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A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation

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Any given pathogenic microbial species typically colonizes a limited number of plant species. Plant species outside of this host range mount nonhost disease resistance to attempted colonization by the, in this case, non-adapted pathogen. The underlying mechanism of nonhost immunity and host immunity involves the same non-self detection systems, the combined action of nucleotide-binding and leucine-rich repeat (NB-LRR) proteins and pattern recognition receptors (PRRs). Here we hypothesize that the relative contribution of NB-LRR- and PRR-triggered immunity to nonhost resistance changes as a function of phylogenetic divergence time between host and nonhost. Similarly, changes in pathogen host range, e.g. host range expansions, appear to be driven by variation in pathogen effector repertoires, in turn leading to reproductive isolation and subsequent pathogen speciation.

Section snippets

Host range and nonhost resistance: two sides of the same coin

It is intriguing that pathogenic microbial species differ markedly in the number of plant species (the so-called ‘host range’, see Glossary) they are able to colonize in natural habitats. Although some microbes are highly specialized and can infect only a single plant species (narrow host range), others are able to either colonize a few or a considerable number of hosts, which can sometimes belong to different plant families (broad host range). Notably, microbes with either a narrow or broad

Molecular determinants of nonhost resistance in plant species that are distantly related to the natural host

Insight into the genetic and molecular determinants of host range in filamentous pathogens that prevent microbial colonization on a nonhost comes from studies on the dicotyledonous reference species, Arabidopsis thaliana (Arabidopsis) and Blumeria graminis f. sp. hordei (Bgh), an obligate biotrophic fungus that in nature colonizes monocotyledonous barley (Hordeum vulgare). The monocot–dicot split occurred approximately 200 My ago [12]. Dicotyledonous Arabidopsis is a nonhost for Bgh in nature

Molecular determinants of nonhost resistance in plant species that are closely related to the natural host

A characteristic feature of the nonhost resistance studies using Arabidopsis and Bgh was the employment of a nonhost plant species that, in phylogenetic terms, is distantly related to its natural monocot host. A different class of plant (and pathogen) genes contributing to host range restriction was identified in experiments using nonhosts that have diverged from the natural hosts relatively recently. For example, Magnaporthe oryzae, the causal agent of the blast disease on many

A unifying concept for nonhost resistance

How can the seemingly contradictory results of the above mentioned studies on nonhost resistance be synthesized into a unifying conceptual framework? We hypothesize that both NB-LRR- and PRR-triggered immunity contribute to nonhost resistance such that with increasing phylogenetic divergence time between two plant species the relative effectiveness of PRR-triggered immunity increases whereas the relative contribution of NB-LRR protein-triggered immunity decreases (Figure 1). One mechanistic

Rapidly evolving pathogen effector repertoires appear to define the pathogen host range

Although the majority of potentially pathogenic microbes can be kept in check by the two-tiered immune system outlined above, pathogenic microbes have evolved the capacity to colonize individual plant species and, as a consequence, cause disease. Accumulating evidence suggests that effector proteins, small polypeptides secreted by the microbe and operating either in the apoplast or inside the plant cell, are pivotal for microbial pathogenesis [43]. The cellular targets for fungal effectors in

A potential molecular mechanism for host range alterations

Pathogens might also evolve the capacity to colonize new host species that are either closely (host range expansions) or distantly (host jumps) related to their present hosts. A recent example of a host range expansion is the spreading of the rice blast disease to wheat in Brazil [60]. Evolutionary evidence for the occurrence of host jumps is provided by the comparative analysis of microbial and host phylogenies. While congruent phylogenies are compatible with a history of co-speciation and

Presumptive molecular mechanisms of effector repertoire diversification

Assuming that effector repertoires indeed define host range and are key determinants that allow host range expansion and host jumps, pathogen species with a large and diversified composition of effectors should have a higher chance to increase their host range. Also, the rate with which effector diversity can be generated should impact the ability to colonize new host species. There are several molecular mechanisms that likely contribute to the generation of effector diversity: (i) positive

Pathogen speciation as a consequence of host range alterations

It is conceivable that changes in host range also impact on, and possibly even represent a key event for pathogen speciation. Host range expansion and especially host jumps create potential reproductive barriers, the main driving force of speciation. Considering that host jumps are rare events, in the case of heterothallic fungi the colonization of a new host species by a representative of one mating type does not yet allow sexual reproduction on the new host species because the population

Outlook

A key feature of the nonhost resistance model we propose here is its dependence on the same three core components also operating in host immunity: PRRs, NB-LRR proteins, and effectors. Thus, we have derived a molecular framework for nonhost resistance and pathogen host range from first principles of the innate immune system. Whilst NB-LRR proteins play a dominant role in interactions with host-adapted pathogens due to successful interception of PRR-triggered immunity by effector action, the

Acknowledgements

We thank Jeff Dangl, Jane Parker and Richard O’Connell for helpful comments on the manuscript. Work in the laboratories of PSL and RP is supported by grants from the Max-Planck Society and the Deutsche Forschungsgemeinschaft (DFG, SFB670 and SPP1212).

Glossary

Accession
taxonomic classifier for host plants below the species level. Accessions refer to individuals of a plant population that were collected from specific geographic regions and often have different NB-LRR protein arsenals. Differential growth of individuals of a pathogen species then serves to define different strains/isolates/races of a given pathogen species.
Co-speciation
concerted speciation of a host and its pathogen. The reproductive isolation and subsequent speciation (sexual

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