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Department of Plant Pathology Molecular Plant Pathology Laboratory

Tanaka Lab – Research

 

Extracellular ATP signaling in plant defense – a damaged-self recognition system

Although ATP is generally considered to be the energy currency molecule in the living cell, ATP also acts as a danger signal for damaged-self recognition in multicellular organisms when it is released into the extracellular space following cellular damage. Extracellular ATP is recognized at the cell surface by purinoceptors, evoking immune responses and healing of damage. In animals, the two types of purinoceptor, P2X (ligand gated channel) and P2Y (G-protein coupled receptor), recognize extracellular ATP to activate intracellular signaling cascades, which have been well studied as a therapeutic concept in efforts to dampen pathological inflammation and to control stress responses.

Figure 1. Extracellular ATP, released after cellular damage, acts as a danger signal for plant defense response. Once cytosolic ATP is released into the extracellular milieu (ECM) following cellular damage by enemy attack (e.g., insect herbivory or pathogen infection), ATP acts a danger signal to trigger defense responses. Picture was reproduced from Tanaka et al. (2014) doi:10.3389/fpls.2014.00446.

In plants, a variety of environmental stresses induce release of extracellular ATP, as summarized in a previous review article (Tanaka et al., 2014 doi:10.3389/fpls.2014.00446), suggesting that plants use the ATP molecule to perceive damage. Recently, the first plant purinoceptor was discovered (Choi, Tanaka et al., 2014 doi:10.1126/science.343.6168.290). This receptor, in contrast to animal systems, is a lectin-receptor serine/threonine kinase, named P2K1 (K is for kinase).  Studies of mutants lacking this receptor, demonstrated that extracellular ATP is a signal involved in the plant response to various stresses, including wounding, perhaps to evoke plant defense responses. Interestingly, plant enemies (herbivores and pathogens) are reported to have a strategy to interfere with extracellular ATP signaling by hydrolyzing the molecule. Therefore, extracellular ATP is proposed to act as an initial front-line signal in many plant defense responses (Figure 1). To fully understand the mechanisms by which plants recognize and respond to stress, it is essential to determine the role of extracellular ATP signaling in the plant defense system.

Our long-term goal is to achieve in-depth understanding of the molecular mechanisms mediating extracellular ATP signaling during plant defense responses, both by expanding the current understanding of defense signaling networks, and also by opening new research initiatives into innate immunity. Our hypothesis is that ATP released after cellular damage (e.g., by pathogen or herbivore attacks), triggers an ATP-specific downstream signaling pathway via activation of the P2K receptor, which in turn interacts with other stress hormone signaling pathways to maximize plant immune responses. The objectives of this project are as follows: (1) Elucidation of sensing mechanism of extracellular ATP by the P2K receptor; (2) Identification and functional analysis of molecular components that comprise a complex with, or act downstream of, the P2K receptor; and (3) Identification and characterization of signaling networks between extracellular ATP and other stress hormone signaling pathways, so as to elucidate the important role of extracellular ATP in plant defense response.

Funding sources