Hypersensitive response

Source: Wikipedia, the free encyclopedia.
For hypersensitivity response in humans, see Hypersensitivity.

Hypersensitive response (HR) is a mechanism used by plants to prevent the spread of infection by

viruses, fungi and even insects.[2]

Lesions caused by the plant hypersensitive response

HR is commonly thought of as an effective defence strategy against biotrophic plant

pathogens such as Phytophthora infestans which at the initial stages of the infection act as biotrophs but later switch to a necrotrophic lifestyle. It is proposed that in this case HR might be beneficial in the early stages of the infection but not in the later stages.[3]

Genetics

The first idea of how the hypersensitive response occurs came from

genes that are involved in the plant-pathogen interactions tend to evolve at a very rapid rate.[5]

Mechanism of plant NLR protein activation after pathogen invasion

Very often, the resistance mediated by

virulence factors.[7]

Mechanism

HR is triggered by the plant when it recognizes a

pathogens.[8]

In phase one of the HR, the activation of

efflux of hydroxide and potassium to the outside the cells, and an influx of calcium and hydrogen ions into the cells.[9]

In phase two, the cells involved in the HR generate an

cellular membrane function, in part by inducing lipid peroxidation and by causing lipid damage.[9]

The alteration of ion components in the cell and the breakdown of cellular components in the presence of ROS result in the death of affected cells, as well as the formation of local lesions. Reactive oxygen species also trigger the deposition of lignin and callose, as well as the cross-linking of pre-formed hydroxyproline-rich glycoproteins such as P33 to the wall matrix via the tyrosine in the PPPPY motif.[9] These compounds serve to reinforce the walls of cells surrounding the infection, creating a barrier and inhibiting the spread of the infection.[10] Activation of HR also results in disruption of the cytoskeleton, mitochondrial function and metabolic changes, all of which might be implicated in causing cell death.[11][12][13]

Direct and indirect activation

HR can be activated in two main ways: directly and indirectly. Direct binding of the

virulence factors are integrated into the NLRs. An example of this can be observed in plant resistance to the rice blast pathogen, where the RGA5 NLR has a heavy-metal-associated (HMA) domain integrated into its structure, which is targeted by multiple effector proteins.[15]

An example of indirect recognition: AvrPphB is a type III effector protein secreted by Pseudomonas syringae. This is a protease which cleaves a cellular kinase called PBS1. The modified kinase is sensed by RPS5 NLR.[16]

The Resistosome

Recent structural studies of CC-NLR

proteins downstream of them, which are then activated to form the resistosomes and induce HR.[17]

NLR pairs and networks

It is known that NLRs can function individually but there are also cases where the NLR

genes of both the sensor and the respective helper NLR are usually paired in the genome and their expression could be controlled by the same promoter. This allows the functional pair, instead of individual components, to be segregated during cell division and also ensures that equal amounts of both NLRs are made in the cell.[18]

The receptor pairs work through two main mechanisms: negative regulation or cooperation.

In the negative regulation scenario, the sensor NLR is responsible for negatively regulating the helper NLR and preventing cell death under normal conditions. However, when the effector protein is introduced and recognized by the sensor NLR, the negative regulation of the helper NLR is relieved and HR is induced.[19]

In the cooperation mechanisms, when the sensor NLR recognizes the effector protein it signals to the helper NLR, thus activating it.[20]

Recently, it was discovered that in addition to acting as singletons or pairs, the plant NLRs can act in networks. In these networks, there are usually many sensor NLRs paired to relatively few helper NLRs.[20]

NLR Singleton, Pair and Network

One example of

proteins involved in NLR networks are those belonging to the NRC superclade. It seems that the networks evolved from a duplication event of a genetically linked NLR pair into an unlinked locus which allowed the new pair to evolve to respond to a new pathogen. This separation seems to provide plasticity to the system, as it allows the sensor NLRs to evolve more rapidly in response to the fast evolution of pathogen effectors whereas the helper NLR can evolve much slower to maintain its ability to induce HR. However, it seems that during evolution new helper NLRs also evolved, supposedly, because certain sensor NLRs require specific helper NLRs to function optimally.[20]

