Stabilisation of polymorphism in multi-locus gene-for-gene relationships

A. Tellier and J. K. M. Brown

Department of Disease and Stress Biology, John Innes Centre, Norwich, NR4 7UH, UNITED KINGDOM

In the gene-for-gene (GFG) relationship, plant defences are only effective when a resistance gene interacts with a specific avirulence gene in the parasite. A major challenge for theoreticians has been to account for the maintenance of genetic polymorphism in this system, for which there is much evidence from field and molecular data. Constitutive costs of resistance and virulence are the most obvious explanations, but evidence for high values of such costs is limited.

We have developed a new theoretical framework to investigate gene-for-gene co-evolution. This predicts a general theoretical condition required to obtain stable polymorphism and enables links to be developed between theory and realistic situations in nature. Based on this theory, the maintenance of polymorphism in gene-for-gene interactions can be explained by taking into account such factors as spatially structured populations, year-to-year survival of a seed bank and the epidemiology of the pathogen. A key development of previous theory is that host plants may be attacked within one growing season by a succession of possibly different genotypes, virulent or avirulent, of a polycyclic parasite. Under this assumption and assuming high auto-infection rates, stable polymorphism can be achieved with realistically small constitutive costs of gene-for-gene resistance and virulence.

In a multi-locus GFG system, we show that in monocyclic diseases, polymorphism is only transient and is due to the recurrent appearance of new genotypes by mutations. In polycyclic diseases, however, stable polymorphism at both loci in host and parasites, i.e. maintenance of all possible genotypes, can be maintained with high auto-infection rates and moderate disease severity. Multi-locus gene-for-gene interactions therefore reduce further the costs of resistance and virulence needed for polymorphism to be stable. We also compare the co-evolutionary outcome in multi-locus GFG systems (e.g. RPM1, RPS2 in A. thalliana) with another common recognition system in plants, a system in which a several alleles at one locus in the plant recognise avirulence genes at different loci in the pathogen in an allele-for-gene (AFG) system (e.g. the Mla locus in Barley). We show that co-existence of these two recognition systems depends on the relative values of the two types of costs: adding a new resistance locus (multi-locus GFG) compared to adding a new resistance allele at the AFG locus. Polycyclic diseases and high auto-infection rates increase the likelihood of maintaining polymorphism and the co-existence of these two recognition systems in panmictic populations.