A MODEL FOR THE EVOLUTION OF FORMAE SPECIALES AND RACES

The basis of host-parasite specificity has been discussed by many and virulent cultures suggested involvement of four major genes. phytopathologists and other researchers. With the accumulation Each of the four genes corresponded to a single resistance gene of experimental data from genetic, cytological, and biochemical in wheat and was considered to be an AVR gene under the control studies, some basic concepts of host-parasite specificity have been of gene-for-gene interactions (15,18). The distortion of segregation developed. Day (2) distinguished two types of host-parasite interratios was not detected. Therefore, it is highly unlikely that the action: One determines whether or not a plant is a host for a modified model is applicable to our system. parasite, and the other determines the gene-for-gene specificity. What if there are many SSP genes in a forma specialis that Ellingboe (3) introduced the term basic compatibility to designate have small but additive effects like polygenes? In this case, F, a state of harmony between a host and a parasite developed by cultures that carry no SSP genes would occur in a very low ratio their interactions over a period of time and assumed that the and hardly affect the ratios resulting from the segregation of AVR gene-for-gene relationship was superimposed on basic compatgenes. In order to reconcile Heath's (9) modified model with our ibility. Heath (6) presented a more generalized concept. Specificity genetic evidence, SSP genes must be like polygenes. determining host species range was termed plant species specificity, Here I will argue that the evolution of formae speciales can and specificity determining cultivar range within a given host be explained by applying the original basic compatibility model species was termed cultivar specificity. In the former, compatibility (6), if the usage of the term nonhost is changed. A general is specific, and the resistance involved (nonhost resistance) is definition of nonhost is very difficult to give (7). Niks (11) called genetically complex. In the latter, incompatibility is specific, and a plant species a nonhost to a microbial strain when all members the resistance involved (cultivar resistance) is controlled by geneof the plant species were resistant to the strain. This definition for-gene interactions. Cultivar resistance was considered to be implies that a plant species is a nonhost to a forma specialis superimposed on basic compatibility resulting from the first type if all members of the plant species are resistant to the forma of interaction. This model was called the basic compatibility model specialis (11). Heath (8) argued that plant species that were of specificity (9). taxonomically related to host species of a forma specialis in Although this model has been widely accepted as a basic conquestion, but were hosts of other formae speciales, should not cept, some experimental data might be interpreted as suggesting be considered as typical nonhosts. However, it has been general that nonhost resistance is controlled by major genes (12), or that usage to call such plant species nonhosts, and Heath (9) has plant species specificity is controlled by gene-for-gene interactions followed this usage. The contradiction between the concept of (9). To address the apparent contradiction between the concept the basic compatibility model and experimental evidence in fungal and the evidence, Heath (9) presented a modified model for the systems (9,12) appears to be attributable to the traditional usage evolution of biotypes (formae speciales in fungi or pathovars in of the term nonhost. In my opinion, wheat is a host not only bacteria) and races. of E. g. tritici but also of E. g. agropyri. E. g. tritici establishes My coworkers and I showed that gene-for-gene interactions basic compatibility with both wheat and wheatgrass. These ideas played a role in determining the forma specialis-genus specificity may be supported by cytological data. Tosa et al (16) found that in the Erysiphe graminis DC. -gramineous plant system (15,18). E. g. agropyri penetrated cell walls of wheat leaves in the same Heath (9) suggested that our data could be explained by applying manner as E. g. tritici, and that the resistance of wheat leaves the modified model. In this letter I first discuss whether or not to E. g. agropyri was attributable to the hypersensitive reaction her modified model is compatible with our data, and second, of epidermal cells, a common factor in cultivar resistance. This present another model that illustrates the evolution of formae was the case in wheatgrass leaves inoculated with E. g. tritici. speciales and races of biotrophic fungi. Tosa and Sakai (18) concluded that the forma specialis-genus Heath's modified model assumes that parasite biotypes evolved specificity is a case of cultivar specificity, rather than plant species from a common ancestor carrying potential avirulence (AVR) specificity. On the basis of this concept, a hypothetical model genes by acquiring different species specificity (SSP) genes. In was constructed that illustrated the evolution of formae speciales her example, biotype 1 carries SSPW and SSPX to establish and races (Fig. 1). basic compatibility with plant species 1, and biotype 2 carries An ancestral fungus became a parasite of a range of ancestral SSPY and SSPZ to establish basic compatibility with plant species plant species by acquiring SSP genes to establish basic 2. If so, these genes should segregate in progenies from a cross compatibility with the plant species. The parasite also carried between the two biotypes. For simplification, let us assume that potential avirulence genes (Axl-Ax4 and Ayl-Ay4) that the parasite is haploid and that these genes are inherited indecontrolled characters other than avirulence. The host species pendently. Then, a fourth part of the F, population from biotype gradually evolved into several genera, X, Y, and so on. In this 1 X biotype 2 carries neither SSPW nor SSPX. When plant species process, plant genus X acquired resistance genes, Rxl and Rx2, 1 is inoculated with the F, population, the progeny without SSPW that recognized fungal features or products controlled by Axl or SSPX should induce nonhost resistance and distort ratios and Ax2, respectively. A portion of the parasite population accomresulting from the segregation of AVR genes. Tosa (14) crossed modated itself to plant genus X by rendering Axl and Ax2 E. graminis f. sp. tritici (parasitic on wheat) with E. graminis nonfunctional through random mutations and became forma f. sp. agropyri (parasitic on wheatgrass), and inoculated wheat specialis X. On the other hand, plant genus Y acquired other cultivars with their F, cultures. Segregation ratios of avirulent resistance genes, Ryl and Ry2, that corresponded to Ayl and Ay2, respectively. Another portion of the parasite population became virulent to plant genus Y by mutating Ayl and Ay2 and @ 1992 The American Phytopathological Society became forma specialis Y. These processes led to the establish-