The gene-for-gene relationship was discovered by the late Harold Henry Flor who was working with rust (Melampsora lini) of flax (Linum usitatissimum). Flor was the first scientist to study the genetics of both the host and parasite and to integrate them into one genetic system. Gene-for-gene relationships are a widespread and very important aspect of plant disease resistance.
Flor showed that the inheritance of both resistance in the host and parasite ability to cause disease is controlled by pairs of matching genes. One is a plant gene called the resistance (R) gene. The other is a parasite gene called the avirulence (Avr) gene. Plants producing a specific R gene product are resistant towards a pathogen that produces the corresponding Avr gene product.
Clayton Oscar Person was the first scientist to study plant pathosystem ratios rather than genetics ratios in host-parasite systems. In doing so, he discovered the differential interaction that is common to all gene-for-gene relationships and that is now known as the Person differential interaction.
Classes of resistance gene
There are several different classes of R Genes. The major classes are the NBS-LRR genes and the cell surface pattern recognition receptors (PRR). The protein products of the NBS-LRR R genes contain a nucleotide binding site (NBS) and a leucine rich repeat (LRR). The protein products of the PRRs contain extracellular, juxtamembrane, transmembrane and intracellular non-RD kinase domains.
Within the NBS-LRR class of R genes are two subclasses: -
- One subclass has an amino-terminal Toll/Interleukin 1 receptor homology region (TIR). This includes the N resistance gene of tobacco against tobacco mosaic virus (TMV).
- The other subclass does not contain a TIR and instead has a leucine zipper region at its amino terminal.
The PRR class of R genes includes the rice XA21 resistance gene that recognizes the ax21 peptide  and the Arabidopsis FLS2 peptide that recognizes the flg22 peptide from flagellin.
There are other classes of R genes, such as the extracellular LRR class of R genes; examples include rice Xa21D  for resistance against Xanthomonas and the cf genes of tomato that confer resistance against Cladosporium fulvum.
The Pseudomonas tomato resistance gene (Pto) belongs to a class of its own. It encodes a Ser/Thr kinase but has no LRR. It requires the presence of a linked NBS-LRR gene, prf, for activity.
Specificity of resistance genes
R gene specificity (recognising certain Avr gene products) is believed to be conferred by the leucine rich repeats. LRRs are multiple, serial repeats of a motif of roughly 24 amino acids in length, with leucines or other hydrophobic residues at regular intervals. Some may also contain regularly spaced prolines and arginines.
LRRs are involved in protein-protein interactions, and the greatest variation amongst resistance genes occurs in the LRR domain. LRR swapping experiments between resistance genes in flax rust resulted in the specificity of the resistance gene for the avirulence gene changing.
Recessive resistance genes
Most resistance genes are autosomal dominant but there are some, most notably the mlo gene in barley, in which monogenic resistance is conferred by recessive alleles. mlo protects barley against nearly all pathovars of powdery mildew.
The term “avirulence gene” remains useful as a broad term that indicates a gene that encodes any determinant of the specificity of the interaction with the host. Thus, this term can encompass some conserved microbial signatures (also called pathogen or microbe associated molecular patterns (PAMPs or MAMPs)) and pathogen effectors (e.g. bacterial type III effectors and oomycete effectors) as well as any genes that control variation in the activity of those molecules.
There is no common structure between avirulence gene products. Because there would be no evolutionary advantage to a pathogen keeping a protein that only serves to have it recognised by the plant, it is believed that the products of Avr genes play an important role in virulence in genetically susceptible hosts.
Unlike the MAMP or PAMP class of avr genes that are recognized by the host PRRs, the targets of bacterial effector avr proteins appear to be proteins involved in plant innate immunity signaling, as homologues of Avr genes in animal pathogens have been shown to do this. For example, the AvrBs3 family of proteins possess DNA binding domains, nuclear localisation signals and acidic activation domains and are believed to function by altering host cell transcription.
The guard hypothesis
In only some cases is there direct interaction between the R gene product and the Avr gene product. For example, both FLS2 and XA21 interact with the microbial peptides. In contrast, for the NBS-LRR class of R genes, direct interaction has not been shown for most of the R/avr pairs. This lack of evidence for a direct interaction led to the formation of the guard hypothesis for the NBS-LRR class of R genes.
This model proposes that the R proteins interact, or guard, a protein known as the guardee which is the target of the Avr protein. When it detects interference with the guardee protein, it activates resistance.
