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THE GENETIC BASIS OF HOST-PATHOGEN SPECIFICITY IN PLANT DISEASE RESISTANCE

An essay by Angela Moncrieff.

Introduction

Plants are constantly confronted with a wide variety of potential pathogens within their environment. Nevertheless, the development of disease is the exception rather than the rule, due to the highly efficient nature of the coordinated systems of passive and active defences that have evolved in plants Link to Passive Defenses and Active Defenses. These defences generally limit the host range of a microorganism capable of causing plant disease to the members of a single plant genus or species, and affect all races of a particular pathogen similarly. However, plant disease resistance can also be induced in specific plant cultivars within the host range, or only in response to specific races of pathogen.

The specificity of plant responses to pathogens can be classified into two broad categories. Non-specific resistance (general, non-host or basic resistance) is a response to all races of a particular pathogen, and occurs in all cultivars of a host plant species. In contrast, specific resistance is dependent upon the presence of a particular pathogen race, a particular host plant cultivar, or both. The underlying genetic basis of each type of plant disease resistance differs according to the genetic makeup of both plant and pathogen.

Non-specific Plant Disease Resistance

Non-specific plant disease resistance is multi-component, relying upon a foundation of passive plant defences Link, and usually also involving the activation of active defences by non-specific elicitors of biotic origin Link. The combination of defences involved in this type of resistance is highly coordinated and similar for all plant-pathogen interactions. However, substantial variation in both the timing and degree of the active component of plant defence and in environmental factors have been shown to be critical to its success. Whilst stronger, more timely non-specific defence responses are responsible for many incompatible plant-pathogen interactions, weaker non-specific defence responses are often overcome by the pathogen in compatible interactions, and have also been observed in symbiotic relationships with endophytic fungi Link.

The genetic basis underlying non-specific plant disease resistance is complex, and involves multiple genes that encode proteins with a diversity of functions in both partners of the plant-pathogen interaction. These can be divided into pathogenicity genes that determine the ability of the pathogen to cause disease and defence-related genes that enable the plant host to execute defence responses. Both classes of genes contain members that are expressed in a constitutive manner, in addition to genes that are only expressed in response to the interaction of plant and pathogen. Pathogen genes that govern pathogenicity usually encode proteins that have a negative impact on disease resistance. The majority of pathogenicity genes in plant pathogens condition the ability to establish infection, and these include genes that encode proteins with specific roles in adhesion to the plant surface, the formation of penetration structures Link, cell wall degradation, and the synthesis of toxic compounds. However, a number of pathogenicity genes instead govern the ability of the pathogen to defeat plant defences, such as those encoding proteins involved in the detoxification of phytoalexins Link. Plant defence-related genes encode proteins that enable the detection of non-specific elicitors and the activation of an intracellular signalling pathway leading to plant defences, as well as those themselves involved in passive and active plant defences Link to Passive Defenses and Active Defenses.

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Specific Plant Disease Resistance

In contrast to non-specific resistance, specific plant disease resistance appears to be governed by a single gene or a small number of related genes, which encode proteins capable of altering the outcome of an otherwise compatible plant-pathogen interaction. Genes conditioning host-pathogen specificity are found in particular subpopulations of the pathogen, plant host, or both interacting organisms, and specific plant disease resistance can be subdivided into three major categories on this basis.

(a) Race-specific resistance

Race-specific resistance is induced in response to only a particular race of pathogen, but occurs in all cultivars of the host plant. This type of specific disease resistance is dependent upon genetic variation within the pathogen species, and the production of proteins capable of altering the outcome of an otherwise compatible plant-pathogen interaction in only certain pathogen races.

(b) Cultivar-specific resistance

Cultivar-specific resistance is activated only in a specific host plant cultivar, but in reaction to all races of a pathogen species. In a few plant-pathogen systems where non-specific resistance limits the host range of the pathogen to a plant genus, this type of resistance occurs at the level of the host plant species, and is termed species-specific resistance. Cultivar-specific or species-specific resistance relies upon genetic variation within the host plant species or genus, and the production of proteins capable of altering the outcome of an otherwise compatible plant-pathogen interaction in only certain plant cultivars or species. 

