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Open Access Research article

Cadmium exposure and sulfate limitation reveal differences in the transcriptional control of three sulfate transporter (Sultr1;2) genes in Brassica juncea

Clarissa Lancilli1, Barbara Giacomini1, Giorgio Lucchini1, Jean-Claude Davidian2, Maurizio Cocucci1, Gian Attilio Sacchi1 and Fabio Francesco Nocito1*

Author Affiliations

1 Dipartimento di Scienze Agrarie e Ambientali – Produzione, Territorio, Agroenergia, Università degli Studi di Milano, 20133 Milano, Italy

2 Biochimie et Physiologie Moléculaire des Plantes, Unité mixte de recherche, Montpellier SupAgro (Département Biologie et Ecologie), INRA, CNRS, Université de Montpellier 2, 34060 Montpelliercedex 2, France

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BMC Plant Biology 2014, 14:132  doi:10.1186/1471-2229-14-132

Published: 16 May 2014

Abstract

Background

Cadmium (Cd) exposure and sulfate limitation induce root sulfate uptake to meet the metabolic demand for reduced sulfur. Although these responses are well studied, some aspects are still an object of debate, since little is known about the molecular mechanisms by which changes in sulfate availability and sulfur metabolic demand are perceived and transduced into changes in the expression of the high-affinity sulfate transporters of the roots. The analysis of the natural variation occurring in species with complex and highly redundant genome could provide precious information to better understand the topic, because of the possible retention of mutations in the sulfate transporter genes.

Results

The analysis of plant sulfur nutritional status and root sulfate uptake performed on plants of Brassica juncea – a naturally occurring allotetraploid species – grown either under Cd exposure or sulfate limitation showed that both these conditions increased root sulfate uptake capacity but they caused quite dissimilar nutritional states, as indicated by changes in the levels of nonprotein thiols, glutathione and sulfate of both roots and shoots. Such behaviors were related to the general accumulation of the transcripts of the transporters involved in root sulfate uptake (BjSultr1;1 and BjSultr1;2). However, a deeper analysis of the expression patterns of three redundant, fully functional, and simultaneously expressed Sultr1;2 forms (BjSultr1;2a, BjSultr1;2b, BjSultr1;2c) revealed that sulfate limitation induced the expression of all the variants, whilst BjSultr1;2b and BjSultr1;2c only seemed to have the capacity to respond to Cd.

Conclusions

A novel method to estimate the apparent kM for sulfate, avoiding the use of radiotracers, revealed that BjSultr1;1 and BjSultr1;2a/b/c are fully functional high-affinity sulfate transporters. The different behavior of the three BjSultr1;2 variants following Cd exposure or sulfate limitation suggests the existence of at least two distinct signal transduction pathways controlling root sulfate uptake in dissimilar nutritional and metabolic states.

Keywords:
Brassica juncea; Cadmium; Sulfate limitation; High-affinity sulfate transporters