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

Clarissa Lancilli,Giorgio Lucchini,Maurizio Cocucci,Gian Attilio Sacchi,Barbara Giacomini,Fabio Francesco Nocito,Jean-Claude Davidian

doi:10.1186/1471-2229-14-132

Abstract

BackgroundCadmium (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.ResultsThe 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.ConclusionsA 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.

Highlights

Cadmium (Cd) exposure and sulfate limitation induce root sulfate uptake to meet the metabolic demand for reduced sulfur
Cloning and functional characterization of four high-affinity sulfate transporter cDNAs Plant sulfate transporters are encoded by a multi-gene family whose members have specific functions in sulfate acquisition, systemic distribution and subcellular localization [37,38,39]
In this work we identified four sulfate transporter cDNAs expressed in B. juncea roots: one named BjSultr1;1, and three, with closely related sequences, named BjSultr1;2a, BjSultr1;2b and BjSultr1;2c

Summary

Introduction

Cadmium (Cd) exposure and sulfate limitation induce root sulfate uptake to meet the metabolic demand for reduced sulfur. Considering the central role of Cys in sulfur metabolism, it appears evident that both sulfate uptake and the reductive assimilation pathway have to be finely modulated to meet the metabolic demand for sulfur arising from Cys consuming activities, which largely contribute to define the total sulfur requirement of plants Such a demand may consistently vary under the different environmental conditions that plants may experience during their growth. The large amount of PCs produced by Cd stressed plants represents an additional sink for reduced sulfur which, by increasing the metabolic request for both Cys and GSH, generates a typical demanddriven coordinated transcriptional regulation of genes involved in sulfate uptake, sulfate assimilation and GSH biosynthesis Such a response is thought to be essential to satisfy two contrasting needs arising from Cd stress: i) maintaining cell GSH homeostasis; ii) detoxifying heavy metals by means of GSH-consuming activities. A similar activation has been described under sulfate limitation [12,13,14], in this condition plant sulfur needs to sustain the growth do not vary: the induction of sulfate transporters and enzymes along the assimilatory pathway reflects some difficulties in maintaining both an adequate rate of Cys biosynthesis and sulfur-containing compound homeostasis

Methods

Results

Discussion

Conclusion