of speciation

The origin of new species is one of the most central and persistent challenges in , being the process by which the great diversity of is generated. Understanding how 1.5 million fungal species have arisen over the past 500,000,000 is of fundamental importance, yet there are also important consequences regarding agricultural , emerging human , or fungi used for agriculture, industry, and . Although tremendous progress on the origin of species has been made since the book of Darwin’s book (1859), the subject remains heavily debated and with many recent realizations about the that underlie speciation processes. To study speciation (i.e. the origin Figure 1. species. of new species), it seems necessary to first define what a species is. All to the same species, indicating the not revealed many cryptic species in more or less agree that species existence of several hidden or “cryptic” -forming basidiomycete represent different lineages that evolve species within a group known by a fungi, maybe because mating tests and independently, without freely exchanging single taxonomic name. This was the morphological characteristics of the (De Queiroz, 2007). This means case, for instance, in the mushroom cap were already sufficient to that occurs within species, and that were once thought to be the species correctly delimitate most species (Le Gac mating between species is absent or very , but where the strains and Giraud, 2008). exceptional. This is highly applicable from North America could not mate Our modern DNA techniques have to fungi because many, although not with strains from Europe (Anderson et nevertheless revealed a much richer all, species indeed mate and undergo al., 1980; Anderson and Ullrich, 1978). diversity of fungal species than was regular sexual in . More recently, technological advances previously recognized, particularly In fact, the structures we enjoy eating have allowed copying and sequencing among the smaller and less conspicuous are the result of sexual development DNA from regions of fungal , forms (Taylor et al., 2000). Consequently, of basidiomycete fungi, and even of which yield insights directly into the the question of how such new species some ascomycete fungi (e.g. morels and amount of genetic exchange between arise in nature has become a highly ). groups of ; in modern terms, active of research, and fungi provide A major obstacle, particularly for this measure of genetic exchange is a most tractable model for addressing fungi, has been to recognize and central to the very definition of “species.” speciation more broadly across all delimit species in nature. Classically, Such DNA technologies have revealed Continued on page 24. FUNGI Volume 3:4 Fall 2010 23 eukaryotic kingdoms (Giraud et al., 2008; graminicola. This arose of premating barriers in basidiomycete Kohn, 2005). recently, most probably during wheat mushrooms are contrasted by many It has long been believed that species in the Fertile Crescent, ascomycete fungi, including numerous originate mostly through their isolation by sympatric differentiation from pathogens, where there are often in different geographic areas (i.e. pathogens of natural no premating barriers dependent upon “allopatric divergence”) because extrinsic grasses (Stukenbrock et al., 2007). geographic provenance. For example, geographic barriers seemed obvious closely related ascomycete species are impediments to genetic exchange. In able to mate freely when experimentally fact, among the numerous recently Nature of reproductive crossed (Le Gac and Giraud, 2008), discovered complexes of cryptic species, isolation in fungi but at least for many plant pathogenic many appear consistent with such Ascomycetes hybrids are not formed in allopatric divergence, where genetically As seen above, an essential character nature because the species are adapted isolated species occupy non-overlapping of speciation in sexually reproducing to different plants and mating occur geographic ranges. This is the case organisms is the emergence of barriers to on or inside the plants where they grow. for instance in what was known as flow, i.e. mechanisms that prevent As mentioned above, such adaptation Armillaria mellea (Fig. 1), as mentioned matings from spreading genes from to the host plant can itself constitutes above, where North American and one group of organisms into another. a type of premating barrier: fungi do European strains have been shown to Two types of reproductive barriers are not mate with each other because they belong to different species (Anderson et usually distinguished, premating and cannot grow together on the same host al., 1980). Similarly, the genus , postmating, depending on their of plant (Giraud et al., 2006). which contains the mushrooms occurrence, before or after fertilization. Postmating barriers refer to the cultivated for centuries in and Assortative mating is the most inviability and sterility that is often , was shown to encompass seven common premating barrier, which occurs observed in hybrids. In such cases, cryptic species using genealogies based when individuals or are able to crosses between evolutionary lineages on comparing DNA sequences. The bias mating partners to those that are occur and lead to the production of most ancient divergence in the Lentinula similar to themselves. Assortative mating hybrids, but they exhibit little ability to corresponded to species in the Old seems to be especially important in the grow and develop or to further produce World versus the New World, and age reproductive isolation of mushrooms, functional offpsring. For instance, of this divergence could correspond where the clamp connections between crosses among Neurospora species led to the fragmentation of the Laurasian the fungal cells that reflect the onset of to the production of few and abnormal supercontinent (Hibbett, 2001). mating and fructification fruiting structures (perithecia) and In contrast to the wide acceptance of are almost exclusively observed when viability was low (Dettman allopatric divergence, the possibility of the tested mycelia belong to the same et al., 2003b). Relatively few studies have speciation occurring without geographic species (Le Gac and Giraud, 2008). Such reported hybrid inviability or sterility in separation (i.e. “sympatric divergence”) assortative mating has been observed for mushrooms because the experimental had long been dismissed, particularly instance between very close species of induction of is often very for sexual organisms. If populations the saprophyte mushrooms in the genera difficult (unfortunately for mushroom live in the same area and can meet and , , and eaters). It is therefore difficult to analyse exchange genes, it is indeed difficult , or between related species experimentally the progeny of hybrids in to understand how they can become of the ectomycorrhizal mushrooms mushroom-forming fungi. sufficiently isolated and diverge to , and . An interesting and different type become new species. Even relatively However, these premating barriers of reproductive isolation is when a rare matings at each generation should are often weaker when the species do new species originates as the result cause the genetics of the two populations not live in the same geographic area, of hybridization between two extant to become homogenized, which for instance on different continents. species. This phenomenon is not would impede adaptation to different Presumably geographic isolation uncommon in fungi (Olson and resources or habitats (Maynard Smith, prevents selective pressure to prevent Stenlid, 2002). A remarkable example 1966). Theoretical models have shown, crosses between incipient species (Le is that of the however, that sympatric divergence Gac and Giraud, 2008), whereas when × columbiana that emerged from could be possible under certain species live in sympatry there may be hybridization of M. medusa, a parasite conditions, in particular for pathogenic selection to avoid the cost of producing of the poplar tree Populus deltoides, fungi that mate on their host plants, hybrids that would likely be unviable and M. occidentalis’ parasite of the tree or saprophyte fungi that mate within or sterile (i.e. postmating barriers as P. trichocarpa (Newcombe et al., 2000). their specialized (Giraud et described below). In the saprophyte This hybrid emerged in 1997 when al., 2006), because gene exchange can mushroom for instance, a poplar hybrid resistant to the two then occurs only between fungi adapted premating barriers are always complete parental rust species was widely grown to the same host or substrate. Cases of between species from the same continent in California, and the hybrid rust fungus speciation in sympatry by adaptation but species from different continents was able to infect the newly cultivated to different host plants have been can be crossed experimentally (Boidin hybrid poplar. Several other cases have suggested for instance in Mycosphaerella and Lanquetin, 1984). These examples been reported of hybrid speciation in 24 FUNGI Volume 3:4 Fall 2010 fungi, mostly in Ascomycetes, such grouped under the as in the fungal of grasses species name (Moon et al., 2004), but violacea, in the genus of no cases of hybrid speciation are known fungi from grasses in mushrooms, possibly because most of because their similar the close species living in the same area appearance. However, exhibit complete premating