Sulphur deprivation limits Fe-deficiency responses in tomato plants

Abstract

The aim of this work was to clarify the role of S supply in the development of the response to Fe depletion in Strategy I plants. In S-sufficient plants, Fe-deficiency caused an increase in the Fe(III)-chelate reductase activity, 59Fe uptake rate and ethylene production at root level. This response was associated with increased expression of LeFRO1 [Fe(III)-chelate reductase] and LeIRT1 (Fe2+ transporter) genes. Instead, when S-deficient plants were transferred to a Fe-free solution, no induction of Fe(III)-chelate reductase activity and ethylene production was observed. The same held true for LeFRO1 gene expression, while the increase in 59Fe2+ uptake rate and LeIRT1 gene over-expression were limited. Sulphur deficiency caused a decrease in total sulphur and thiol content; a concomitant increase in 35SO4(2-) uptake rate was observed, this behaviour being particularly evident in Fe-deficient plants. Sulphur deficiency also virtually abolished expression of the nicotianamine synthase gene (LeNAS), independently of the Fe growth conditions. Sulphur deficiency alone also caused a decrease in Fe content in tomato leaves and an increase in root ethylene production; however, these events were not associated with either increased Fe(III)-chelate reductase activity, higher rates of 59Fe uptake or over-expression of either LeFRO1 or LeIRT1 genes. Results show that S deficiency could limit the capacity of tomato plants to cope with Fe-shortage by preventing the induction of the Fe(III)-chelate reductase and limiting the activity and expression of the Fe2+ transporter. Furthermore, the results support the idea that ethylene alone cannot trigger specific Fe-deficiency physiological responses in a Strategy I plant, such as tomato.

Ethylene and the Regulation of Physiological and Morphological Responses to Nutrient Deficiencies

“…In the last 10 years, increased ethylene production by roots and/or shoots has been described for other nutrient deficiencies, such as K (Shin and Schachtman, 2004;Benlloch-González et al, 2010), S (Zuchi et al, 2009;Moniuszko et al, 2013), N (Zheng et al, 2013), and Mg (Hermans et al, 2010). The higher ethylene production described for nutrient deficiencies has been further supported by results showing up-regulation of genes implicated in ethylene synthesis.…”

Interaction between the bHLH Transcription Factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 Reveals Molecular Linkage between the Regulation of Iron Acquisition and Ethylene Signaling in Arabidopsis

“…We propose from our results that inactive and active FIT proteins are not stable inside cells and can be degraded, indicated by arrows pointing to ellipses with light gray-white shading. Fe deficiency leads to ethylene production (Romera et al, 1999;Zuchi et al, 2009). EIN3/ EIL1 activated in the ethylene signaling pathway physically interact with FIT, which inhibits proteasomal degradation of FIT (EIN3/EIL1 are represented as dark-gray ellipses; FIT binding to EIN3/EIL1 does not involve the bHLH domain of FIT).…”

“…Experiments with the plant hormone ethylene in different dicot plants indicated a physiological connection between ethylene and iron deficiency signaling. Ethylene is produced upon Fe deficiency (Romera et al, 1999;Zuchi et al, 2009). Applying ethylene precursors such as 1-aminocyclopropane-1-carboxylic acid or ethephon to plants could mimic morphological growth responses of Fe-deficient plants (Romera and Alcantara, 1994;Schmidt et al, 2000).…”

The interplay between sulfur and iron nutrition in tomato

“…Previously, Zuchi et al (2009) showed that, in tomato plants exposed to both S and Fe starvation, no induction of Fe(III)-chelate reductase activity and ethylene production occurred. Thus, S deficiency seems to prevent the development of the typical responses to Fe deficiency in tomato.…”

“…Recently, it was shown that the iron (Fe) use efficiency in maize (Zea mays; Astolfi et al, 2003;Bouranis et al, 2003), barley (Hordeum vulgare; Kuwajima and Kawai, 1997;Astolfi et al, 2006a), tomato (Solanum lycopersicum; Zuchi et al, 2009), and durum wheat (Triticum durum; Zuchi et al, 2012;Ciaffi et al, 2013) increased under adequate S supply. In these studies, it has been suggested that, in grasses (strategy II plants), this effect could be ascribed to a decrease in the production and release of phytosiderophores induced by S deficiency, whereas in tomato (a strategy I plant), the effect was rather caused by an impaired ethylene and nicotianamine (NA) production.…”