Gene-for-gene relationship

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The gene-for-gene relationship is a concept in plant pathology that plants and their diseases each have single genes that interact with each other during an infection. It was proposed by Harold Henry Flor [1] [2] [3] [4] who was working with rust ( Melampsora lini ) of flax ( Linum usitatissimum ). 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. [5] Gene-for-gene relationships are a widespread and very important aspect of plant disease resistance. Another example can be seen with Lactuca serriola versus Bremia lactucae .

Contents

Clayton Oscar Person [6] 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. [5]

Resistance genes

Classes of resistance gene

There are several different classes of R genes. The major classes are the NBS-LRR genes [7] and the cell surface pattern recognition receptors (PRR). [8] 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. [8] [9]

Within the NBS-LRR class of R genes are two subclasses: [7]

The protein products encoded by this class of resistance gene are located within the plant cell cytoplasm.

The PRR class of R genes includes the rice XA21 resistance gene that recognizes the ax21 peptide [10] [11] 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 [12] 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. [13]

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. [14]

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.

Avirulence genes

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. [10]

Intracellular recognition of an avirulence gene product was first demonstrated by Gopalan et al 1996. They found that artificial expression of Pseudomonas syringae's avrB in the host Arabidopsis produced cell death when combined with expression of the host R gene, RPM1 . This proved recognition was occurring intracellularly and not on the surface. [15]

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.

Example: AvrPto is a small triple-helix protein that, like several other effectors, is targeted to the plasma membrane by N-myristoylation. [16] AvrPto is an inhibitor of PRR kinase domains. PRRs signal plants to induce immunity when PAMPs are detected. [17] [18] The ability to target receptor kinases is required for the virulence function of AvrPto in plants. However, Pto is a resistant gene that can detect AvrPto and induce immunity as well. [19] AvrPto is an ancient effector that is conserved in many P. syringae strains, whereas Pto R gene is only found in a few wild tomato species. [18] This suggests recent evolution of the Pto R gene and the pressure to evolve to target AvrPto, turning a virulence effector to an avirulence effector.

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. [20]

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. [21]

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 Pseudomonas 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. [22]

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. [23]

See also

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References

  1. Flor HH (1942). "Inheritance of pathogenicity in Melampsora lini". Phytopath. 32: 653–669.
  2. Flor HH (1947). "Inheritance of reaction to rust in flax". J. Agric. Res. 74: 241–262.
  3. Flor HH (1955). "Host-parasite interaction in flax rust - its genetics and other implications". Phytopathology. 45: 680–685.
  4. Flor HH (1971). "Current status of the gene-for-gene concept". Annu Rev Phytopathol. 9: 275–296. doi:10.1146/annurev.py.09.090171.001423.
  5. 1 2 Robinson RA (1987). Host Management in Crop Pathosystems. Macmillan Publishing Company.
  6. Person CO (1959). "Gene-for-gene relationships in parasitic systems". Can. J. Bot. 37 (5): 1101–1130. doi:10.1139/b59-087.
  7. 1 2 McHale L, Tan X, Koehl P, Michelmore RW (2006). "Plant NBS-LRR proteins: adaptable guards". Genome Biology. 7 (4): 212. doi: 10.1186/gb-2006-7-4-212 . PMC   1557992 . PMID   16677430.
  8. 1 2 Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, et al. (December 1995). "A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21". Science. 270 (5243): 1804–1806. Bibcode:1995Sci...270.1804S. doi:10.1126/science.270.5243.1804. PMID   8525370. S2CID   10548988.
  9. Dardick C, Ronald P (January 2006). "Plant and animal pathogen recognition receptors signal through non-RD kinases". PLOS Pathogens. 2 (1): e2. doi: 10.1371/journal.ppat.0020002 . PMC   1331981 . PMID   16424920.
  10. 1 2 Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC (November 2009). "A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity". Science. 326 (5954): 850–853. Bibcode:2009Sci...326..850L. doi:10.1126/science.1173438. PMID   19892983. S2CID   8726419. (Retracted, see doi:10.1126/science.342.6155.191-a, PMID   24115421,  Retraction Watch . If this is an intentional citation to a retracted paper, please replace {{ retracted |...}} with {{ retracted |...|intentional=yes}}.)
  11. Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, et al. (July 2015). "The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium". Science Advances. 1 (6): e1500245. Bibcode:2015SciA....1E0245P. doi:10.1126/sciadv.1500245. PMC   4646787 . PMID   26601222.
  12. Wang GL, Ruan DL, Song WY, Sideris S, Chen L, Pi LY, et al. (May 1998). "Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution". The Plant Cell. 10 (5): 765–779. doi:10.2307/3870663. JSTOR   3870663. PMC   144027 . PMID   9596635.
  13. 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". Molecular Plant Pathology. 4 (6): 469–477. doi: 10.1046/j.1364-3703.2003.00192.x . PMID   20569406.
  14. DeYoung BJ, Innes RW (December 2006). "Plant NBS-LRR proteins in pathogen sensing and host defense". Nature Immunology. 7 (12): 1243–1249. doi:10.1038/ni1410. PMC   1973153 . PMID   17110940.
  15. Whitham SA, Qi M, Innes RW, Ma W, Lopes-Caitar V, Hewezi T (August 2016). "Molecular Soybean-Pathogen Interactions". Annual Review of Phytopathology. 54 (1). Annual Reviews: 443–468. doi:10.1146/annurev-phyto-080615-100156. PMID   27359370.
  16. Wulf J, Pascuzzi PE, Fahmy A, Martin GB, Nicholson LK (July 2004). "The solution structure of type III effector protein AvrPto reveals conformational and dynamic features important for plant pathogenesis". Structure. 12 (7): 1257–1268. doi: 10.1016/j.str.2004.04.017 . PMID   15242602.
  17. Xin XF, He SY (2013). "Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants". Annual Review of Phytopathology. 51: 473–98. doi:10.1146/annurev-phyto-082712-102321. PMID   23725467.
  18. 1 2 Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, et al. (January 2008). "Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases". Current Biology. 18 (1): 74–80. doi: 10.1016/j.cub.2007.12.020 . PMID   18158241.
  19. Deslandes L, Rivas S (November 2012). "Catch me if you can: bacterial effectors and plant targets". Trends in Plant Science. 17 (11): 644–655. doi:10.1016/j.tplants.2012.06.011. PMID   22796464.
  20. Lahaye T, Bonas U (October 2001). "Molecular secrets of bacterial type III effector proteins". Trends in Plant Science. 6 (10): 479–485. doi:10.1016/S1360-1385(01)02083-0. PMID   11590067.
  21. Van der Biezen EA, Jones JD (December 1998). "Plant disease-resistance proteins and the gene-for-gene concept". Trends in Biochemical Sciences. 23 (12): 454–456. doi:10.1016/S0968-0004(98)01311-5. PMID   9868361.
  22. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (August 2003). "Cleavage of Arabidopsis PBS1 by a bacterial type III effector". Science. 301 (5637): 1230–1233. Bibcode:2003Sci...301.1230S. doi:10.1126/science.1085671. PMID   12947197. S2CID   6418384.
  23. Grzeskowiak L, Stephan W, Rose LE (October 2014). "Epistatic selection and coadaptation in the Prf resistance complex of wild tomato". Infection, Genetics and Evolution. 27: 456–471. doi:10.1016/j.meegid.2014.06.019. hdl: 10449/23790 . PMID   24997333.