Gene-for-gene relationship
Encyclopedia
The gene-for-gene relationship was discovered by 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.
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: -
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 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.
rich repeats. LRRs are multiple, serial repeats of a motif of roughly 24 amino acid
s in length, with leucines or other hydrophobic residues at regular intervals. Some may also contain regularly spaced proline
s and arginine
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.
gene in barley
, in which monogenic resistance is conferred by recessive
allele
s. mlo protects barley against nearly all pathovars of powdery mildew.
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.
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.
Flax
Flax is a member of the genus Linum in the family Linaceae. It is native to the region extending from the eastern Mediterranean to India and was probably first domesticated in the Fertile Crescent...
(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
Plant disease resistance
Plant disease resistance is crucial to the reliable production of food, and it provides significant reductions in agricultural use of fuel, land, water and other inputs. There are numerous examples of devastating plant disease impacts , as well as recurrent severe plant disease issues...
.
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
Clayton Oscar Person
Clayton Oscar Person, CM, FRSC was recognized internationally as an authority on the genetics of host-parasite relations . He was born and raised in Aylesbury, Saskatchewan, Canada and died in Vancouver, British Columbia, Canada...
was the first scientist to study plant pathosystem
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 lifespan inhabiting one host individual and obtaining...
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 nucleotideNucleotide
Nucleotides are molecules that, when joined together, make up the structural units of RNA and DNA. In addition, nucleotides participate in cellular signaling , and are incorporated into important cofactors of enzymatic reactions...
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 tobaccoTobaccoTobacco is an agricultural product processed from the leaves of plants in the genus Nicotiana. It can be consumed, used as a pesticide and, in the form of nicotine tartrate, used in some medicines...
against TMVTMVTMV is a three-letter acronym which may stand for:*Tobacco mosaic virus*The Mars Volta*Trondhjems mekaniske Værksted*True market value*Thermostatic Mixing Valve*Traction Motor Vehicle...
.
- The other subclass does not contain a TIRTIRTir, tir or TIR may mean:* The French term for Schützenfest, a target-shooting competition* Tir , the fourth month in the Iranian calendar* Occasional spelling of the Old Norse theonym Tyr...
and instead has a leucine zipperLeucine zipperA leucine zipper, aka leucine scissors, is a common three-dimensional structural motif in proteins. These motifs are usually found as part of a DNA-binding domain in various transcription factors, and are therefore involved in regulating gene expression...
region at its amino terminal.
The protein
Protein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...
products encoded by this class of resistance gene are located within the plant cell
Plant cell
Plant cells are eukaryotic cells that differ in several key respects from the cells of other eukaryotic organisms. Their distinctive features include:...
cytoplasm
Cytoplasm
The cytoplasm is a small gel-like substance residing between the cell membrane holding all the cell's internal sub-structures , except for the nucleus. All the contents of the cells of prokaryote organisms are contained within the cytoplasm...
.
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
Rice is the seed of the monocot plants Oryza sativa or Oryza glaberrima . As a cereal grain, it is the most important staple food for a large part of the world's human population, especially in East Asia, Southeast Asia, South Asia, the Middle East, and the West Indies...
Xa21D for resistance against Xanthomonas
Xanthomonas
Xanthomonas is a genus of Proteobacteria, many of which cause plant diseases. Most varieties of Xanthomonas are available from the National Collection of Plant Pathogenic Bacteria in the United Kingdom and other international culture collections such as ICMP in New Zealand, CFBP in France, and...
and the cf genes of tomato
Tomato
The word "tomato" may refer to the plant or the edible, typically red, fruit which it bears. Originating in South America, the tomato was spread around the world following the Spanish colonization of the Americas, and its many varieties are now widely grown, often in greenhouses in cooler...
that confer resistance against Cladosporium fulvum
Cladosporium
Cladosporium is a genus of fungi including some of the most common indoor and outdoor molds. Species produce olive-green to brown or black colonies, and have dark-pigmented conidia that are formed in simple or branching chains....
.
