Tandem kinase proteins across the plant kingdom
Plants are an essential part of food production. Worldwide crop production suffers from multiple pathogens, including bacteria, fungi, viruses, protists, and nematodes, which significantly reduce yields. According to the Food and Agriculture Organization, food losses range from 10% to 40% globally each year. Nowadays, chemical methods remain the primary approach for controlling pests and plant diseases. However, chemicals can harm soil fertility, kill beneficial microbes, disrupt soil structure, and lead to pathogen resistance. The most effective long-term solution is to develop crops with built-in resistance genes to these pathogens.
Plant Immunity
How do plants defend themselves from numerous pathogens? Like humans and animals, plants have immune systems that help them recognize and fight off harmful organisms. However, plants lack specialized immune cells that circulate to find and neutralize pathogens. Instead, their immunity relies on specialized receptors acting as molecular sensors. These receptors can detect specific pathogen-associated molecules, which then trigger defense mechanisms.
Plant immunity operates in two primary layers: the first layer is on the cell surface, where receptors recognize external pathogen signals, functioning much like an alarm system for incoming threats. If a pathogen breaches this initial defense, plants activate a second layer of immunity within the cell, responding more specifically to the invader. These intracellular defenders include a unique family of proteins called tandem kinase proteins (TKPs). Our recent research has uncovered remarkable details about this protein family, their evolution and crucial role in plant immunity.
What Sets TKPs Apart?
Protein kinases are one of the largest and oldest groups of enzymes. They evolved as key players in cellular interactomes, forming an integral part in cellular signaling cascades in all life domains. Some organisms learned to exploit their remarkable efficiency as protein binders and adapted this functionality to their specific needs. With such secondary functions taking over, the primary enzymatic role may become obsolete and eventually lost. Such pseudokinases, despite resembling their ancestors, constitute a different actively researched branch of proteins.
An exciting example of such functional plasticity is found in tandem protein kinases (TKPs) recently shown to play a key role in plant immunity. They have a unique architecture containing two or more kinase domains or a combination of kinase and pseudokinase domains. To date, ten experimentally verified tandem kinases were cloned from cereal crops. Seven out of these ten provide resistance to a broad spectrum of pathogen races. Even more impressive is WTK1 that offers resistance to over 2000 genetically and geographically diverse strains of stripe rust, it is a major threat causing significant damage to wheat crops worldwide. Three of the discovered proteins have a non-kinase domain that might be involved in recognizing pathogens proteins. Additionally, one of the experimentally proven TKP contains a transmembrane domain. This suggests that tandem kinases may play a dual role in plant immunity: not only are they involved in intracellular defense, but they also contribute to the first line of defense at the cell membrane.
TKPs Across the Plant Kingdom: A Global Survey
This study demonstrates the widespread occurrence of TKPs across the plant kingdom, as we found TKPs present in every studied species. Our investigation covered 104 plant species, identifying 2,682 TKPs distributed across essential crops such as wheat, rice, and barley, as well as wild and ornamental plants. Remarkably, we discovered the highest number of TKPs—346—in the northern highbush blueberry, while only one TKP was found in sugarcane. This widespread distribution hints at TKPs' vital evolutionary role in plant immunity. We found that tandem kinases can contain up to five kinase domains, but most (90%) have two, similar to those experimentally validated. Half of the dual tandem kinases contain a pseudokinase. These pseudokinases likely act as decoys, luring in pathogen molecules and triggering an immune response. Additionally, 56% of TKPs contain non-kinase domains, they are mostly associated with plant defense systems, such as lectin, leucine-rich repeat, and stress-antifungal domains. Also, nearly a half of discovered TKPs have a transmembrane domain, allowing them to anchor at the cell surface.
Our study provides a crucial resource for data-driven investigations into plant immunity mechanisms, enhancing our understanding of plant immune evolution. Cataloging TKPs across 104 species, we show that these proteins are conserved across the plant kingdom, likely acting as essential immune sensors beyond cereal crops. TKPs have demonstrated resistance to major pathogens, making them promising targets for crop protection research. Our findings also suggest that TKPs evolved independently in various plant species, highlighting their role in adapting to biotic stress.
Looking forward, the next steps involve improved functional characterization of TKPs through experimental approaches, which could reveal new aspects of crop immunity and reduce the need for chemical treatments. By refining our knowledge of TKP functions, we aim to support the development of disease-resistant plants, contributing to safer and more sustainable agricultural practices worldwide.
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