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First published online August 14, 2003; 10.1105/tpc.013516

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The Plant Cell, Vol. 15, 2218-2232, September 2003, Copyright © 2003,
American Society of Plant Biologists

Regulation of Root Ion Transporters by Photosynthesis: Functional Importance and Relation with Hexokinase

Laurence Lejay1,a, Xavier Gansela, Miguel Cerezoa, Pascal Tillarda, Cathrin Müllerb, Anne Krappb, Nicolaus von Wirénc, Françoise Daniel-Vedeled and Alain Gojon2,a

a Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Agro-M/Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique/UM2, 34060 Montpellier Cedex 1, France
b Botanisches Institut der Universität Heidelberg, 69120 Heidelberg, Germany
c Institut für Pflanzenernährung, Universität Hohenheim, 70593 Stuttgart, Germany
d Nutrition Azotée des Plantes, Institut National de la Recherche Agronomique, 78026 Versailles Cedex, France

2 To whom correspondence should be addressed. E-mail gojon{at}ensam.inra.fr; fax 33-4-67-52-57-37

Coordination between the activity of ion transport systems in the root and photosynthesis in the shoot is a main feature of the integration of ion uptake in the whole plant. However, the mechanisms that ensure this coordination are largely unknown at the molecular level. Here, we show that the expression of five genes that encode root NO3-, NH4+, and SO42- transporters in Arabidopsis is regulated diurnally and stimulated by sugar supply. We also provide evidence that one Pi and one K+ transporter also are sugar inducible. Sucrose, glucose, and fructose are able to induce expression of the ion transporter genes but not of the carboxylic acids malate and 2-oxoglutarate. For most genes investigated, induction by light and induction by sucrose are strongly correlated, indicating that they reflect the same regulatory mechanism (i.e., stimulation by photosynthates). The functional importance of this control is highlighted by the phenotype of the atnrt2 mutant of Arabidopsis. In this mutant, the deletion of the sugar-inducible NO3- transporter gene AtNrt2.1 is associated with the loss of the regulation of high-affinity root NO3- influx by light and sugar. None of the sugar analogs used (3-O-methylglucose, 2-deoxyglucose, and mannose) is able to mimic the inducing effect of sugars. In addition, none of the sugar-sensing mutants investigated (rsr1-1, sun6, and gin1-1) is altered in the regulation of AtNrt2.1 expression. These results indicate that the induction of AtNrt2.1 expression by sugars is unrelated to the main signaling mechanisms documented for sugar sensing in plants, such as regulation by sucrose, hexose transport, and hexokinase (HXK) sensing activity. However, the stimulation of AtNrt2.1 transcript accumulation by sucrose and glucose is abolished in an antisense AtHXK1 line, suggesting that HXK catalytic activity and carbon metabolism downstream of the HXK step are crucial for the sugar regulation of AtNrt2.1 expression.




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