(c) Race-cultivar-specific (gene-for-gene) resistance

If both pathogen and host specificity are involved, plant disease resistance is termed race-cultivar-specific resistance, since it results only from the interaction of a particular pathogen race with a particular cultivar of the host plant. This type of resistance is usually referred to as gene-for-gene resistance, because in most cases it requires the presence of both a race-specific avirulence (avr) gene in the pathogen and one or more corresponding cultivar-specific resistance (R) genes in the host plant (Figure 1).

Avirulence and resistance genes are usually dominant genes, which may exist within multigene families, and undergo a high rate of mutation in response to the presence of each other. Maintenance of detrimental avirulence genes is thought to be due to a small, additive, pleiotropic pathogenicity role in the pathogen. In a small number of cases of race-cultivar-specific resistance that involve the production of host-selective toxins, race-cultivar-specific resistance relies upon the absence of either a race-specific gene conditioning toxin production and a cultivar-specific gene governing toxin sensitivity (Figure 2).

Both types of race-cultivar-specific resistance are dependent upon genetic variation within both the pathogen and host species, and the production of proteins by only particular pathogen races and host cultivars, that are capable of acting in combination to alter the outcome of a plant-pathogen interaction. An otherwise compatible interaction results in resistance due to the presence of both avirulence and resistance genes, whereas genes conditioning toxin production and toxin sensitivity cause disease in an otherwise incompatible interaction.

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Mechanisms Underlying Specific Plant Disease Resistance

The biochemical mechanisms responsible for the induction of specific resistance in plant-pathogen interactions are poorly understood, but are likely to vary with both the type of specific resistance and the plant-pathogen system involved. The three most common mechanisms underlying specific resistance appear to be race-specific elicitors, host-selective toxins and race-specific suppressors, but others, as yet unknown, may also exist.

(a) Race-specific elicitors

The majority of cases of race-specific resistance appear to result from the generation by a pathogen of race-specific elicitors of active plant defences Link, and the recognition of these by the plant host. Resistance with this biochemical basis is often also cultivar-specific (and thus gene-for-gene), since the elicitor interacts with a corresponding plant receptor that is usually unique to a particular cultivar of the host plant. The recognition of the elicitor by its receptor is proposed to occur at the plant plasma membrane for most fungal pathogens, and within the plant cell for bacterial and viral pathogens. In bacterial biotrophs such as Xanthomonas and Pseudomonas, which are extracellular plant pathogens, this event is dependent upon a bacterial membrane transport protein that delivers the elicitor into the plant cell, and is encoded by the hrp gene complex Link. Interaction of the elicitor and receptor activates a complex signal transduction pathway resulting in the induction of plant defences against pathogen races harbouring the elicitor. The elicitor is generally the protein that is encoded by the avirulence gene, however in some plant-pathogen interactions the elicitor has been found to be the product of a reaction catalysed by this protein. Resistance genes in some cases directly encode cultivar-specific receptors of race-specific elicitors, and in these cases a direct physical interaction between avirulence and resistance gene products may occur. However resistance proteins are more likely to function by registering interactions between the elicitor and an unknown target protein, or act as unique links in the signalling pathway leading to active plant defences.

(b) Host-selective toxins

Race-cultivar-specific pathogen resistance can also occur due to the production of compounds that are toxic to plants. These host-selective toxins (HSTs) are generated in a race-specific manner, mainly by necrotrophic species of the fungal genera Alternaria and Cochliobolus. A few of the approximately twenty known host-selective toxins are proteins or peptides that are directly encoded by race-specific pathogen genes. However, most are non-protein compounds of low molecular weight that are synthesised in reactions catalysed by proteinaceous race-specific gene products. Following transport into the host plant cell via a highly coordinated delivery system, host-selective toxins cause cellular damage, but only in toxin-sensitive cultivars that harbour a single gene conditioning toxin sensitivity. The mode of action of host-selective toxins is highly variable, but appears to always involve either activation or inhibition of a cultivar-specific protein. For example, T-toxin, produced by C. heterostrophus, serves to activate a cultivar-specific protein capable of forming destructive membrane pores, whereas HC-toxin from C. carbonum inhibits a cultivar-specific version of an enzyme that modifies DNA-bound proteins to cause disturbances in gene expression.

