Gene-for-gene relationship

Last updated

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]

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. [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

Related Research Articles

<i>Arabidopsis thaliana</i> Model plant species in the family Brassicaceae

Arabidopsis thaliana, the thale cress, mouse-ear cress or arabidopsis, is a small plant from the mustard family (Brassicaceae), native to Eurasia and Africa. Commonly found along the shoulders of roads and in disturbed land, it is generally considered a weed.

Pattern recognition receptors (PRRs) play a crucial role in the proper function of the innate immune system. PRRs are germline-encoded host sensors, which detect molecules typical for the pathogens. They are proteins expressed mainly by cells of the innate immune system, such as dendritic cells, macrophages, monocytes, neutrophils, as well as by epithelial cells, to identify two classes of molecules: pathogen-associated molecular patterns (PAMPs), which are associated with microbial pathogens, and damage-associated molecular patterns (DAMPs), which are associated with components of host's cells that are released during cell damage or death. They are also called primitive pattern recognition receptors because they evolved before other parts of the immune system, particularly before adaptive immunity. PRRs also mediate the initiation of antigen-specific adaptive immune response and release of inflammatory cytokines.

<span class="mw-page-title-main">Innate immune system</span> One of the two main immunity strategies

The innate, or nonspecific, immune system is one of the two main immunity strategies in vertebrates. The innate immune system is an alternate defense strategy and is the dominant immune system response found in plants, fungi, insects, and primitive multicellular organisms.

Systemic acquired resistance (SAR) is a "whole-plant" resistance response that occurs following an earlier localized exposure to a pathogen. SAR is analogous to the innate immune system found in animals, and although there are many shared aspects between the two systems, it is thought to be a result of convergent evolution. The systemic acquired resistance response is dependent on the plant hormone, salicylic acid.

<span class="mw-page-title-main">Hypersensitive response</span>

Hypersensitive response (HR) is a mechanism used by plants to prevent the spread of infection by microbial pathogens. HR is characterized by the rapid death of cells in the local region surrounding an infection and it serves to restrict the growth and spread of pathogens to other parts of the plant. It is analogous to the innate immune system found in animals, and commonly precedes a slower systemic response, which ultimately leads to systemic acquired resistance (SAR). HR can be observed in the vast majority of plant species and is induced by a wide range of plant pathogens such as oomycetes, viruses, fungi and even insects.

Leptosphaeria maculans is a fungal pathogen of the phylum Ascomycota that is the causal agent of blackleg disease on Brassica crops. Its genome has been sequenced, and L. maculans is a well-studied model phytopathogenic fungus. Symptoms of blackleg generally include basal stem cankers, small grey lesions on leaves, and root rot. The major yield loss is due to stem canker. The fungus is dispersed by the wind as ascospores or rain splash in the case of the conidia. L. maculans grows best in wet conditions and a temperature range of 5–20 degrees Celsius. Rotation of crops, removal of stubble, application of fungicide, and crop resistance are all used to manage blackleg. The fungus is an important pathogen of Brassica napus (canola) crops.

<i>Pseudomonas syringae</i> Species of bacterium

Pseudomonas syringae is a rod-shaped, Gram-negative bacterium with polar flagella. As a plant pathogen, it can infect a wide range of species, and exists as over 50 different pathovars, all of which are available to researchers from international culture collections such as the NCPPB, ICMP, and others.

<span class="mw-page-title-main">NOD-like receptor</span> Class of proteins

The nucleotide-binding oligomerization domain-like receptors, or NOD-like receptors (NLRs), are intracellular sensors of pathogen-associated molecular patterns (PAMPs) that enter the cell via phagocytosis or pores, and damage-associated molecular patterns (DAMPs) that are associated with cell stress. They are types of pattern recognition receptors (PRRs), and play key roles in the regulation of innate immune response. NLRs can cooperate with toll-like receptors (TLRs) and regulate inflammatory and apoptotic response.

Resistance genes (R-Genes) are genes in plant genomes that convey plant disease resistance against pathogens by producing R proteins. The main class of R-genes consist of a nucleotide binding domain (NB) and a leucine rich repeat (LRR) domain(s) and are often referred to as (NB-LRR) R-genes or NLRs. Generally, the NB domain binds either ATP/ADP or GTP/GDP. The LRR domain is often involved in protein-protein interactions as well as ligand binding. NB-LRR R-genes can be further subdivided into toll interleukin 1 receptor (TIR-NB-LRR) and coiled-coil (CC-NB-LRR).

