CASE STUDY 10.1 Plant–pathogen interactions: pathogens as biotic stress factors

Printer-friendly version

Barbara Howlett

 Gene expression in plants is highly responsive to many factors in the physical environment, but we also need to consider how plants respond to biotic factors. As an extended example, we take a look at an exciting area of plant biology: plant–pathogen interactions. In the late 1950s, scientists first recognised that the outcome of an interaction between plant and pathogen is often determined by the products of genes from both organisms. Pathogen genes were first identified in the mid-1980s but it took several more years before any of the plant genes involved were cloned and sequenced. By characterising these genes, we are beginning to comprehend the sometimes subtle interactions and signal transduction pathways involved in pathogen perception by the plant. This knowledge should lead to novel strategies for combating plant disease.

Cellular events arising in ‘gene for gene’ systems

A model for the interaction between a pathogen and a plant in a ‘gene for gene’ system is illustrated here (Figure 1). The avirulence gene product (Avr) is secreted by the pathogen and interacts with the resistance gene product (Res), either at the plant cell membrane or within the cytoplasm. We think this stimulates a cascade of events in the plant cell, which includes activation of protein kinases, increased ion fluxes across the cell membrane, and an oxidative burst where reactive oxygen species (superoxide anion (O2), hydrogen peroxide) are produced that cross-link structural proteins in the plant cell wall. These events in turn activate plant defence responses, including the ‘hypersensitive response’ where rapid necrosis of plant cells adjacent to the pathogen results in the plant sacrificing a few cells to stop invasion. In addition, expression of a series of genes leads to production of ‘pathogenesis-related proteins’ (for example, glucanase, chitinase, thaumatin-like proteins) and synthesis of phytoalexins (anti-microbial com-pounds, see Figure 1).

Many of these events still occur in the absence of com-plementary resistance and avirulence genes, but more slowly and to a lesser extent. To complete the resistance–pathogenicity equation, we find expression of pathogen genes essential for invasion, especially toxins and enzymes that degrade plant cell walls and cuticles. Some of the enzymes release small cell wall fragments which in turn elicit transcription of a series of plant genes which activate plant resistance responses as described above. The speed, magnitude and site of these combined responses determines whether a plant is resistant or susceptible.

Resistance and avirulence genes determine whether infection occurs in ‘gene for gene’ systems


Figure 1 Cellular and molecular interactions between pathogen and plant cells during recognition and responses to infection. Host resistance depends on induction of one or more response pathways. Pathogen virulence depends on a lack of host-recognised avirulence gene products.

(Based on Baron and Zambryski 1995).

The ‘gene for gene’ concept refers to plant–pathogen systems where resistance only occurs when a dominant resistance gene in the plant and a corresponding dominant avirulence gene in the pathogen are both present. The notion of an avirulence gene appears at first glance to be counter-intuitive, as we might not expect it to be advantageous for a pathogen to have a gene preventing it from successfully invading a plant. We believe that this may be explained by avirulence genes having an essential, but as yet undefined, role in the pathogen. For a pathogen to overcome resistance and cause disease, the avirulence gene must be inactivated or deleted. In the constant battle between invader and defender, there is strong pressure for co-evolution of both pathogen and plant.

Since 1984, more than 40 avirulence genes, almost all from bacteria, have been cloned. These genes appear to have few features in common. Cloning resistance genes has been far more difficult, mainly because plants have much larger and more complex genomes than microorganisms. Molecular tech-niques such as tagging genes via transposable elements, positional cloning and mutational analysis have enabled identifi-cation of resistance genes. Analysis of nucleotide sequences of the dozen or more resistance genes cloned from monocotyledons and dicotyledons conferring resistance to fungi, bacteria or viruses has resulted in the surprising finding that, in contrast to the diverse avirulence genes, many resistance genes have conserved structural features. Several have repeated series of amino acid sequences rich in leucine, which may be involved in protein–protein interactions. Some resistance proteins also show sequence similarities to protein kinases, suggesting that protein phosphorylation may be a component of the signal transduction pathways.

Systemic acquired resistance

Infection of plants often leads to a phenomenon called systemic acquired resistance (SAR). This is a whole-plant response with some conceptual analogies to animal immune responses and leads to enhanced resistance to subsequent attacks by the same or even unrelated pathogens. SAR is associated with increased systemic (meaning throughout the whole organism, rather than just at the site of infection) expression of many of the plant defence genes described above.

Salicylic acid plays an important role in systemic acquired resistance.

Externally applied salicylic acid can induce SAR. Levels of this compound increase 50-fold after infection of tobacco plants that are resistant to tobacco mosaic virus, while there is no increase in susceptible tobacco. The increase in salicylic acid correlates with production of pathogenesis-related proteins (Figure 1). Salicylic acid may also bind to and directly inhibit catalases which normally inactivate reactive oxygen species such as hydrogen peroxide. The resulting increased levels of hydrogen peroxide then induce peroxidase-catalysed cross-linking of plant cell walls.

More of the role of salicylic acid in SAR has been revealed by experiments on transgenic tobacco plants expressing a gene for an enzyme that degrades salicylic acid (salicylic acid hydroxylase). These plants do not exhibit SAR and are more susceptible to viral, bacterial and fungal pathogens than non-transgenic plants lacking salicylic acid hydroxylase. However, we are still uncertain whether salicylic acid is the translocated signal responsible for inducing SAR throughout the plant. SAR can also be induced by analogues of salicylic acid. Some of these are potentially attractive as plant protection compounds against a broad spectrum of diseases in many crops.