Futile Transmembrane NH4 +Cycling: A Cellular Hypothesis to Explain Ammonium Toxicity in Plants
Most higher plants develop severe toxicity symptoms when grown on ammonium (NH4 +) as the sole nitrogen source. Recently, NH4 +toxicity has been implicated as a cause of forest decline and even species extinction. Although mechanisms underlying NH4 +toxicity... Ausführliche Beschreibung
|1. Person:||Britto, Dev T.|
|Weitere Personen:||Siddiqi, M. Yaeesh verfasserin; Kronzucker, Herbert J. verfasserin|
in Proceedings of the National Academy of Sciences of the United States of America Vol. 98, No. 7 (2001), p. 4255-4258
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Copyright: Copyright 1993-2001 National Academy of Sciences of the United States of America
Most higher plants develop severe toxicity symptoms when grown on ammonium (NH4 +) as the sole nitrogen source. Recently, NH4 +toxicity has been implicated as a cause of forest decline and even species extinction. Although mechanisms underlying NH4 +toxicity have been extensively sought, the primary events conferring it at the cellular level are not understood. Using a high-precision positron tracing technique, we here present a cell-physiological characterization of NH4 +acquisition in two major cereals, barley (Hordeum vulgare), known to be susceptible to toxicity, and rice (Oryza sativa), known for its exceptional tolerance to even high levels of NH4 +. We show that, at high external NH4 +concentration ([NH4 +] o), barley root cells experience a breakdown in the regulation of NH4 +influx, leading to the accumulation of excessive amounts of NH4 +in the cytosol. Measurements of NH4 +efflux, combined with a thermodynamic analysis of the transmembrane electrochemical potential for NH4 +, reveal that, at elevated [NH4 +] o, barley cells engage a high-capacity NH4 +-efflux system that supports outward NH4 +fluxes against a sizable gradient. Ammonium efflux is shown to constitute as much as 80% of primary influx, resulting in a never-before-documented futile cycling of nitrogen across the plasma membrane of root cells. This futile cycling carries a high energetic cost (we record a 40% increase in root respiration) that is independent of N metabolism and is accompanied by a decline in growth. In rice, by contrast, a cellular defense strategy has evolved that is characterized by an energetically neutral, near-Nernstian, equilibration of NH4 +at high [NH4 +] o. Thus our study has characterized the primary events in NH4 +nutrition at the cellular level that may constitute the fundamental cause of NH4 +toxicity in plants.