The Pseudomonas
Pseudomonas
Pseudomonas is a genus of gammaproteobacteria, belonging to the family Pseudomonadaceae containing 191 validly described species.Recently, 16S rRNA sequence analysis has redefined the taxonomy of many bacterial species. As a result, the genus Pseudomonas includes strains formerly classified in the...
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 leucineLeucine
Leucine is a branched-chain α-amino acid with the chemical formula HO2CCHCH2CH2. Leucine is classified as a hydrophobic amino acid due to its aliphatic isobutyl side chain. It is encoded by six codons and is a major component of the subunits in ferritin, astacin and other 'buffer' proteins...
rich repeats. LRRs are multiple, serial repeats of a motif of roughly 24 amino acid
Amino acid
Amino acids are molecules containing an amine group, a carboxylic acid group and a side-chain that varies between different amino acids. The key elements of an amino acid are carbon, hydrogen, oxygen, and nitrogen...
s in length, with leucines or other hydrophobic residues at regular intervals. Some may also contain regularly spaced proline
Proline
Proline is an α-amino acid, one of the twenty DNA-encoded amino acids. Its codons are CCU, CCC, CCA, and CCG. It is not an essential amino acid, which means that the human body can synthesize it. It is unique among the 20 protein-forming amino acids in that the α-amino group is secondary...
s and arginine
Arginine
Arginine is an α-amino acid. The L-form is one of the 20 most common natural amino acids. At the level of molecular genetics, in the structure of the messenger ribonucleic acid mRNA, CGU, CGC, CGA, CGG, AGA, and AGG, are the triplets of nucleotide bases or codons that codify for arginine during...
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 but there are some, most notably the mloMLO
MLO may refer to:*Malibu Locals Only, a group of youths local to Malibu, California*Medio-lateral Oblique, a standard view used in mammography...
gene in barley
Barley
Barley is a major cereal grain, a member of the grass family. It serves as a major animal fodder, as a base malt for beer and certain distilled beverages, and as a component of various health foods...
, in which monogenic resistance is conferred by recessive
Recessive
In genetics, the term "recessive gene" refers to an allele that causes a phenotype that is only seen in a homozygous genotype and never in a heterozygous genotype. Every person has two copies of every gene on autosomal chromosomes, one from mother and one from father...
allele
Allele
An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...
s. 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 encompasssome 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
Virulence
Virulence is by MeSH definition the degree of pathogenicity within a group or species of parasites as indicated by case fatality rates and/or the ability of the organism to invade the tissues of the host. The pathogenicity of an organism - its ability to cause disease - is determined by its...
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
Homology (biology)
Homology forms the basis of organization for comparative biology. In 1843, Richard Owen defined homology as "the same organ in different animals under every variety of form and function". Organs as different as a bat's wing, a seal's flipper, a cat's paw and a human hand have a common underlying...
of Avr genes in animal pathogens have been shown to do this. For example, the AvrBs3 family of proteins possess DNA
DNA
Deoxyribonucleic acid is a nucleic acid that contains the genetic instructions used in the development and functioning of all known living organisms . The DNA segments that carry this genetic information are called genes, but other DNA sequences have structural purposes, or are involved in...
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 hypothesisHypothesis
A hypothesis is a proposed explanation for a phenomenon. The term derives from the Greek, ὑποτιθέναι – hypotithenai meaning "to put under" or "to suppose". For a hypothesis to be put forward as a scientific hypothesis, the scientific method requires that one can test it...
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
Arabidopsis thaliana
Arabidopsis thaliana is a small flowering plant native to Europe, Asia, and northwestern Africa. A spring annual with a relatively short life cycle, arabidopsis is popular as a model organism in plant biology and genetics...
is able to respond to two completely unrelated avirulence factors from P. syringae
Pseudomonas syringae
Pseudomonas syringae is a rod shaped, Gram-negative bacterium with polar flagella. It is a plant pathogen which can infect a wide range of plant species, and exists as over 50 different pathovars, all of which are available to legitimate researches via international culture collections such as the...
. 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
Two-hybrid screening
Two-hybrid screening is a molecular biology technique used to discover protein–protein interactions and protein–DNA interactions by testing for physical interactions between two proteins or a single protein and a DNA molecule, respectively.The premise behind the test is the activation of...
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.