Calcium signaling in plant-microbe interaction

Introduction

Calcium ion (Ca²⁺) is an important second messenger involved in many signaling pathways in plants. The intracellular concentration of Ca²⁺ connects the extracellular stimuli, including the signal of microbes, to intracellular and allow the respond in plants. Since Ca²⁺ cannot be synthesized or degraded by plant, its concentration in the cytoplasm of a plant cell ([Ca²⁺]_cyt) is completely dependent on the entry of external source or release of Ca²⁺ from its intracellular stores. The concentration is regulated tightly by various membrane proteins, such as Ca²⁺ permeable channels, transporters, and Ca²⁺ pumps. Different microbe signals trigger distinctive Ca²⁺ elevation patterns, referred to as Ca²⁺ signature, that can be different from each other from various aspects: amplitude, duration, frequency, spatial distribution, and times of cycle in [Ca²⁺]_cyt changes. The Ca²⁺ signature produced by microbe signal can be decoded by downstream effectors and will result in transcriptional reprogramming of the defense or symbiosis-related genes by the transcription factors, causing different responses by plants.

Detection of Microbes

The detection of microbes by pattern-recognition receptors (PRRs), a type of receptor protein located on the plasma membrane of a plant cell, is the first step of a Ca²⁺ signaling event. PRRs are capable of recognizing microbe-associated molecular patterns (MAMPs), molecules specific to microbes, as well as damage-associated molecular patterns (DAMPs), molecules released by damaged or dying cells of self.

Flagellin-sensitive 2 (FLS2) is an example of PRRs that recognize MAMPs of pathogenic microbes in plants. It recognizes the flagellin protein in bacteria flagellum. Another example is LysM-receptor kinase 5 (LYK5) and chitin elicitor receptor kinase 1 (CERK1) receptor complex, which recognize chitin in the cell wall of fungi.

MAMPs of symbiotic microbes are also detected by PRRs. Rhizobia and mycorrhizal fungi releases Nod factors and Myc factors, and the molecules in them, for example, lipochitooligosaccharides, are recognized by PRRs such as Nod factor perception (NFP), LysM receptor kinase 3/4 (LYK3/4), and symbiosis receptor kinase (DMI2).

DAMPs, which are resulted from pathogen attacks, signifies the present of pathogens and are also recognized by PRRs, including plant endogenous peptide 1 receptor 1 (PEPR1) and PEPR2, and trigger the formation of a Ca²⁺ signature.

Formation of Ca²⁺ Signature

After a PRR’s detection of microbes, it triggers an influx of Ca²⁺ ion from outside the cell, resulting in a unique Ca²⁺ signature. The activated PRRs can either trigger the entry of Ca²⁺ by itself or by activating downstream receptor. If PRRs trigger the influx by itself, there are two possibilities. The first possibility is that it can form a complex with the Ca²⁺ ion channels on the membrane physically and regulate the activity of the channels. The alternative is to produce a signaling molecule binds to Ca²⁺ permeable channels or Ca²⁺ pumps and activate them. The other mechanism is to activate a downstream receptor-like cytoplasmic kinases (RLCKs). The RLCKs then provoke the production of reactive oxygen species (ROS), such as H₂O₂. The ROS interact with Ca²⁺ channels and cause the rise in [Ca²⁺]_cyt.

Decoding of Ca²⁺ Signature

Ca²⁺ signature is decoded by Ca²⁺ sensor proteins. There are various types of sensor proteins in plants, and they respond to the rise in [Ca²⁺]_cyt in two different ways. The first possibility is that Ca²⁺ binds to sensor proteins such as Calmodulin (CaM) and CaM-like proteins (CMLs) and change their structures, enabling them to bind to their targets. They then bind to calcineurin b-like proteins (CBLs). CBLs interact with CBL-interacting protein kinases (CIPKs), an enzyme. The second possible way a sensor can decode the Ca²⁺ Signature is that the sensor has a kinase domain of its own and can phosphorylate other molecules directly. An example of this type of sensor is Ca²⁺-dependent protein kinases (CDPKs or CPKs).

This can cause changes in both transcriptional and post-transcriptional level. At post-transcriptional level, the phosphorylation events by CIPKs, CDPKs or CPKs activate NADPH oxidase in the cell membrane and leads to an increase in the level of ROS production. The ROS produced act as a signaling molecule to promote the influx of Ca²⁺, forming a positive-feedback loop, although its mechanism is not yet known. At transcriptional level, Ca²⁺-modified CaM can bind to transcription factors that promote the transcription of gene related to plant immunity, for example, the gene for synthesize of salicylic acid in plants, causing the whole plant to be ready for pathogen attack.

Ca²⁺ signal as a negative regulator

Although Ca²⁺have been evolved to be utilized as a ubiquitous secondary messenger in plants, it is, by its nature, still a toxin, and long term exposure to high Ca²⁺ level can eventually leads to harm to plant cells, even cell death. So, Ca²⁺ ions cannot keep being present in the cytoplasm. In fact, Ca²⁺ signal can also act as a negative regulator that down regulates the influx of Ca²⁺. It can down regulate it from two processes: formation and decoding of Ca²⁺ signature.

In the formation of Ca²⁺ signature, some CPKs can bind to BIK1, phosphorylate it, thus promoting its degradation and preventing it from

References

Edited by Yueqi Song, student of Joan Slonczewski for BIOL 116 Information in Living Systems, 2021, Kenyon College.