isolation or with the advent of intersterility, impeding the production of new techniques for viable hybrids. DNA sequencing, anther-smut fungi were reassigned to the Asexual fungi of fungi related to the rusts (as distant Many fungi appear exclusively clonal, a reassignment as without any ability to undergo sexual between rust fungi reproduction. In asexual fungi, the and the familiar theoretical issues of species formation mushroom-forming are completely different from those in ), sexual organisms. There is no mating to illustrating how the new homogenize the gene pools or prevent molecular paradigm divergence between populations. Any Figure 2. of in the anthers of now drives classification new form of a gene (an allele) allowing the plant Silene uniflora. of fungal species adaptation to a new environment can (Swann et al., 1999). thus give rise to a new and isolated on wild plant species in the carnation More recently, DNA sequencing has , essentially a new “species.” The family (Caryophyllaceae), and these revealed little to no exchange of genes difficulty in asexual organisms is rather fungi have a remarkable life history; they between anther-smut fungi found on to understand why discrete entities exist different hosts, even when they occur that we can recognize as species instead in sympatry, and new species are now of continuous distributions of characters. being named based upon this modern A possible explanation for this is that molecular criterion (Le Gac et al., 2007a). asexual species seem to emerge regularly Curiously, diverse anther-smut fungi are from sexual species, but do not last able to recognize and mate with each for very long in ecological . For other, and there appears to be no negative instance, in the fungus , there effect based upon how distant the species seem to be many recent asexual species are (Le Gac et al., 2007b). It may be deriving from sexual species in the genus that the mating signals (pheromones (LoBuglio et al., 1993). and receptors) are highly conserved, Another explanation for the existence and in fact the pair of two alternate of discrete asexual species could be the Figure 3. Sporidia of Microbotryum mating receptors in Microbotryum has adaptation to particular environments, mating on a medium. an origin nearly as old as the fungal or for pathogens to different hosts. The (Devier et al., 2009). However, clonal fungus Penicillium marneffei for produce fungal in place of the the viability of hybrids, and even more instance, the causal agent of plant’s pollen and are then spread to new so their fertility, are greatly reduced in in immuno-compromised humans, hosts by the normal insect pollinators, comparison to non-hybrids (De Vienne exhibits geographic endemicity despite resulting in a disease called “anther et al., 2009; Le Gac et al., 2007b; Sloan long-distance migration via aerially smut” (Fig. 2). The conspicuous disease et al., 2008). Like many fungi, there is a dispersed spores. Different clones of symptoms and the ease of culturing high rate of change in the the fungus seem to be associated with Microbotryum in the lab (Fig. 3) caught structure among Microbotryum (Zolan different environmental conditions, the attention of early mycologists and 1995; Perlin 1997), and this can inhibit which suggested that adaptation to naturalists, who used anther-smut the division that would normally these environments is constraining the fungi to address questions about produce the haploid gametes (De Vienne ’s ability to successfully disperse specialization, Mendelian inheritance et al., 2009). Nevertheless, there is in nature (Fisher et al., 2005). of mating factors, and barriers to evidence of rare and quite ancient genetic reproduction (Goldschmidt, 1928; Kniep, exchange between Microbotryum species 1919; Liro, 1924). Recently, applications that may have given rise to a new species , of molecular approaches and DNA (Devier et al., 2010), and the conditions the anther-smut pathogen sequencing have provided many new necessary for this mode of speciation are insights into the dynamics of speciation currently being pursued. Basidiomycete fungi in the genus in these fungi. Microbotryum are found as pathogens Anther-smut fungi were originally Continued on page 26. FUNGI Volume 3:4 Fall 2010 25 annosum