Bioinformatic analysis of plant NLRs has shown that there is a conserved MADA motif at the N-terminus of helper NLRs but not sensor NLRs. Around 20% of all CC-NLRs have the MADA motif, implying the motif's importance for the execution of HR.[21]

Regulation

Accidental activation of HR through the NLR

proteins are immediately ubiquitinated and degraded by the proteasome.[22] It has been observed that in many cases, if the chaperone proteins involved in NLR biosynthesis are knocked-out, HR is abolished and NLR levels are significantly reduced.[23]

The domain structure of a typical plant NLR

proteins prevents the spontaneous exchange of ADP for ATP and thus activation of HR. Only when a virulence factor is sensed, the ADP is exchanged for ATP.[14]

proteins involved in ROS production during pathogen invasion.[3]

HR is also a temperature-sensitive process and it has been observed that in many cases plant-pathogen interactions do not induce HR at temperatures above 30 °C, which subsequently leads to increased susceptibility to the

pathogens are not understood in detail, however, research suggests that the NLR protein levels might be important in this regulation.[25] It is also proposed that at higher temperatures the NLR proteins are less likely to form oligomeric complexes, thus inhibiting their ability to induce HR.[26]

It has also been shown that HR is dependent on the light conditions, which could be linked to the activity of

chloroplasts and mainly their ability to generate ROS.[27]

Mediators

Several

oxidative deamination of polyamines, especially putrescine, and releases the ROS mediators hydrogen peroxide and ammonia.[28] Other enzymes thought to play a role in ROS production include xanthine oxidase, NADPH oxidase, oxalate oxidase, peroxidases, and flavin containing amine oxidases.[9]

In some cases, the cells surrounding the lesion synthesize

bacterial cell walls; or by delaying maturation, disrupting metabolism, or preventing reproduction of the pathogen
in question.

Studies have suggested that the actual mode and sequence of the dismantling of plant cellular components depends on each individual plant-pathogen interaction, but all HR seem to require the involvement of

protein synthesis, an intact actin cytoskeleton, and the presence of salicylic acid.[8]

Pathogen evasion

genes.[29]

Systemic immunity

Local initiation of HR in response to certain necrotrophic

genes to induce HR response only when the pathogen is present but not at any other time. This approach, however, has been mostly unfeasible as the modification also leads to a substantial reduction in plant yields.[3]

Hypersensitive response as a driver for plant speciation

It has been noticed in Arabidopsis that sometimes when two different plant lines are crossed together, the offspring show signs of hybrid necrosis. This is due to the parent plants containing incompatible NLRs, which when expressed together in the same cell, induce spontaneous HR.[31]

This observation raised a hypothesis that plant

populations from the same species develop incompatible NLRs in response to different pathogen effectors, this can lead to hybrid necrosis in the F1 offspring, which substantially reduces the fitness of the offspring and gene flow to subsequent generations.[32]

Comparison to animal innate immunity

Both plants and animals have NLR

proteins which seem to have the same biological function – to induce cell death. The N-termini of plant and animal NLRs vary but it seems that both have LRR domains at the C-terminus.[33]

A big difference between animal and plant NLRs is in what they recognise. Animal NLRs mainly recognise

viruses and viruses do not have PAMPs as they are rapidly evolving. Animals, on the other hand, have intracellular pathogens.[34]

The vast majority of plant lineages, except for certain

Arthropods.[33]

Upon recognition of

caspases.[37]

See also

References

  1. ^ Freeman S (2003). "Chapter 37: Plant Defense Systems". Biological Science. Prentice Hall. Archived from the original on 2012-12-01. Retrieved 2007-01-12.
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