<span class="mw-page-title-main">Plant disease resistance</span> Ability of a plant to stand up to trouble

Plant disease resistance protects plants from pathogens in two ways: by pre-formed structures and chemicals, and by infection-induced responses of the immune system. Relative to a susceptible plant, disease resistance is the reduction of pathogen growth on or in the plant, while the term disease tolerance describes plants that exhibit little disease damage despite substantial pathogen levels. Disease outcome is determined by the three-way interaction of the pathogen, the plant and the environmental conditions.

BRI1-associated receptor kinase 1 is an important plant protein that has diverse functions in plant development.

<span class="mw-page-title-main">Effector-triggered immunity</span>

Effector-triggered immunity (ETI) is one of the pathways, along with the pattern-triggered immunity (PTI) pathway, by which the innate immune system recognises pathogenic organisms and elicits a protective immune response. ETI is elicited when an effector protein secreted by a pathogen into the host cell is successfully recognised by the host. Alternatively, effector-triggered susceptibility (ETS) can occur if an effector protein can block the immune response triggered by pattern recognition receptors (PRR) and evade immunity, allowing the pathogen to propagate in the host.

Guard theory is a branch of immunology which concerns the innate sensing of stereotypical consequences of a virulence factor or pathogen. This is in contrast to the classical understanding of recognition by the innate immune system, which involves recognition of distinct microbial structures- pathogen-associated molecular patterns (PAMPs)- with pattern recognition receptors (PRRs). Some of these stereotypical consequences of virulence factors and pathogens may include altered endosomal trafficking and changes in the cytoskeleton. These recognition mechanisms would work to complement classical pattern recognition mechanisms.

<span class="mw-page-title-main">Bacterial blight of soybean</span> Bacterial plant disease

Bacterial blight of soybean is a widespread disease of soybeans caused by Pseudomonas syringaepv. glycinea.

Mitogen-activated protein kinase (MAPK) networks are the pathways and signaling of MAPK, which is a protein kinase that consists of amino acids serine and threonine. MAPK pathways have both a positive and negative regulation in plants. A positive regulation of MAPK networks is to help in assisting with stresses from the environment. A negative regulation of MAPK networks is pertaining to a high quantity of reactive oxygen species (ROS) in the plant.

<span class="mw-page-title-main">Leucine-rich repeat receptor like protein kinase</span>

Leucine-rich repeat receptor like protein kinase are plant cell membrane localized Leucine-rich repeat (LRR) receptor kinase that play critical roles in plant innate immunity. Plants have evolved intricate immunity mechanism to combat against pathogen infection by recognizing Pathogen Associated Molecular Patterns (PAMP) and endogenous Damage Associated Molecular Patterns (DAMP). PEPR 1 considered as the first known DAMP receptor of Arabidopsis.

PEPR 1 and PEPR2 are homolog kinases that act as enzymes on other proteins. They attach a phosphate group to specific proteins, called phosphorylation. These reactions can cause the function of the phosphorylated proteins to change. Both PEPR 1 and PEPR 2 can be classified as receptor kinases, which serve an important role in immunity in plants. Receptor kinases have the ability to change the conformation of receptors by adding the phosphate group. These specific receptor kinases serve as a pattern recognition receptor, or PRR, that can quickly and efficiently recognize many different molecular patterns or signatures that are unique to each pathogen. They can also detect different danger signals released from the host and respond accordingly. More specifically, the proteins contain leucine-rich repeat segments that interact outside of the cell. This leucine-rich repeat is a structural motif present in some proteins that has specific functions due to its folded structure. This fold can contain many repeating amino acids, but the most common is the hydrophobic leucine, hence the name. PEPR1 and PEPR2 are present in plants and are involved in several immune system processes. Their ability to change the conformation of receptors can have an effect on signaling processes within plants, allowing the plant to have a system of immunity in place in case of an infection or pathogen.

<span class="mw-page-title-main">Gene-for-gene interactions in rust fungi</span>

The study of gene-for-gene interactions uncovers genetic components, evolutionary impacts, and ecological/economic implications between rust fungi and plants. Rust fungi utilize the gene-for-gene interaction to invade host plants. Conversely, host plants utilize the gene-for-gene interaction to prevent invasion of rust fungi.

Brian John Staskawicz ForMemRS is professor of plant and microbial miology at the University of California, Berkeley and scientific director of agricultural genomics at the Innovative Genomics Institute (IGI).

AvrPphB SUSCEPTIBLE 1/PBS1 is a protein kinase acting upon serine and threonine. It is a Receptor-Like Cytoplasmic Kinase, of Subfamily VII. It is the guardee of RESISTANCE TO PSEUDOMONAS SYRINGAE 5/RPS5. PBS1 is cleaved by an effector, AvrPphB, used by Pseudomonas syringae pv. phaseolicola, serving as an immunological decoy to signal RPS5 that an attack is underway as reviewed by Kourelis et al. 2016.

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.
  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. Annual Reviews. 54 (1): 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.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.