Duality of jacalin-related lectin: Master regulator and chaperone

Main text

Lectins have chaperone-like activity with carbohydrate-binding sites, which are key in cellular homeostasis. However, the specific interactions between lectins and endoplasmic reticulum (ER) proteins during stress are unclear. Recently, Das et al. (2023) revealed the critical role of lectins in root-cap stress response through regulating ER stress-responsive proteins, suggesting pathways for enhancing plant resilience.

Structural insights into jacalin-related lectins

Jacalin-related lectins (JRLs) are a diverse family of proteins present in a variety of organisms, ranging from simple to complex (Raval et al., 2004). These proteins share a common structural feature, the jacalin domain, which is composed of a beta-prism motif with three four-stranded anti-parallel beta-sheets (Sankaranarayanan et al., 1996). This specific and complex structure creates a carbohydrate-binding site that allows lectins to selectively bind to carbohydrate molecules (Weis and Drickamer, 1996). The interactions between lectins and carbohydrates are governed by thermodynamic principles, allowing for a reversible binding process that does not permanently change either the lectins or the carbohydrates. This dynamic is a cornerstone of bioenergetics, facilitating essential cellular functions that would naturally occur (Dam et al., 2009). These interactions enable lectins to perform a variety of biological functions, such as facilitating cellular communication and acting as molecular chaperones. In their role as chaperones, lectins can adapt their structure to engage with and stabilize other proteins upon binding to carbohydrate ligands, thus contributing to the maintenance of protein balance within the cell. This chaperone-like function is essential for the cell’s ability to manage stress and preserve protein functionality (De Coninck and Van Damme, 2021).

JRLs in plant defense: Key players in environmental stress responses

In plants, JRLs are also located at strategic sites such as the root cap, poised to detect environmental changes (Das et al., 2023). Their specialized carbohydrate-binding capability may play a critical role in the plant’s initial defense against various challenges, such as soil salinity or pathogen attack (He et al., 2017; Han et al., 2019). The binding of carbohydrates to JRLs can trigger a change in the lectin shape, setting off a chain of cellular signals. This structural shift can enable JRLs to interact with other proteins within the cell, potentially acting as linkers in the assembly of signaling pathways and amplifying signal transduction. Some JRLs have been reported to protect plants from pathogens by mimicking plant carbohydrate receptors or by directly engaging with pathogen-associated molecular patterns to initiate defense mechanisms (Han et al., 2019). They are also implicated in plant growth and response to environmental stresses. For example, the Arabidopsis AtJAC1 gene is involved in regulating the timing of flowering, and rice-derived OsJAC1 responds to DNA damage from gamma radiation, illustrating the role of JRLs in plant development and stress adaptation (Xiao et al., 2015; Jung et al., 2019). Given their involvement in cell signaling and homeostasis, it is reasonable to suggest that JRLs may serve dual purposes: as regulators of gene expression and as stabilizers of protein structure. This dual functionality may warrant categorizing certain lectins as “master regulator chaperones.”

Emerging insights from Das et al.: JRLs in root-cap stress management

Recent research by Das et al. (2023) using single-cell analysis has shed light on the role of JRLs in the root cap. They found that salt-responsive proteins in root-cap cells are either upregulated or translated in response to salt stress. The study identified key components of the salt signaling pathway that are active in the root cap, such as calcium sensors and NADPH oxidases. It also highlighted the importance of proton pumps and ion channels in maintaining ion balance under salt stress. Their findings also demonstrated that root-cap tissues contain a network of proteins, including ER chaperones and components of the unfolded protein response and ER-associated degradation pathways, which are crucial for ion homeostasis and protein management under stress. Of particular interest is JAL10, a protein localized to the ER that activates genes associated with ER stress in response to salt (Figure 1). Plants lacking JAL10 exhibit increased sensitivity to salt stress, as seen in compromised seed germination, reduced root growth, and decreased biomass. Additionally, JAL10 is not only responsive to salt stress but also to ER stress caused by agents such as dithiothreitol, underscoring its broader significance in the ER stress response. The interaction of JAL10 with other proteins indicates a complex interplay between salt stress and ER stress pathways, which is critical for maintaining cellular equilibrium during adverse conditions (Figure 1). The formation of specific protein–protein interaction networks in response to salt stress, particularly in root-cap cells, provides insight into how these cells might rewire their protein interactions to manage the effects of stress (Das et al., 2023).

Figure 1.

Schematic representation of the abiotic stress response in plants.

The diagram illustrates the process by which plants respond to stress. The figure delineates the role of lectins as mitigating agents in alleviating ER stress, thereby contributing to the plant’s adaptive response to stress. Key structural and functional components are detailed, showcasing the molecular and cellular interactions during the stress response. Created with BioRender.com.

Exploring biochemical pathways: The future of JRL research and applications

In the future, investigating the biochemical pathways in which JRLs are involved will be essential. This is particularly important for understanding the functional outcomes of JRLs on protein folding, aggregation, degradation, and post-translational modifications. This research should also focus on the regulatory role of JRLs, exploring how they influence the expression of genes associated with ER stress and the unfolded protein response. The presence of chaperone-like activity in lectins, particularly in their interactions with the ER, indicates an adaptive response to a variety of environmental stressors. Furthermore, the diversity observed in JRLs across different species is a reflection of their adaptive evolution (Raval et al., 2004). This evolutionary process is evident in their unique carbohydrate-binding affinities and functional roles, likely a result of the distinct ways by which lectin genes are organized and regulated within the genome. To gain deeper insights into the molecular adaptation and functional versatility of lectins in response to stress, developing new techniques, such as the quencher-fluorophore system, are invaluable. This system employs a “quencher” molecule that dampens the fluorescence of a “fluorophore” molecule, such as GFP, under normal conditions. However, upon binding to specific carbohydrates, the lectins undergo conformational changes that separate the quencher from the fluorophore, leading to an increase in fluorescence. This change in fluorescence can be directly visualized and quantified, providing insights into the interactions between JRLs and specific carbohydrates during the stress response in plant cells. Such a method allows for the exploration of lectins at the molecular level, which particularly focuses on the structural biology and binding dynamics of JRLs.

Collectively, the study by Das et al. (2023) unveils a complex interaction between JRLs and proteins active during ER stress. The critical role of the ER in protein folding becomes compromised under stress, leading to the accumulation of misfolded proteins and the activation of the unfolded protein response. JRLs, particularly JAL10, play a dual role in this process, both detecting and mitigating the effects of stress to preserve cellular health. Methods such as increasing the expression of JRLs or modifying the carbohydrate-binding domains of JRLs could strengthen or fine-tune the plants’ stress response mechanisms. Furthermore, understanding the specific interplay between JRLs and ER proteins could lead to the identification of stress resistance biomarkers, streamlining breeding programs to rapidly identify resistant/tolerant plant varieties.

Author contributions

G.A. wrote the manuscript.

Published: January 24, 2024