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• W2036555935 abstract "In a recent letter to New Phytologist, Selosse & Schardl (2007) convincingly argued that, after the allopolyploid hybrid grass endophytic Neotyphodium spp. were first formed, they were ‘saved’ by conversion to vertical transmission, with the primary sexual horizontal transmission mechanisms of the ‘parent’ species being lost. They further argued that the hybrids probably arose through parasexual crosses after the dual colonization of a plant species which was an ‘unusual’ host for both the ‘parental’ pathogenic Epichloë species. Rightly, in our opinion, they stated that their model ‘emphasizes the role and consequences of hybridization in fungal evolution’, adding that ‘[it] may apply to a much wider range of fungi’. Whilst we agree with these authors on the important role that interspecific hybridization giving rise to allopolyploid hybrids can play in fungal evolution and accept that their model may apply to other fungi, particularly other endophytes, we wish to point out that it does not apply to the two known cases of allopolyploid fungal plant pathogens. Vascular wilt diseases caused by Verticillium species occur in a wide range of dicotyledonous hosts. The pathogens are soil-borne hemibiotrophs, infecting via roots and colonizing the plant before long-lived resting structures (microsclerotia or dark resting mycelium for the two most important species) are produced during a necrotrophic stage. Resting structures are returned to the soil in plant debris and may persist for several years in the absence of hosts (Pegg & Brady, 2002). Long-spored Verticillium dahliae isolates have been shown to be allopolyploid (or amphihaploid, a term we have previously used to describe the specific case of two almost entire haploid genomes, each derived from different species, occurring in a single nucleus; Barbara & Clewes, 2003; Collins et al., 2003) hybrids between haploid, short-spored V. dahliae and a second species, initially thought to be V. albo-atrum (Karapapa et al., 1997) but which is molecularly distinct from known isolates of this species and may represent a currently undescribed species (Barbara & Clewes, 2003; Collins et al., 2003; E. Clewes et al., unpublished). Molecular studies have divided the allopolyploid isolates into three types, which in part parallel host specificity in the field (Collins et al., 2003; E. Clewes et al., unpublished). With very few possible exceptions the hybrids occur only in crucifers and with two main exceptions only long-spored isolates have been obtained from crucifers. Both long- and short-spored isolates occur in horseradish (Armoracia rusticana) in the USA (Babadoost et al., 2004) and in horticultural crucifer crops (notably Chinese cabbage (Brassica rapa) and Japanese radish (Raphanus sativus)) in Japan (Horiuchi et al., 1990). Many other species can be infected with allopolyploid isolates experimentally but at present there is no evidence that natural infection of species outside the Brassicaceae is important or that they actually act as reservoirs for such isolates in the field, as has been suggested might occur (Johansson et al., 2006). Whilst both allopolyploid and haploid isolates of V. dahliae can be seed-borne (Pegg & Brady, 2002), occasionally at high rates, for example, in lettuce (Lactuca sativa) (Vallad et al., 2005), the levels of allopolyploid isolates in seed from naturally infected plants, where studied, appear to be low (e.g. Heppner & Heitefuss, 1995) and the primary route of transmission of allopolyploids in crucifers is horizontal via resting structures (microsclerotia) returned to the soil in plant debris. At present, when or where these three groups of hybrids arose is not known, or even if they represent three separate hybridizations or divergent lines from a single event, but unless they have subsequently reverted to horizontal transmission (which seems unlikely) the hybrids have not been ‘saved’ by switching to vertical transmission in the continuing presence of horizontally transmitted ‘parents’ as proposed for endophytes by Selosse & Schardl (2007). However, the novel host part of the endophyte model may apply to the Verticillium hybrids. Apart from the exceptions already mentioned, nonhybrid isolates of either V. dahliae or V. albo-atrum are not isolated from crucifers in the field. As the ‘nondahliae’ parent has not been unequivocally identified, be it either V. albo-atrum (as originally suggested by Karapapa et al., 1997) or another species (Collins et al., 2003, 2005), we cannot rule out the possibility that it infects crucifers (perhaps only occasionally or in a little-studied species or geographic region) but as candidate isolates with the appropriate molecular attributes have been sought in crucifers but not found (Barbara & Clewes, 2003; Collins et al., 2003, 2005) we assume that it normally occurs in a noncrucifer host. Therefore it is probable, but not certain, that the hybrid has an altered host range relative to its ‘parents’. As these fungi have no sexual stage, we assume that hybridization occurred through hyphal fusion followed by nuclear fusion. In accordance with the model of Selosse & Schardl (2007), the most obvious site for this would be in a dually colonized crucifer which is a poor host for both the parental haploid