Iron deprivation results in a rapid but not sustained increase of the expression of genes involved in iron metabolism and sulfate uptake in tomato (Solanum lycopersicum L.) seedlings Anna Rita Paolacci 1 , Silvia Celletti 1 , Giulio Catarcione 1 , Malcolm J. Hawkesford 2 , Stefania Astolfi 1 * and Mario Ciaffi 1 1 DAFNE, University of Tuscia, via S.C. de Lellis 01100, Viterbo, Italy, 2 Rothamsted Research, West Common, Harpenden, Hertfordshire AL5 2JQ, UK. *Correspondence: sastolfi@unitus.it Abstract Characterization of the relationship between sulfur and iron in both Strategy I and Strategy II plants, has proven that low sulfur availability often limits plant capability to cope with iron shortage. Here it was investigated whether the adaptation to iron deficiency in tomato (Solanum lycopersicum L.) plants was associated with an increased root sulfate uptake and translocation capacity, and modified dynamics of total sulfur and thiols accumulation between roots and shoots. Most of the tomato sulfate transporter genes belonging to Groups 1, 2, and 4 were significantly upregulated in iron‐deficient roots, as it commonly occurs under S‐deficient conditions. The upregulation of the two high affinity sulfate transporter genes, SlST1.1 and SlST1.2, by iron deprivation clearly suggests an increased root capability to take up sulfate. Furthermore, the upregulation of the two low affinity sulfate transporter genes SlST2.1 and SlST4.1 in iron‐deficient roots, accompanied by a substantial accumulation of total sulfur and thiols in shoots of iron‐starved plants, likely supports an increased root‐to‐shoot translocation of sulfate. Results suggest that tomato plants exposed to iron‐deficiency are able to change sulfur metabolic balance mimicking sulfur starvation responses to meet the increased demand for methionine and its derivatives, allowing them to cope with this stress. Keywords: Iron; strategy I; sulfate accumulation; sulfate transporters; tomato Citation: Paolacci AR, Celletti S, Catarcione G, Hawkesford MJ, Astolfi S, Ciaffi M (2014) Iron deprivation results in a rapid but not sustained increase of the expression of genes involved in iron metabolism and sulfate uptake in tomato (Solanum lycopersicum L.) seedlings. J Integr Plant Biol 56(XX): 1–13. doi: 10.1111/jipb.12110 Edited by: Toru Fujiwara, University of Tokyo, Japan Received Jul. 10, 2013; Accepted Sept. 17, 2013 Available online on Sept. 30, 2013 at www.wileyonlinelibrary.com/ journal/jipb © 2013 Institute of Botany, Chinese Academy of Sciences INTRODUCTION Iron (Fe) is an essential element for plant growth and development, being required as a redox‐active metal for physiological and metabolic processes including photosynthe- sis, respiration, nitrogen assimilation, hormone biosynthesis, production, and scavenging of reactive oxygen species, osmoprotection, and pathogen defense (Hänsch and Mendel 2009). Despite its abundance in the Earth’s crust, Fe is sparingly soluble under aerobic conditions, especially in high pH and calcareous soils, which account for about 30% of the world’s cultivated soils (Guerinot and Yi 1994). Thus, Fe deficiency is a widespread agricultural problem that hinders plant growth and causes significant yield losses (Mori 1999). As plants are the primary food source for humans, the nutritional state of plants is of central importance to health (Grusak and Dellapenna 1999). According to the World Health Organization, Fe deficiency is one of the most widespread human nutritional disorders in the world affecting over 30% of the world’s population affected (Hind and Guerinot 2012). Thus, increasing the ability of plants to acquire and store Fe will have positive effects on plant and human nutrition. To cope with Fe deficiency, higher plants have developed two distinct Fe acquisition mechanisms, termed Strategy I and Strategy II (Marschner et al. 1986). The Strategy II system is restricted to graminaceous plants, which secrete mugineic acid (MA) family phytosiderophores (PSs) from their roots to chelate and solubilize Fe 3þ in the rhizosphere (Takagi 1976). The Fe 3þ –PS complexes are then taken up by root cells through the action of Yellow Stripe 1 (YS1) proteins (Murata et al. 2006). Strategy I, used by all except graminaceous plants, involves the mobilization of Fe 3þ ions from soil particles by rhizosphere acidification, likely driven by an increase in plasma membrane H þ ATPase activity, the induction of a ferric chelate reductase activity, which allows higher reduction rate of Fe 3þ to Fe 2þ , and the uptake of the resulting Fe 2þ via an Fe 2þ transporter. Arabidopsis and tomato have been widely used as model species to study the Strategy I mechanism (Ivanov et al. 2012). In Arabidopsis the Ferric Reductase Oxidase 2 (FRO2) gene encodes the ferric chelate reductase that reduces Fe at the root–soil interface (Robinson et al. 1999), and the IRON‐ REGULATED TRANSPORTER1 (IRT1) gene encodes a high affinity Fe 2þ transporter, which together mobilize Fe 2þ across the root epidermal plasma membrane into root cells (Vert et al. 2002). AtFRO2 and AtIRT1 are often found co‐regulated (Vert et al. 2003) and their expression is controlled by a bHLH transcription factor named FER‐like Iron‐deficiency Transcription factor (FIT)(Bauer et al. 2007). Putative FRO2, IRT1, and FIT orthologs have been identified in a number of Strategy I species including tomato (see Ivanov et al. 2012 for review). Similarly to FRO2, IRT1 and FIT in Arabidopsis, the functional Free Access Research Article JIPB Journal of Integrative Plant Biology www.jipb.net November 2013 | Volume 56 | Issue XXXX | XXX-XXX