(c) Race-specific suppressors

Race-specific resistance can also result from pathogen production of race-specific suppressors that inhibit a non-specific resistance response. To date, race-specific suppressors have been described for only a few species of biotrophic plant-pathogenic fungi, including Phytophthora infestans. In contrast to race-specific elicitors, they are proposed to interfere with elicitor binding, signal transduction, gene expression or plant defences to suppress the non-specific resistance response towards races that harbour them. Race-specific suppressors may be proteins directly encoded by pathogen genes governing race-specificity, or may be non-protein compounds produced by reactions catalysed by these proteins. Plant disease resistance in cases involving race-specific suppressors may or may not also be cultivar-specific (and thus gene-for-gene), depending on whether or not the actual mechanism of suppression involves a cultivar-specific plant molecule.

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The Relationship Between Non-specific and Specific Resistances

The connection linking non-specific and specific resistances is rarely considered and thus poorly understood. However, it is likely that the relationship between these two forms of resistance differs depending on the particular type of specific resistance and the biochemical mechanism involved in its induction.

Specific resistance conditioned by race-specific elicitor molecules is generally of a higher intensity and more successful than non-specific plant disease resistance, and also involves an oxidative burst that is diphasic in nature. These observations indicate that this type of specific resistance may be composed of a race-specific component to resistance, which is supplementary to and superimposed upon an unsuccessful non-specific resistance response. A common signalling pathway leading to defence responses may be activated to different degrees by both non-specific elicitors and race-specific elicitors resulting from the same plant-pathogen interaction. The highly conserved nature of plant resistance mechanisms and the observation that different pathogen races can elicit defence responses that differ only in intensity both support this hypothesis. However, different pathogen races can also induce resistance responses that contain unique defence components. For example, the hypersensitive response Link is rarely induced by non-specific elicitors, but almost always occur during a race-specific resistance response. This indicates that different signalling pathways, possibly convergent at some point, may be activated by non-specific and race-specific elicitors (Figure 3).

Specific resistance conditioned by host-selective toxins or race-specific suppressor molecules by definition cannot involve the elicitation of a supplementary resistance response. Specificity of resistance in these cases must therefore involve modification or negation of an otherwise successful non-specific resistance response that occurs in all pathogen subpopulations and all host cultivars. The presence of race-specific suppressors in some pathogen races could be expected to prevent or lessen the non-specific defence response, either in its entirety by interfering with elicitor binding or an early signalling step, or in part by obstructing a late signalling step or an actual defence process (Figure 4).

In contrast, the activity of host-selective toxins is probably superimposed on a non-specific resistance response occurring in its entirety, and merely lessens its influence by killing host plant cells before their defences can be fully activated.

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Conclusion

Plant disease resistance is a complex phenomenon that most commonly occurs in a non-specific manner, as a result of multiple genes conditioning the ability of the pathogen to cause disease and enabling the plant host to mount an effective defence response. However, plant disease resistance can also be induced only in response to particular pathogen races (race-specific resistance), only in particular host plant cultivars (cultivar-specific resistance), or only when both a specific pathogen race and plant cultivar interact (race-cultivar-specific or gene-for-gene resistance). This host-pathogen specificity can be attributed to a single gene or a small number of related genes enabling the production of race-specific elicitors, host-selective toxins, or race-specific suppressors in different host-pathogen systems. Specific plant disease resistance resulting from race-specific elicitors is probably superimposed upon a non-specific resistance response that has been overcome in the host range of the pathogen. In contrast, host-selective toxins and race-specific suppressors most likely achieve host-pathogen specificity in disease resistance through the modification or negation of an otherwise successful non-specific resistance response.

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References

Agrios, G. N. (1997) Plant Pathology, 4th edn. Academic Press, San Diego. pp 115-142.

Dickinson, C. H. and Lucas, J. A. (1982) Plant Pathology and Plant Pathogens. Blackwell Scientific Publications, Oxford. pp 168-183.

Gabriel, D. W. (1989) Genetics of plant parasite populations and host-parasite specificity. In Kosuge, T. and Nester, E. W. (Eds) Plant-Microbe Interactions: Molecular and Genetic Perspectives, Volume 3. McGraw-Hill, New York.

Jalali, B. L. and Bhargava, S. (2002) Gene expression during host plant and fungal pathogen interactions. Proceedings of the National Academy of Sciences of India 72: 235-255.

Wolpert, T. J.; Dunkle, L. D. and Ciuffetti, L. M. (2002) Host-selective toxins and avirulence determinants: What's in a name? Annual Review of Phytopathology 40: 251-285.

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