species; spread of the hybrids to other crucifers and host selection would then have led to the development of a widespread host-specific pathogen. The identity of the host in which hybridization occurred is not known. Horseradish or the horticultural crucifer crops of Japan seem unlikely, as haploid V. dahliae infect them commonly and they would not have provided the necessary selective advantage. A crucifer slightly more resistant to haploid isolates than these but still susceptible to low-level infection seems more likely. An alternative scenario is that fusion between the ‘parent’ haploid species occurred in a doubly-infected noncrucifer plant which is a good host for both species. However, in such a host, there would be no immediate selective advantage for the hybrid and the fused nuclei, presumably few in number relative to those of the ‘parental’ species, would have to have been incorporated into microsclerotia, returned to the soil and infected a new (crucifer?) host resistant to the ‘parental’ species before they had any selective advantage. A second alternative is that hyphal fusion occurred before root penetration following germination of resting structures of the two ‘parent’ haploid species physically close in the soil. In this scenario, it is possible that the first host of the hybrid was actually a complete nonhost for the haploid species (as long as it was capable of stimulating germination of the resting structures) and would therefore apply much stronger selection pressure for the novel pathogenicity of the hybrid. Whether fusion between the hypha from germinating resting structures is possible has not been studied. Neither part of the model proposed for grass endophytes by Selosse & Schardl (2007) appears to hold for allopolyploid hybrids of Botrytis which occur exclusively on onion (Allium cepa) and related species and can cause neck rot, most often in storage. These hybrids and their ‘parents’ are soil-borne pathogens overwintering as sclerotia on debris or free in the soil. Although they can be seed-borne, transmission is primarily horizontal. Botrytis allii has been divided into two groups, one with small conidia and 16 chromosomes and the other with large spores and 32 chromosomes (Shirane et al., 1989). Molecular studies using a number of markers have convincingly shown that isolates of the 32-chromosome type are not autodiploids derived from the 16-chromosome type as suggested by Shirane et al. (1989) but arose as an allopolyploid hybrid between Botrytis aclada and Botrytis byssoidea (Nielsen et al., 2001; Nielsen & Yohalem, 2001; Yohalem et al., 2003; Staats et al., 2005). It has now been proposed that the name B. allii be applied specifically to the hybrid species (Yohalem et al., 2003). None of the three species has a sexual stage and it has been suggested that sclerotia may have acted as a recipient for spermatia (microconidia) produced by B. aclada (Staats et al., 2005). As all three species infect Allium, the hybridization presumably took place either on a common host or in the soil near it. There seems no reason to invoke a species that is a poor host for the ‘parents’ but good for the hybrid as no new host specificity has arisen. As with Verticillium, transmission of both the hybrids and haploid ‘parents’ remains primarily horizontal and a switch to vertical transmission does not account for the success of the hybrids. This may need re-investigation, however. Transmission of B. allii from seed to seedling has been reported, but, both in the original study (Tichelaar, 1967) and in more recent studies on seed transmission (du Toit et al., 2004; Chilvers et al., 2007), B. allii and B. aclada were not differentiated and it may be that only one of the species is transmitted in this way, possibly giving it an advantage. In contrast to Verticillium, it is also difficult to make a case for a new host specificity ‘saving’ the hybrid as all three species cause neck rots of onion with little, if any, difference between them (D. Yohalem, pers. com.). There may be some so far unnoticed ecological difference between the species that led to the hybrid persisting in the continued presence of the parental species, but to date we have seen no suggestions as to what advantage the hybrid B. allii might have. As noted at the beginning of this letter, Selosse & Schardl (2007) have proposed a convincing model to explain the initial success of allopolyploid hybrid grass endophytes, based on a switch to vertical transmission and the development of new host specificities. Two examples of allopolyploid plant pathogens are known. New host specificity may be sufficient to explain the existence of the hybrid Verticillium isolates in cruciferous hosts, but neither hybrid has switched to primarily vertical transmission and to date we have seen no explanation for the success of B. allii on onions. In conclusion, the evidence suggests that their model cannot be applied directly to the currently known plant pathogenic allopolyploid hybrids. We are grateful to David Yohalem, East Malling Research, for his helpful comments on a draft of this letter." @default.
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• W2036555935 title "Two allopolyploid ascomycete fungal plant pathogens were not rescued by vertical transmission" @default.
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