The gene-for-gene relationship was discovered by Harold Henry Flor who was working with rust (''

Melampsora lini ''Melampsora lini'' is a species of fungus and plant pathogen found in Ireland and commonly known as flax rust. Life cycle The pathogen is an obligate biotroph meaning that each stage of its cycle is dependent on having a living host. The dir ...

'') of

flax Flax, also known as common flax or linseed, is a flowering plant, ''Linum usitatissimum'', in the family Linaceae. It is cultivated as a food and fiber crop in regions of the world with temperate climates. Textiles made from flax are known in ...

('' 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. Gene-for-gene relationships are a widespread and very important aspect of

plant disease resistance 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 pathoge ...

. Another example can be seen with ''

Lactuca serriola ''Lactuca serriola'', also called prickly lettuce, milk thistle (not to be confused with '' Silybum marianum'', also called milk thistle), compass plant, and scarole, is an annual or biennial plant in the tribe Cichorieae within the family Aster ...

'' versus ''

Bremia lactucae ''Bremia lactucae'' is a plant pathogen. This microorganism causes a disease of lettuce (''Lactuca sativa'') denominated as downy mildew. Some other strains can be found on 36 genera of Asteraceae including ''Senecio'' and ''Sonchus''. Experime ...

''. Clayton Oscar Person was the first scientist to study plant

pathosystem A pathosystem is a subsystem of an ecosystem and is defined by the phenomenon of parasitism. A plant pathosystem is one in which the host species is a plant. The parasite is any species in which the individual spends a significant part of its lifes ...

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.

Resistance genes

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 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 o ...

(PRR). The protein products of the NBS-LRR R genes contain a

nucleotide Nucleotides are organic molecules consisting of a nucleoside and a phosphate. They serve as monomeric units of the nucleic acid polymers – deoxyribonucleic acid (DNA) and ribonucleic acid (RNA), both of which are essential biomolecu ...

binding site (NBS) and a

leucine rich repeat A leucine-rich repeat (LRR) is a protein structural motif that forms an α/β horseshoe fold. It is composed of repeating 20–30 amino acid stretches that are unusually rich in the hydrophobic amino acid leucine. These tandem repeats comm ...

(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 Tobacco is the common name of several plants in the genus '' Nicotiana'' of the family Solanaceae, and the general term for any product prepared from the cured leaves of these plants. More than 70 species of tobacco are known, but the ...

against

tobacco mosaic virus ''Tobacco mosaic virus'' (TMV) is a positive-sense single-stranded RNA virus species in the genus ''Tobamovirus'' that infects a wide range of plants, especially tobacco and other members of the family Solanaceae. The infection causes characteri ...

(TMV). *The other subclass does not contain a TIR and instead has a

leucine zipper A leucine zipper (or leucine scissors) is a common three-dimensional structural motif in proteins. They were first described by Landschulz and collaborators in 1988 when they found that an enhancer binding protein had a very characteristic 30-amin ...

region at its amino terminal. The

protein Proteins are large biomolecules and macromolecules that comprise one or more long chains of amino acid residues. Proteins perform a vast array of functions within organisms, including catalysing metabolic reactions, DNA replication, res ...

products encoded by this class of resistance gene are located within the

plant cell Plant cells are the cells present in green plants, photosynthetic eukaryotes of the kingdom Plantae. Their distinctive features include primary cell walls containing cellulose, hemicelluloses and pectin, the presence of plastids with the capab ...

cytoplasm In cell biology, the cytoplasm is all of the material within a eukaryotic cell, enclosed by the cell membrane, except for the cell nucleus. The material inside the nucleus and contained within the nuclear membrane is termed the nucleoplasm. ...

. 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 Rice is the seed of the grass species '' Oryza sativa'' (Asian rice) or less commonly ''Oryza glaberrima'' (African rice). The name wild rice is usually used for species of the genera '' Zizania'' and '' Porteresia'', both wild and domesticat ...

Xa21D for resistance against ''

Xanthomonas ''Xanthomonas'' (from greek: ''xanthos'' – “yellow”; ''monas'' – “entity”) is a genus of bacteria, many of which cause plant diseases. There are at least 27 plant associated ''Xanthomonas spp.'', that all together infect at least 400 ...

'' and the ''cf'' genes of

tomato The tomato is the edible berry of the plant ''Solanum lycopersicum'', commonly known as the tomato plant. The species originated in western South America, Mexico, and Central America. The Mexican Nahuatl word gave rise to the Spanish word ...

that confer resistance against ''

Cladosporium fulvum ''Passalora fulva'' is a fungal plant pathogen Plant pathology (also phytopathology) is the scientific study of diseases in plants caused by pathogens (infectious organisms) and environmental conditions (physiological factors). Organisms ...

