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Mutual Potentiation of Plant Immunity by Cell-surface and Intracellular Receptors

Bruno Pok Man Ngou, Hee-Kyung Ahn, Pingtao Ding, Jonathan DG Jones

Posted on: 29 April 2020

Preprint posted on 17 April 2020

Article now published in Nature at http://dx.doi.org/10.1038/s41586-021-03315-7

and

Pattern-recognition receptors are required for NLR-mediated plant immunity

Minhang Yuan, Zeyu Jiang, Guozhi Bi, Kinya Nomura, Menghui Liu, Sheng Yang He, Jian-Min Zhou, Xiu-Fang Xin

Posted on:

Preprint posted on 22 April 2020

Article now published in Nature at http://dx.doi.org/10.1038/s41586-021-03316-6

Good friends boost you up when you most need it. Two kinds of plant immune responses work together to overcome wily pathogens, with one type of response bolstering the other when it falters.

Selected by Sruthi S Balakrishnan

Categories: biochemistry, cell biology, microbiology, molecular biology, plant biology

Background

In a bid to keep up with constantly changing pathogens, the innate immune system of plants has evolved to have two different angles of attack1. Their first line of defence, termed Pattern Triggered Immunity (PTI) is activated when the receptors on plant cells sense molecular signatures borne by the pathogens. These are usually represented by conserved amino acid motifs that are essential for pathogens to function. The PTI triggers responses like reactive oxygen species (ROS) production and callose deposition in plant cells. While these measures are effective, some pathogens are smarter and have evolved means to avoid such attacks. They release molecules known as “effectors” to thwart the PTI and intercept the immune response. This makes the plant susceptible to infection again.

Fortunately, plants have evolved alongside the pathogens to develop a second type of innate immune response to deal with these effectors, known as Effector Triggered Immunity (ETI). The ETI response can either recognise effectors directly or through their interactions with other accessory proteins. ETI often acts as a suicide bomber, activating a hypersensitive cell death response (HR) and forcibly killing infected cells to prevent the spread of infection.

The PTI and ETI systems have always been thought to act sequentially but independently. They have only recently been discovered to share common elements, but the cellular responses they evoke appear to be distinct2. The preprints discussed here show not only do the two systems interact, but the activation of PTI is essential for ETI to function. Through the use of mutants that can explicitly trigger either PTI or ETI and a range of infection protocols, the two groups have shown that ETI acts via receptors unique to PTI. They also show that activation of ETI can boost the efficiency of PTI and prolong the duration of the immune response.

 

Key Results

The first preprint, by Ngou et al., used specific molecules to selectively induce PTI, ETI or a combination of both in transgenic Arabidopsis thaliana, using components from Pseudomonas syringae to induce immune responses. One of the first readouts they checked was ROS production, which is triggered by PTI. They found that when ETI was co-induced along with PTI, the ROS production effect was stronger and lasted for a longer duration than by PTI induction alone. This effect was also true for other PTI responses such as callose deposition and expression of PTI-induced genes. None of these effects were seen when only ETI was induced.

They next assessed the effect of ETI induction on several signalling components required for PTI, such as MAP kinases and NADPH oxidases. When both ETI and PTI were co-induced, the overall mRNA levels, activation levels and duration of activation of these enzymes were higher than by PTI induction alone. As seen earlier, these components did not respond when only ETI was activated.

The necessity for ETI arises when pathogens bypass PTI through the use of effectors and make plants susceptible to infection. When a virulent strain was used to infect plants and activate PTI, the researchers saw that, over time, the levels of PTI components reduced and the plants became susceptible to infection. When ETI was artificially induced in this scenario, the PTI components were once again upregulated and the plant defences kicked in. This led them to suggest that ETI exists as means of boosting the PTI response and not as a separate immune response. This was supported by another experiment showing that, in PTI-deficient Arabidopsis, ETI-boosted immunity could not be triggered. ETI therefore also appeared to rely on PTI components for establishing effective resistance, and could reinstate PTI responses in the event of susceptibility.

The second preprint, by Yuan et al., used PTI-deficient mutants and avirulent strains of Pseudomonas syringae to study the interaction between PTI and ETI. The first result they found was that the presence of PTI receptors is vital for the activation of ETI-boosted resistance, same as reported in the first preprint. In addition, these PTI-impaired plants showed very mild ETI responses and slow HR.

They next assessed the production of ROS by both the immune systems. PTI alone usually triggers a short burst of ROS, whereas ETI and PTI together trigger a longer and more sustained burst. Using PTI-deficient mutant plants, they found that PTI activation is required for the ETI-enhanced ROS burst. They also saw that ROS production by both systems is mediated by the activity of RBOHD, an NADPH oxidase.  Essentially, it appeared that both systems work in tandem to coordinate the ETI-enhanced ROS burst that is induced by PTI.

Mirroring the results from the first preprint, this group also found that induction of ETI can upregulate the expression levels of several genes required for the PTI response.

