Mating-type recognition

In self-sterile Ascomycetes (e.g., O. ulmi s.l.), mating controls initial fusion of the male and female sex cell (plasmogamy) and the subsequent formation of dikaryotic ascogenous hyphae necessary to form zygotes {[563]}. As applies to most fungi, the function of the mating-type recognition system of O. ulmi s.l. is to provide ascospore inoculum to facilitate survival and dispersal of the DED fungus at different stages of its life cycle. Since d-factors may not be transmitted through to the ascospores produced after mating between d-infected isolates, fitness will be ensured for a proportion of the fungal population {[541]}.

The mating-type system of O. ulmi s.l. involves two compatibility types – A and B – which are determined by two alleles – A and B – at the single mating-type locus mt. Inheritance of these alleles occurs in a normal Mendelian fashion. O. ulmi s.l. strains with various divergent genome architectures can be sexually compatible. However, incompatibility is observed when the mt alleles are the same {[530]}. Production of perithecia is used as a criterion for successful mating {[230]}. The two mating-types of O. ulmi s.l. are bisexual, i.e., they are able to function as either a female recipient or a male donor {[530]}.

Schafer et al. {[568]} and Ansina et al. {[569]} reported the presence of the O. ulmi mating types Ab, AB, and aB. However, according to Mitchell et al. {[174]} these three mating-type classes are due to mixture of isolates or pseudo-selfing in aging cultures. Pseudo-selfing – a phenomenon first described for O. novo-ulmi race NAN – is used to refer to the sporadic formation of perithecia in single mating-type cell cultures of the DED fungus. Mating type A arises from mating type B, e.g., by mutation from the B allele to the A allele at the mt locus, resulting in ascospores that segregate in a 1:1 ratio for mating types A and B. Whereas in a mycelially growing culture the mutated nuclei will probably be suppressed, in liquid shake cultures the yeast-like cells carrying the mutation may develop freely {[567]}. The reverse phenomenon (i.e., B type arising from mating type A cultures) is also found. Pseudo-selfing appears to occur more frequently in O. novo-ulmi (race NAN and EAN) mating type A cultures than in mating type B cultures. The perithecia produced after pseudo-selfing tend to have an irregular shape and form fewer ascospores, and are often smaller than those formed after normal outcrossing. In addition, the “pseudo-selfing” perithecia require a prolonged incubation period (3-6 weeks). On the elm twig surface, the presence of patches of felty, white mycelium is frequently associated with these perithecia {[541]}.

Cell suspensions of O. ulmi – either mating type A or B – are usually self-sterile, cross-fertile hermaphrodites. However, Holmes {[560],[564]} showed the occasional loss of the ability to act as a recipient (female) irrespective of mating type in laboratory cultures of O. ulmi that had been transferred several times onto cherry agar over a three-month period. Perithecia were found only when these cultures were used as a second inoculum. Female-only cultures have not been found {[560]}. Apparently, it is important to distinguish between the compatibility types A and B and sex(femaleness/maleness) {[541]}. The unisexual males-only cultures are as pathogenic as normal bisexual cultures (565}. The ability to mate of a stored O. ulmi culture dramatically decreases with time and is not enhanced after passage through elm trees and reisolation {[566]}.

The frequency of mating types A and B varies among species within the O. ulmi s.l. complex {[174],[535],[541]}. While as shown in Table 5 the mating type A:B ratio in nature is approximately the same for O. ulmi and O. himal-ulmi, mating type B predominates for the two races of O. novo-ulmi. Besides being species-specific, mating-type frequency appears to depend on the status of the DED epidemic and to vary geographically. In European O. ulmi isolates, the mating type A:B ratio approaches the overall 1:1; in North America, however, mating type A predominates for the latter species {[174]}. The mean value for the portion of mating type A in a population of O. novo ulmi is 15% {[520],[541],[561],[562]}. Hoegger et al. {[129]} report that 20 out of 52 O. novo-ulmi isolates in Switzerland exhibited mating type A (38%). This relatively high mating-type A frequency in Switzerland may be explained by the assumption that a clonal population of the DED fungus at the disease front (which commonly exhibits a low portion of mating type A) changes into a heterogeneous, post-epidemic population with increasing A-type frequencies. In a more heterogeneous population, influences of fungal pathogens (e.g., mycoviruses) will be diminished {[520],[521],[527]}.

Mating-type loci in ascomycetous fungi are sometimes found to play a role in processes other than mating, e.g., vegetative incompatibility, sexual dimorphism, ascospore dimorphism, and virulence {[563]}. A major vic locus appears to be linked to the mating-type locus mt in O. ulmi (1 unit or less, {[530]}). The mating-type system of O. novo-ulmi acts independently of the vegetative incompatibility (vic) system {[9]}. However, it has been suggested that in O. novo-ulmi the mt locus functions as a major regulatory gene of general colony development {[530]}. The locus for tolerance to the fungicides carbendazim (MBC) and iprodione are shown to be linked to the mt locus in O. ulmi and O. novo-ulmi {[571]}. For O. novo-ulmi race NAN and EAN, the mating-type alleles influence mycelial development {[541]}. Mating type A isolates tend to form numerous protoperithecia, exhibit lower growth rates, and are generally less pathogenic than B-type isolates {[312],[541],[572],[573]}. However, the recent experiments by Et-Touil et al. {[494]} did not show a linkage between the mt locus of O. novo-ulmi EAN and the pathogenicity gene Pat1. The scarcity of the A type in natural populations of O. novo-ulmi may be a result of the negative effect of the A mt allele on the fitness of this fungus {[535]}. Though much more fertile than B types, selection appears to occur against A types {[530],[588]}.