The basidiomycete is responsible for - and butt-rot on and has long been considered as a single species with a wide host range. However, experimental crosses have revealed that not all strains would mate one with each other (Stenlid and Karlsson, 1991). Three groups have been defined based on intersterility, and they showed different ecological preferences: The S group (renamed H. parviporum) is a pathogen almost exclusively of (Picea abies) in most parts of Europe and of Siberian fir () in northeastern Europe, while the P group (H. annosum) is found mostly on , and the F group (renamed H. abietum) is more saprophytic, although sometimes also pathogenic on spruce species. Experimental crosses revealed that five genes were involved in intersterility (Chase and Ullrich, 1990). In agreement with the expectation that Figure 4. Symptoms of inaequalis on . premating isolation should be selected for in sympatry, intersterility appeared years. The first breakdowns of the Vf Consistent with this idea, measures of lower among allopatric strains of resistance were reported in 1988 from the success of fungal isolates different groups (from North America , in 1989 from England, and of Vf and non-Vf host varieties on the and Europe) than between sympatric then in several other European countries. reciprocal host type in fact showed a strains. The differentiation of these In France, the first isolates breaching Vf strict host specificity of the two fungal Heterobasidion species was suggested to resistance have been observed in 1995 populations. This host specificity barrier have occurred following the migration from a single orchard of cider apples in may thus alone be responsible for the of the main spruce and fir hosts, into Normandy. The subsequent spread of observed reproductive isolation between Europe from eastern Asia (Johannesson the disease on this cider variety sympatric populations of V. inaequalis. and Stenlid, 2003). in Northwest France was monitored over 10 years. Genetic analysis showed that a single mutation overcame Vf Conclusion , resistance and subsequently spread the in fungal populations. However, the In conclusion, major advances on virulent and avirulent fungal populations speciation in fungi are currently being Venturia inaequalis is an ascomycete have remained genetically separated made, and their broad distribution, responsible for the scab disease on despite their co-occurrence in orchards biological importance, and easy of apples (Malus spp.) (Fig. 4), and appears containing both resistant and susceptible experimental manipulations have led to be a good model for sympatric trees (Guérin et al., 2007; Guérin and fungi to be among the most tractable speciation in fungal pathogens. Genes Le Cam, 2004). What could explain models for the general study of conferring resistance to the pathogen their isolation in the face of a life cycle speciation across all of have been identified in apple trees and with regular ? The (Giraud et al., 2008; Kohn, 2005). used in orchard production. Most of hypothesis of inter-sterility was not Fungi also exhibit some specific and the resistance genes are however no supported by the observation that viable interesting modes of speciation, and longer efficient as novel virulences progeny could be produced between many open questions remain which will having evolved in the fungal populations. them experimentally (Benaouf and Parisi, be fascinating to explore. One interesting exception is the Vf 2000). Reproductive isolation could resistance gene. This resistance gene be due to a mere host specialization to has long been considered as a unique Vf and non-Vf host varieties (Giraud Acknowledgements example of durable plant resistance, et al., 2006) since this fungus mates conferring complete field immunity within the leaves of its host tree after We acknowledge the grants ANR 06- to V. inaequalis during more than 40 having grown an infectious . BLAN-0201 and ANR 07-BDIV-003. We 26 FUNGI Volume 3:4 Fall 2010 thank Bruno Le Cam for the picture of Microbotryum violaceum species Giraud T. 2007a. Phylogenetic evidence the apple scab. complex to investigate possible events of of host-specific cryptic species in the speciation by hybridization. Mycologia anther smut fungus. Evolution 61: 15–26. 102:689-96. Le Gac, M., Hood M. E., Giraud References Cited Fisher, M. C., Hanage W. P., de Hoog T. 2007b. Evolution of reproductive S., Johnson E., Smith M. D., White isolation within a parasitic fungal Anderson, J. B., Korhonen K., Ullrich N. 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J., Kroken S., polymorphism at pheromone receptor Le Gac, M., Giraud T. 2008. Existence Kasuga T., Geiser D. M., Hibbett D. S., genes in basidiomycetes. Genetics 181: of a pattern of reproductive character Fisher M. C. 2000. Phylogenetic species 209–23. displacement in but not recognition and species concepts in Devier, B, G. Aguileta, M. E. Hood, and in . Journal of Evolutionay Fungi. Fungal Genetics and Biology 31: T. Giraud, T. 2010. Using phylogenies Biology 21: 761-72. 21-32. of pheromone receptor genes in the Le Gac, M., Hood M. E., Fournier E., FUNGI Volume 3:4 Fall 2010 27