Tomato plants infected with Botrytis cinerea. (Image credit: Scot Nelson, https://www.flickr.com/photos/62295966@N07/5830204360)

We typically experience optimal health most of the time. Our bodies are amazingly resilient against nature’s elements. But how does our body know when it is under attack by invading pathogens? Usually, there are several manifestations. We may feel pain, nausea, or weakness, and know that something is off. Although these are not pleasurable sensations, they are associated with important processes that eventually allow our bodies to fight against dangerous infections. For example, a fever is a sign that our body is fighting off infection by harmful bacteria or viruses. It is also part of the healing process, as it stimulates our immune response and creates an unfavorable environment for pathogenic microbes.

Just like us, plants need to sense when they are under attack by harmful microbes, and mount a defense response. This is important since many different pests and pathogens can infect plants. Plant pathogens are broadly divided into two types: “biotrophs”, which feed on living plant tissues and weaken but typically do not kill the infected plant, and “necrotrophs”, which kill the plant cells early during infection and then feed on the dead tissues.

One of the most devastating necrotrophic plant pathogens is the fungus Botrytis cinerea, which is the causative agent of gray mold in a wide range of plant hosts, such as tomato, pepper, strawberry, grape and other crops. These fungi create an “ashy” mass of spores on the infected plant tissues. A recent study by Zhang and colleagues (2018) provides molecular insights into how invasion by B. cinerea can be detected and sometimes eventually overcome by tomato plants.

Molecular Danger Signals

How does a plant “sense” that it is under attack? We know that molecular components from pathogens called “microbe-associated molecular patterns” or MAMPs can be detected by plants. These MAMPs are like molecular IDs that plants detect to activate immunity. In addition to these microbe-derived molecules, plants can also sense remnants of cellular damage caused by pathogens. These host-derived “damage-associated molecular patterns” or DAMPs serve as danger signals, alerting the plants of pathogen invasion and stimulating an immune response.

In the model plant Arabidopsis thaliana, short peptides called phytosulfokines (PSKs) are known to act as danger signals that are produced by the plant when it is suffering an attack from certain necrotrophs. Using this information, Zhang et al. looked for genes encoding PSKs in tomato plants. They found that some of the tomato PSK genes are “switched on” and begin churning out more PSK peptides after infection by the Botrytis pathogen. Pre-treating tomato plants with the PSK peptide protected them against subsequent infection. When infected by the pathogen, plants that had been pre-treated with PSKs showed more robust health, higher photosynthetic efficiency, and lower pathogen levels and cell death than untreated plants.

Pre-treatment with the PSK peptide (but not the inactive dPSK version) protects tomato plants against Botrytis pathogen infection. (Image credit: Zhang et al., 2018, Plant Cell)

The Plant’s Alarm Detector

The PSK signals themselves would be useless without sensors or receptors to perceive them and relay the message for mounting an immune response. If PSK peptides effectively signal that plant damage is allowing pathogens to enter, how does the plant detect them? Based on similarities to known receptors of the PSK peptides from other plants, the authors found and tested two candidate tomato PSK Receptors, PSKR1 and PSKR2. They found that PSKR1 binds the PSK signal more tightly and is more functionally important than PSKR2. Lowering the expression of the PSKR1 gene alone made plants more susceptible to pathogenic Botrytis. This suggests that PSKR2 might function to detect a yet unidentified signal in tomato plants.

Effecting a Protective Response

Once signals are detected by their corresponding receptors, there needs to be fast and tunable processes to relay this message and allow the plant to respond quickly and appropriately. Most of the time, signaling is modulated by messengers such as hormones and other small molecules.

To uncover how sensing of the PSK peptide protects plants, Zhang and colleagues measured the changes in hormone levels in tomato plants after PSK treatment. Interestingly, the amounts of the typical plant defense-associated hormones salicylic acid and jasmonic acid did not change, but levels of the plant growth-associated hormone auxin increased. In support of the hypothesis that the increase of auxin is important in this defense response, PSK peptide treatment could not protect mutant plants that are defective in responding to auxin.

Moreover, PSK treatment also leads to increased levels of cytosolic calcium — another cell signaling messenger. Calcium accumulation allows plants to make more auxin, further increasing their resistance to Botrytis. When the PSKR1 gene was silenced, this led to a dramatically reduced cytosolic calcium burst and compromised plant immunity.

Creating a Comprehensive Security System

Plant cells have many receptors, including some that recognize molecular signals that originate in the invading microbe itself (MAMPs). Other receptors (like PSKR1) recognize a plant-derived DAMP (like PSK) that is triggered by pathogen invasion. Although it detects host-derived DAMPs, PSKR1 resembles a number of other receptors that recognize microbe-derived MAMPs. This is a clue that some of the plants’ large arsenal of receptors may have evolved from a more general ancestral receptor.

Overall, this study revealed detailed clues into how plants can sense, respond, and protect themselves against an agriculturally important necrotrophic (“dead tissue-loving”) pathogen like B. cinerea. This is important since well-studied plant resistance mechanisms against biotrophic (“living tissue-loving”) pathogens usually are not effective against necrotrophs. Studying tomato immunity through the PSK signal also led to the novel discovery connecting auxin and calcium signaling, a significant advance in our understanding of these fundamental biological processes and, hopefully, in improving crop resistance in the field.

Christian Danve M. Castroverde

MSU-DOE Plant Research Laboratory and MSU Plant Resilience Institute

Michigan State University, East Lansing, MI

castrov3@msu.edu

ORCID: 0000–0002–9982–8451

Read the research paper on which this story is based:

Zhang, H., Hu, Z., Lei, C., Zheng, C., Wang, J., Shao, S., Li, X., Xia, X., Cai, X., Zhou, J., Zhou, Y., Yu, J., Foyer, C.H., Shi, K. (2018). A Plant Phytosulfokine Peptide Initiates Auxin-Dependent Immunity through Cytosolic Ca2+ Signaling in Tomato. Plant Cell 30: 652–667. https://doi.org/10.1105/tpc.17.00537.

Further reading:

Author unknown. What causes a fever? Scientific American. https://www.scientificamerican.com/article/what-causes-a-fever/

AbuQamar, S., Moustafa, K., Tran, L.S. (2017). Mechanisms and strategies of plant defense against Botrytis cinerea. Critical Reviews in Biotechnology 37:262–274. https://doi.org/10.1080/07388551.2016.1271767.

Plant Cell Extracts

Cutting edge research in plant science from The Plant Cell, published by the American Society of Plant Biologists. Background image credit: Tom Donald.

Christian Danve M. Castroverde

Written by

Postdoctoral Research Associate, Michigan State University

Plant Cell Extracts

Cutting edge research in plant science from The Plant Cell, published by the American Society of Plant Biologists. Background image credit: Tom Donald.

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