Table 1.
Components of the phenotype of RLP-mediated resistance operating in leaves of arable and/or horticultural crops against hemibiotrophic fungal pathogens that colonise an apoplastic niche
| Pathogen (hemibiotrophic)a | Nicheb | Hostc | R gened | Phenotype |
Refs | ||||
|---|---|---|---|---|---|---|---|---|---|
| Host cell deathe (dpi) | Pathogen death | Limits pathogen biomassf | Limits asexual sporulationg | Prevents sexual sporulationh | |||||
|
Pyrenopeziza brassicaei |
Subcuticular |
Brassica napus |
PBR1, PBR2 |
CD (<14) |
No |
Yes |
Yes |
No |
[8] |
|
Venturia inaequalisj |
Subcuticular |
Malus domestica |
HcrVf2 |
CD (2-11) |
No |
Yes |
Yes |
n/k |
[42,53,70] |
|
Rhynchosporium communek |
Subcuticular |
Hordeum vulgare |
Rrs1 |
CD (<21) |
No |
Yes |
Yes |
n/k |
[11,37,55,71] |
|
Cladosporium fulvuml |
Intercellular (mesophyll) |
Solanum lycopersicum |
Cf-2,4,4E,9 |
CD (<4) |
No |
Yes |
Yes |
n/k |
[72,73] |
|
Leptosphaeria. maculansm |
Intercellular (mesophyll) |
B. napus |
Rlm6, LepR3 |
CD (<7) |
No |
Yes |
Yes |
Yes |
[32,43] |
| Zymoseptoria triticin | Intercellular (mesophyll) | Triticum aestivum | STB genes? | No | No | Yes | Yes | No | [74] |
These hemibiotrophic pathogens are in order with most ‘biotrophic’ first and most ‘necrotropic’ last. This ranking may be somewhat subjective but P. brassicae is the most ‘biotrophic’ because its pathogenicity cannot be maintained in artificial culture.
The niche occupied by these hemibiotrophic pathogens after initial infection of leaf tissues at the time when the R gene is operating during the endophytic growth phase; frequently, these pathogens later switch to a necrotrophic phase and occupy niches in other plant tissues.
Host for which the phenotype of R gene action was studied; sometimes, the pathogen also attacks closely related hosts.
Specific R gene(s) that has been studied. Cloned RLP genes are in bold; these all encode RLPs. Mapped R genes with a described phenotype are underlined. It is assumed that the less well-characterised R genes also encode RLPs.
The mode of host cell death is not well characterised and is simply referred to as cell death (CD).
Evidence obtained by microscopy, ELISA, or quantitative PCR that the pathogen grows less extensively in host plants with the R gene than in those without it.
Evidence of no or limited asexual sporulation associated with colonisation by the pathogen.
Evidence of sexual sporulation associated with subsequent colonisation of senescent leaf tissue by the pathogen.
Occupies a subcuticular niche. It is suggested that there are two resistance loci. One locus (PBR2) on chromosome A1 is associated with necrotic flecking and a limitation of asexual sporulation; subsequent sexual sporulation is not affected.
Spores form germ tubes that penetrate the cuticle and proliferate into subcuticular stromata. Host damage does not occur until onset of asexual sporulation. Speed of the resistance response depends on the R gene. HcrVf2 triggers cell death. The effect of R gene-mediated resistance on sexual reproduction is not known (n/k).
The Rrs1 gene has not been cloned but it interacts genetically with the nip1 gene encoding a Cys-rich secreted peptide. Collapse of single or a few epidermal cells was reported to occur in both resistant and susceptible plants but then to continue only in susceptible plants. Asexual conidia are produced on resistant hosts, although less extensively than on susceptible hosts. Given that the teleomorph has not yet been found, it is not possible to assess an effect on sexual sporulation, even though population studies suggest that sexual reproduction and different mating types occur on the same leaf.
After entry through stomata, hyphae are arrested in the substomatal cavity after contact with mesophyll cells. Mesophyll cells in close proximity to hyphae undergo CD, which is controlled by Cf genes. The pathogen does not necessarily die and can sporulate in genotypes carrying Cf-1 or Cf-3 genes. Although different mating types exist, the sexual stage has not been identified.
The pathogen penetrates through stomata and then grows in intercellular spaces. In the resistant host, CD around the site of penetration is associated with containment of the pathogen. In the susceptible host, there is extensive CD, lesion formation, and production of asexual spores in pycnidia, followed by spread of the pathogen along the leaf petiole to the stem, where sexual sporulation occurs. The R gene LepR3 has recently been cloned.
STB genes are not associated with host cell death, but do reduce pathogen biomass and asexual sporulation without preventing sexual sporulation.