In essence, the two groups identified the requirement of the PTI receptors in activating ETI responses. ETI also appears to be a means of bolstering a faded PTI response, hence overcoming any susceptibility induced by pathogens. They also laid the groundwork for uncovering the specific mechanisms behind the crosstalk.

 

What I Liked

Both studies address an often-overlooked question in the field of plant immunity, which is the potential crosstalk between PTI and ETI. They also appear to have worked together to coordinate the preprint uploads and have referred to each other’s work in their respective manuscripts. They not only proved the existence of two-way communication between the two pathways, but also sought to provide mechanistic details of the same.

 

Questions for the Authors

  1. The ETI system basically appears to have two functions – restore PTI and independently trigger HR and ROS, etc. Which of these is more effective at deterring pathogens?
  2. In the absence of susceptibility, if PTI alone is a more effective immune response, why does ETI need to have the secondary effects of HR and inflammasome formation? Is it a means of buying time until all the PTI components are restored?

Tags: arabidopsis, immunity, phytopathology, plant

doi: https://doi.org/10.1242/prelights.19631

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Author's response

Pingtao Ding shared about Mutual Potentiation of Plant Immunity by Cell-surface and Intracellular Receptors

The ETI system basically appears to have two functions – restore PTI and independently trigger HR and ROS, etc. Which of these is more effective at deterring pathogens?

This question is very philosophical and almost too idealistic to answer. What we believe is that in a real world with a constantly changing environment, functions of ETI either restoring PTI or activating HR are both fundamentally important for plant adaptation. If specifically referring to resistance against pathogens, we believe that ETI restoring PTI plays a more important role at thwarting pathogenesis, as HR, in some cases, is dispensable for resistance against pathogens#. In addition, we would like to highlight:

1) Our study shows that ROS production largely relies on PTI (almost zero ROS in the PTI receptor mutant background), and establishing effective ROS, as part of many immune responses, is required for preventing bacterial growth.

2) We propose that PTI and other ETI-associated pathways could act independently and, collectively, they lead to robust resistance to halt pathogens. Mutating either one of them could lead to less effective or even compromised resistance.

Reference:

# Castel B, Ngou PM, Cevik V, Redkar A, Kim DS, Yang Y, Ding P, Jones DGJ. Diverse NLR immune receptors activate defence via the RPW 8‐NLR NRG1. New Phytologist. 2019 Apr; 222(2): 966–980.

In the absence of susceptibility, if PTI alone is a more effective immune response, why does ETI need to have the secondary effects of HR and inflammasome formation? Is it a means of buying time until all the PTI components are restored?

These are very interesting questions. To give proper answers, here we need to clarify several concepts.

1) To address the first part of these questions: both PTI and ETI are only activated upon perceptions of corresponding ligands, so ETI-triggered HR is not activated if there are only PTI ligands.

In addition, the concept of inflammasome formation is relatively new and believed to be very first steps ETI initiation upon effector recognition. Only strongly activated of ETI culminates in HR as a consequence.

2) It really depends how we look into the cases, so yes you can consider activation of ETI in addition to PTI serves as a means of buying time from a very subjective view. However, in a real world, pathogens and plants interactions are not a rule-fixed game. From an evolutionary view, both pathogens and plants thrive to survive and pass their DNAs into next round of lives as possible as they can, so PTI and ETI serving as part of the immune mechanisms in plants will do whatever they can to win the battle.

To win a battle, similarly to that in the human world, timing of launching effective defence system is the key, so any delay of immune activation will lead the loss of the game. So back to studies from both of our two groups, we have provided evidence and a new reasonable working model, in which, PTI alone is not enough to halt pathogen (because effectors can suppress immunity) and ETI is required to boost strong defence but the enhancement is PTI-dependent. As a result, our studies clarify how ETI and PTI pathways interact with each other.

and

Xiufang Xin shared about Pattern-recognition receptors are required for NLR-mediated plant immunity

The ETI system basically appears to have two functions – restore PTI and independently trigger HR and ROS, etc. Which of these is more effective at deterring pathogens?

1) Our study shows that ROS production largely relies on PTI (almost zero ROS in the PTI receptor mutant background), and ROS is important for preventing bacterial growth.

2) We propose that PTI and other ETI-associated pathways could act independently and, collectively, they lead to robust resistance to halt pathogens. Mutating either one of them could lead to compromised ETI.

In the absence of susceptibility, if PTI alone is a more effective immune response, why does ETI need to have the secondary effects of HR and inflammasome formation? Is it a means of buying time until all the PTI components are restored?

1) I think there is a misunderstanding here. HR and “inflammasome” formation are not secondary effects of ETI. ETI responses lead to HR (a consequence) and “inflammasome” formation is at the NLR protein activation stage (a very early response).

2) In real cases of infection by virulent pathogens, PTI alone is not enough to halt pathogen (because effectors can suppress immunity) and ETI is required to boost strong defense. Our studies clarify how ETI and PTI pathways interact with each other.

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