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Extracellular ATP Functions as an Endogenous External Metabolite Regulating Plant Cell Viability
Stephen Chivasaa,
Bongani K. Ndimbab,
William J. Simonc,
Keith Lindseyc, and
Antoni R. Slabasc,1
a Creative Gene Technology, Integrative Cell Biology Laboratory, School of Biological and Biomedical Sciences, University of Durham, Durham DH1 3LE, United Kingdom b Department of Biotechnology, University of the Western Cape, Bellville, Cape Town, South Africa c School of Biological and Biomedical Sciences, University of Durham, Durham DH1 3LE, United Kingdom
1 To whom correspondence should be addressed. E-mail a.r.slabas{at}durham.ac.uk; fax 44-191-3341295.
Abstract:
ATP is a vital molecule used by living organisms as a universalsource of energy required to drive the cogwheels of intracellularbiochemical reactions necessary for growth and development.Animal cells release ATP to the extracellular milieu, whereit functions as the primary signaling cue at the epicenter ofa diverse range of physiological processes. Although recentfindings revealed that intact plant tissues release ATP as well,there is no clearly defined physiological function of extracellularATP in plants. Here, we show that extracellular ATP is essentialfor maintaining plant cell viability. Its removal by the cell-impermeanttraps glucose–hexokinase and apyrase triggered death inboth cell cultures and whole plants. Competitive exclusion ofextracellular ATP from its binding sites by treatment with ß,-methyleneadenosine5'-triphosphate, a nonhydrolyzable analog of ATP, also resultedin death. The death response was observed in Arabidopsis thaliana,maize (Zea mays), bean (Phaseolus vulgaris), and tobacco (Nicotianatabacum). Significantly, we discovered that fumonisin B1 (FB1)treatment of Arabidopsis triggered the depletion of extracellularATP that preceded cell death and that exogenous ATP rescuesArabidopsis from FB1-induced death. These observations suggestthat extracellular ATP suppresses a default death pathway inplants and that some forms of pathogen-induced cell death aremediated by the depletion of extracellular ATP.
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-methyleneadenosine 5'-triphosphate, a nonhydrolyzable analog of ATP, also resulted in death. The death response was observed in Arabidopsis thaliana, maize (Zea mays), bean (Phaseolus vulgaris), and tobacco (Nicotiana tabacum). Significantly, we discovered that fumonisin B1 (FB1) treatment of Arabidopsis triggered the depletion of extracellular ATP that preceded cell death and that exogenous ATP rescues Arabidopsis from FB1-induced death. These observations suggest that extracellular ATP suppresses a default death pathway in plants and that some forms of pathogen-induced cell death are mediated by the depletion of extracellular ATP. 