''. The ''

Pseudomonas ''Pseudomonas'' is a genus of Gram-negative, Gammaproteobacteria, belonging to the family Pseudomonadaceae and containing 191 described species. The members of the genus demonstrate a great deal of metabolic diversity and consequently are able t ...

'' 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 Leucine (symbol Leu or L) is an essential amino acid that is used in the biosynthesis of proteins. Leucine is an α-amino acid, meaning it contains an α- amino group (which is in the protonated −NH3+ form under biological conditions), an α- ...

rich repeats. LRRs are multiple, serial repeats of a motif of roughly 24

amino acid Amino acids are organic compounds that contain both amino and carboxylic acid functional groups. Although hundreds of amino acids exist in nature, by far the most important are the alpha-amino acids, which comprise proteins. Only 22 alpha ...

s in length, with leucines or other

hydrophobic In chemistry, hydrophobicity is the physical property of a molecule that is seemingly repelled from a mass of water (known as a hydrophobe). In contrast, hydrophiles are attracted to water. Hydrophobic molecules tend to be nonpolar and, ...

residues at regular intervals. Some may also contain regularly spaced

proline Proline (symbol Pro or P) is an organic acid classed as a proteinogenic amino acid (used in the biosynthesis of proteins), although it does not contain the amino group but is rather a secondary amine. The secondary amine nitrogen is in the p ...

s and

arginine Arginine is the amino acid with the formula (H2N)(HN)CN(H)(CH2)3CH(NH2)CO2H. The molecule features a guanidino group appended to a standard amino acid framework. At physiological pH, the carboxylic acid is deprotonated (−CO2−) and both the am ...

s. 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 In genetics, dominance is the phenomenon of one variant (allele) of a gene on a chromosome masking or overriding the effect of a different variant of the same gene on the other copy of the chromosome. The first variant is termed dominant and t ...

but there are some, most notably the '' mlo'' gene in

barley Barley (''Hordeum vulgare''), a member of the grass family, is a major cereal grain grown in temperate climates globally. It was one of the first cultivated grains, particularly in Eurasia as early as 10,000 years ago. Globally 70% of barley p ...

, in which monogenic resistance is conferred by

recessive In genetics, dominance is the phenomenon of one variant ( allele) of a gene on a chromosome masking or overriding the effect of a different variant of the same gene on the other copy of the chromosome. The first variant is termed dominant an ...

allele An allele (, ; ; modern formation from Greek ἄλλος ''állos'', "other") is a variation of the same sequence of nucleotides at the same place on a long DNA molecule, as described in leading textbooks on genetics and evolution. ::"The chrom ...

s. ''mlo'' protects barley against nearly all

pathovar A pathovar is a bacterial strain or set of strains with the same or similar characteristics, that is differentiated at infrasubspecific level from other strains of the same species or subspecies on the basis of distinctive pathogenicity to one o ...

s 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. 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 ''Arabidopsis'' (rockcress) is a genus in the family Brassicaceae. They are small flowering plants related to cabbage and mustard. This genus is of great interest since it contains thale cress (''Arabidopsis thaliana''), one of the model organ ...

'' produced cell death when combined with expression of the host R gene, '' RPM1''. This proved recognition was occurring intracellularly and not on the surface. 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 Virulence is a pathogen's or microorganism's ability to cause damage to a host. In most, especially in animal systems, virulence refers to the degree of damage caused by a microbe to its host. The pathogenicity of an organism—its ability to ...

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. AvrPto is an inhibitor of PRR kinase domains. PRRs signal plants to induce immunity when PAMPs are detected. 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. 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. 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 The innate, or nonspecific, immune system is one of the two main immunity strategies (the other being the adaptive immune system) in vertebrates. The innate immune system is an older evolutionary defense strategy, relatively speaking, and is the ...

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 signal A nuclear localization signal ''or'' sequence (NLS) is an amino acid sequence that 'tags' a protein for import into the cell nucleus by nuclear transport. Typically, this signal consists of one or more short sequences of positively charged lysines o ...

s 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 A hypothesis (plural hypotheses) is a proposed explanation for a phenomenon. For a hypothesis to be a scientific hypothesis, the scientific method requires that one can test it. Scientists generally base scientific hypotheses on previous obse ...

for the NBS-LRR class of R genes. This

model A model is an informative representation of an object, person or system. The term originally denoted the plans of a building in late 16th-century English, and derived via French and Italian ultimately from Latin ''modulus'', a measure. Models c ...

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 ''Arabidopsis thaliana'', the thale cress, mouse-ear cress or arabidopsis, is a small flowering plant native to Eurasia and Africa. ''A. thaliana'' is considered a weed; it is found along the shoulders of roads and in disturbed land. A winter ...

'' is able to respond to two completely unrelated avirulence factors from ''

Pseudomonas syringae ''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 inte ...

''. 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.

References

{{DEFAULTSORT:Gene-For-Gene Relationship Phytopathology Agronomy