Role of extracellular ATP in plants

ATP is a ubiquitous compound in all living cells; it not only provides the energy to drive many biochemical reactions, but also functions in signal transduction as a substrate for kinases, adenylatecyclases, etc. However, ATP was also shown to be an essential signaling agent outside of cells, where it is referred to as extracellular ATP (eATP). An extensive literature exists in animials implicating eATP in numerous cellular processes, including neurotransmission, immune responses, cell growth, and cell death. Initial observations of effects of eATP in animals were met with considerable skepticism. However, this changed when the plasma membrane-localized receptors, purinoceptors of the P2X and P2Y classes, were identified and shown to mediate the effects of eATP.

In contrast, relatively little has been done to examine the role of eATP in plants. However, over the past several years, eATPhas been implicated in a variety of plant processes, including root-hair growth, stress responses, gravitropism, cell viability, pathogen responses and thigmotropism. In previous work from our lab (see picture; Kim et al. 2006), the release of eATP from root cells was directly imaged by using a luciferase construct engineered to bind to plant cell wall cellulose. In our Weerasinghe et al. (2009), we again used this reporter to measure the release of eATP, at levels of 60 nM, from root cells in response to touch. Wounding is known to release uM amounts of eATP. Considering the history with eATP in animals, we sought to identify the receptor for eATP in plants, which lack canonical P2X and P2Y receptors. This work culminated in our recent paper identifying DORN1 (doesn’t respond to nucleotides) as the primary eATP receptor in Arabidopsis (Choi et al., 2015). DORN1 is a lectin receptor-like kinase and, therefore, identifies a new family of purinoreceptors (P2K).

The laboratory is continuing our characterization of DORN1 and other proteins involves in eATP recognition, as well as exploring the role that eATP signaling plays in plant growth and development.

Selected, recent publications from the lab on this topic:

Cao, Yangrong, Kiwamu Tanaka, Cuong T. Nguyen and Gary Stacey (2014) Extracellular ATP is a central signaling molecule in plant stress responses. Curr. Op. Plant Biol. 20: 82-87

Choi, Jeongmin, Tanaka, Kiwamu, Cao, Yangrong, Xi, Yue, Qiu, Jing, Liang, Yan, Sang Yeol Lee, Stacey, Gary (2014) Identification of a plant receptor for extracellular ATP. Science Vol. 343 no. 6168 pp. 290-294

Choi, Jeongmin, Kiwamu Tanaka, Yangrong Cao, Yan Liang, Sang Yeol Lee, and Gary Stacey. (2014) Extracellular ATP, a danger signal, is recognized by DORN1 in Arabidopsis. Biochem. J. 463(3):429-37

Kim, Sung-Yong Kim, MayandiSivaguru and Gary Stacey (2006) Evidence for Extracellular ATP in plants: Localization and functional Significance in root hair growth and signaling Plant Physiol. 142: 984-992

Kiwamu Tanaka, Jeongmin Choi, Yangrong Cao, and Gary Stacey. 2014. Extracellular ATP as a damage associated molecular pattern (DAMP) signal in plants. Frontiers in Plant Science 5:446

Weerasinghe, Ravisha R., Sarah J. Swanson, Seiko Okada, Michele B. Garrett, Sung-Yong Kim, Gary Stacey, Richard C. Boucher, Simon Gilroy, and Alan M. Jones (2009) Theresenitization to-touch set point in Arabidopsis roots is regulated by the heterotrimeric G protein complex. FEBS Lett. 583(15):2521-2526