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

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.

The interplay between sulfur and iron nutrition in tomato

“…The expression of both SlFRO1 and SlIRT1 genes is controlled by the basic helix-loop-helix (bHLH) transcription factor SlFER. Their expression was detected only in roots under all nutritional conditions analyzed, and as previously described (Paolacci et al, 2014), the relative amounts of their transcripts in roots of control plants were markedly different (Fig. 4).…”

“…The expression of genes involved in Fe homeostasis (SlFRO1, SlIRT1, and SlFER) and coding for STs of groups 1, 2, and 4 (SlST1.1, SlST1.2, SlST2.1, SlST2.2, and SlST4.1) were analyzed by qRT-PCR as described in Paolacci et al, 2014. In particular, qRT-PCR analyses were performed using an Mx3000PTM Real-Time PCR System with Brilliant SYBR Green QPCR Master Mix (STRA-TAGENE) according to manufacturer's protocols in 25-mL reaction volumes containing 1 mL of each 5-fold diluted cDNA and 150 nM forward and reverse primers (reported for each analyzed gene in Paolacci et al, [2014]).…”

“…In particular, qRT-PCR analyses were performed using an Mx3000PTM Real-Time PCR System with Brilliant SYBR Green QPCR Master Mix (STRA-TAGENE) according to manufacturer's protocols in 25-mL reaction volumes containing 1 mL of each 5-fold diluted cDNA and 150 nM forward and reverse primers (reported for each analyzed gene in Paolacci et al, [2014]). Standard curves based on five points, corresponding to a 5-fold dilution series (1:1-1:625) from pooled cDNA, were used to compute the PCR efficiency of each primer pair.…”

“…Thus, S deficiency seems to prevent the development of the typical responses to Fe deficiency in tomato. However, it was also recently shown that Fe deficiency significantly up-regulated most of the sulfate transporter (ST) genes belonging to groups 1, 2, and 4 in tomato roots (Paolacci et al, 2014). This interaction between S and Fe triggers the activation of complex response mechanisms to assumingly maintain plant primary metabolism function and maintain adequate levels of Cys, Met, and their derivatives as well as Fe-S clusters as essential building blocks of various enzymes.…”

A Program for Iron Economy during Deficiency Targets Specific Fe Proteins

“…It is of interest to place our findings in the context of studies that have reported on the general effects of Fe deficiency on chlorophyll synthesis and photosynthesis that have been well documented in the literature (Spiller and Terry, 1980;Andaluz et al, 2006;Nishio and Terry, 1983;Nishio et al, 1985;Sharma, 2007;Timperio et al, 2007;Laganowski et al, 2009;Msilini et al, 2011;Ciaffi et al, 2013;Paolacci et al, 2014;Rodríguez-Celma et al, 2013). Some studies on Fe depletion in plants reported that PSI was the major target of Fe deficiency (Nishio et al, 1985;Timperio et al, 2007), whereas we saw a major effect on the cytochromeb 6 f complex and less on PSI.…”