Trends in Plant Science
OpinionA molecular evolutionary concept connecting nonhost resistance, pathogen host range, and 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
References (79)
Host-microbe interactions: shaping the evolution of the plant immune response
Cell
(2006)Nonhost resistance to Phytophthora: novel prospects for a classical problem
Curr. Opin. Plant Biol.
(2001)Linking the emergence of fungal plant diseases with ecological speciation
Trends Ecol. Evol.
(2010)Comparative sequence analysis of wheat and barley powdery mildew fungi reveals gene colinearity, dates divergence and indicates host pathogen co-evolution
Fungal Genet. Biol.
(2011)Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps
Mycol. Res.
(2008)Phylogenetic relationships of Peronospora and related genera based on nuclear ribosomal ITS sequences
Mycol. Res.
(2003)- et al.
Phylogenetic signal in plant pathogen-host range
Proc. Natl. Acad. Sci. U.S.A.
(2007) - et al.
The plant immune system
Nature
(2006) - et al.
Plant and animal sensors of conserved microbial signatures
Science
(2010) Chitin signaling and plant disease resistance
Plant Signal. Behav.
(2008)