Several experiments support this hypothesis, e.g. the Rpm1 gene in Arabidopsis thaliana is able to respond to two completely unrelated avirulence factors from P. syringae. The guardee protein is RIN4, which is hyperphosphorylated by the Avr proteins. Another high profile study that supports the guard hypothesis shows that the RPS5 pair uses PBS1, a protein kinase as a guardee against AvrPphB.
Yeast two-hybrid studies of the tomato Pto/Prf/AvrPto interaction showed that the Avirulence protein, AvrPto, interacted directly with Pto despite Pto not having an LRR. This makes Pto the guardee protein, which is protected by the NBS-LRR protein Prf. However, Pto is a resistance gene alone, which is an argument against the guard hypothesis.
- Flor H.H. (1942). "Inheritance of pathogenicity in Melampsora lini". Phytopath 32: 653–669.
- Flor H.H. (1947). "Inheritance of reaction to rust in flax". J. Agric. Res. 74: 241–262.
- Flor H.H. (1955). "Host-parasite interaction in flax rust - its genetics and other implications". Phytopathology 45: 680–685.
- Flor H.H. (1971). "Current status of the gene-for-gene concept". Annu Rev Phytopathol 9: 275–296. doi:10.1146/annurev.py.09.090171.001423.
- Robinson, Raoul A. (1987) Host Management in Crop Pathosystems, Macmillan Publishing Company
- Person C.O. (1959). "Gene-for-gene relationships in parasitic systems". Can. J. Bot. 37: 1101–1130. doi:10.1139/b59-087.
- McHale L, Tan X, Koehl P, Michelmore RW (2006). "Plant NBS-LRR proteins: adaptable guards.". Genome Biol 7 (4): 212. doi:10.1186/gb-2006-7-4-212. PMC 1557992. PMID 16677430.
- Song W-Y Wang G-L, Zhu L-H Fauquet C, Ronald P (1995). "A receptor kinase-like protein encoded by the rice disease resistance gene Xa21". Science 270 (5243): 1804–1806. doi:10.1126/science.270.5243.1804. PMID 8525370.
- Dardick C, Ronald P (January 2006). "Plant and animal pathogen recognition receptors signal through non-RD kinases". PLoS Pathog. 2 (1): e2. doi:10.1371/journal.ppat.0020002. PMC 1331981. PMID 16424920.
- Sang-Won Lee, Sang-Wook Han, Malinee Sririyanum, Chang-Jin Park, Young-Su Seo, Pamela C. Ronald (6 November 2009). "A Type I–Secreted, Sulfated Peptide Triggers XA21-Mediated Innate Immunity.". Science 326 (5954): 850–853. doi:10.1126/science.1173438. PMID 19892983.
- Wang GL, Ruan DL, Song WY, Sideris S, Chen L, Pi LY, Zhang S, Zhang Z, Fauquet C; et al. (1998). "The rice disease resistance gene, Xa21D, encodes a receptor-like molecule with a LRR domain that determines race specific recognition and is subject to adaptive evolution". Plant Cell 10 (5): 765–779. doi:10.2307/3870663. PMC 144027. PMID 9596635.
- Zhang L, Meakin H, Dickinson M (November 2003). "Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP". Mol. Plant Pathol. 4 (6): 469–77. doi:10.1046/j.1364-3703.2003.00192.x. PMID 20569406.
- DeYoung BJ, Innes RW (December 2006). "Plant NBS-LRR proteins in pathogen sensing and host defense". Nat. Immunol. 7 (12): 1243–9. doi:10.1038/ni1410. PMC 1973153. PMID 17110940.
- Lahaye T, Bonas U (October 2001). "Molecular secrets of bacterial type III effector proteins". Trends Plant Sci. 6 (10): 479–85. doi:10.1016/S1360-1385(01)02083-0. PMID 11590067.
- Van Der Biezen, E.; Jones, J. D. G. (1998). "Plant disease-resistance proteins and the gene-for-gene concept". Trends in Biochemical Sciences 23 (12): 454–451. doi:10.1016/S0968-0004(98)01311-5. PMID 9868361
- Shao, F; Golstein, Ade,Stoutemyer, Dixon, Innes (2003-08-29). "Cleavage of Arabidopsis PBS1 by a bacterial type III effector.". Science 301 (5637): 1230–3. doi:10.1126/science.1085671. PMID 12947197.