Table 2.
Components of the phenotype of nucleotide binding site (NBS) leucine-rich repeat (LRR) receptor (NLR)-mediated resistance or susceptibility operating in leaves of arable and horticultural crops against obligate biotrophic, hemibiotrophic or necrotrophic fungal or oomycete pathogens that colonise an intracellular niche
| Pathogen (obligate biotrophic; hemibiotrophic; or necrotrophic)a | Fungus (F) or oomycete (O) | Nicheb | Hostc | NLR gened | Phenotype |
Refs | ||||
|---|---|---|---|---|---|---|---|---|---|---|
| Host cell deathe (dpi) | Pathogen death | Limits pathogen biomassf | Limits asexual sporulation | Limits sexual sporulation | ||||||
| Blumeria graminis (b)g | F | Intracellular (epidermal) | Hordeum vulgare | Mla genes | HR (<1) | Yes | n/ah | n/a | n/a | [61] |
| Bremia lactucae (b)i | O | Intracellular (epidermal) | Lactuca serriola | Dm3 | HR (<1) | Yes | n/a | n/a | n/a | [63] |
| Puccinia striiformis (b)j | F | Intracellular (mesophyll) | Triticum aestivum | Yr1 | HR (<1) | Yes | n/a | n/a | n/a | [62] |
| Phytophthora infestans (h)k | O | Intracellular (epidermal) | Solanum tuberosum | R1, R3b | HR (1-2) | Yes | n/a | n/a | n/a | [65] |
| Magnaporthe grisea (h)l | F | Intracellular (epidermal) | Oryza sativa | Pi-ta | HR (<2) | Yes | n/a | n/a | n/a | [64] |
| Phaeosphaeria nodorum (n)m | F | Dying host cell (epidermal) | Triticum aestivum | Tsn1, Snn1-4 | PCD (<2) | No | No | No | No | [25] |
| Cochliobolus victoriae (n)n | F | Dying host cell (epidermal) | Avena sativa | Vb | PCD (<1) | No | No | No | n/k | [39–41] |
Pathogens are categorised as obligate biotrophic (b), hemibiotrophic (h), or necrotropic (n).
The niche occupied by biotrophic, hemibiotrophic or necrotrophic pathogens after initial infection of leaf tissues at the time when the NLR gene is operating; frequently, hemibiotrophic pathogens subsequently switch from a biotrophic to a necrotrophic mode and may then occupy niches in other plant tissues.
Host for which the phenotype of the NLR gene action was studied; sometimes, the pathogen also attacks other related hosts.
NLR genes confer resistance against biotrophic and hemibiotrophic pathogens, but they can be hijacked by host-selective toxins from necrotrophic fungi. This list of NLR gene(s) is not exhaustive.
The mode of host cell death can be clearly defined in the case of the hypersensitive response (HR). DNA laddering and heterochromatin condensation are used as evidence for programmed cell death (PCD).
The presence of an NLR gene promotes more extensive growth and sporulation of the necrotrophic pathogens that produce the corresponding host-selective toxin.
Colonisation of epidermal cells by means of haustoria. Mla genes are associated with a rapid HR.
Not applicable (n/a) for obligate biotrophic pathogens because the HR generally causes pathogen death; it is not possible to assess these aspects of the phenotype of resistance.
Penetration of epidermal cells leads to primary vesicle formation, which is impeded by Dm genes and associated with an HR.
Colonisation of mesophyll cells by means of haustoria. Yr1 is associated with a rapid HR.
Occupies epidermal niche after penetration; the HR impairs the pathogen.
The Pi-ta gene triggers an HR that results in death of the pathogen.
As the Tox1 protein is recognised by Ssn1, the pathogen penetrates the epidermis in the presence of light and causes PCD. ToxA is constitutively expressed and the effector is recognised by Tsn1, which contains NBS-LRR domains characteristic of cytosolic NLRs.
Germinating spores produce victorin before penetration of susceptible oats expressing the Vb gene. Although Vb has not yet been cloned, LOV1, which confers victorin susceptibility in Arabidopsis thaliana, contains an NBS-LRR domain. Vb may well be identical to Pc-2, which confers resistance to the biotrophic rust fungus Puccinia coronata. Cochliobolus victoriae has mating type genes but to our knowledge the sexual stage has not been discovered. PCD in response to victorin has also recently been referred to as victorin-induced cell death (VICD).