Abstract
In this study the chromate accumulation and tolerance were investigated in Zea mays L. in relation to sulfur availability since sulfate may interact with chromate for
transport into the cells. Chromate inhibited sulfate uptake when supplied to plants
for a short-term period, whereas phosphate uptake remained unchanged. Sulfate absorption
was also reduced in S-starved (-S) and S-supplied (+S) plants treated for 2 d with
0.2 mM chromate and the concomitant repression of the root high-affinity sulfate root
transporter ZmST1;1 transcript accumulation was observed. Conversely, the plasma membrane H+ -ATPase Mha2 was unaffected by chromate in +S plants, allowing to exclude a general effect of
chromate on the active membrane transport. As observed for sulfate uptake, chromate
uptake was enhanced in -S condition and decreased in both +S and -S plants after 2
d of Cr treatment. Chromate reduced the concentration of sulfur and sulfate in +S
plants to the basal level of -S plants, and maximum chromium accumulation was recorded
in S-deprived plants. Analysis of transcript abundance of genes involved in sulfate
assimilation revealed differential regulation by chromate, which was only partly related
to sulfur availability and to the levels of thiols. This work shows for the first
time that chromate specifically represses sulfate uptake, and such repression occurs
without the implication of the candidate regulatory metabolites of the sulfate transport
system in plants.
Key words
Chromate - sulfate - uptake - maize - gene expression - thiols.
References
1
Aldrich M. V., Gardea-Torresdey J. L., Peralta-Videa J. R., Parsons J. G..
Uptake and reduction of Cr(VI) to Cr(III) by Mesquite (Prosopis spp.): chromate-plant interaction in hydroponics and soil media studied using XAS.
Environmental Science and Technology.
(2003);
37
1859-1864
2
Barceló J., Porchenrieder C. H., Ruano A., Gunse B..
Leaf water potential in Cr(VI) treated bean plants (Phaseolus vulgaris L).
Plant Physiology Supplement.
(1985);
77
163-174
3 Barceló J., Poschenrieder C..
Chromium in plants. Canali, S., Tittarelli, F., and Sequi, P., eds. Chromium Environmental Issues. Milan;
Franco Angeli (1997): 101-129
4
Bolchi A., Petrucco S., Tenca P. L., Foroni C., Ottonello S..
Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response
to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine.
Plant Molecular Biology.
(1999);
39
527-537
5
Bradford M. A..
A rapid and sensitive method for the quantification of microgram quantities of protein
utilizing the principle of the protein-dye binding.
Analytical Biochemistry.
(1976);
72
248-254
6
Buchner P., Stuiver C. E. E., Westerman S., Wirtz M., Hell R., Hawkesford M. J., De
Kok L. J..
Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2 S and pedospheric sulfate nutrition.
Plant Physiology.
(2004);
136
3396-3408
7
Cervantes C., Campos-García J., Devars S., Gutiérrez-Corona F., Loza-Tavera H., Torres-Guzmá J. C.,
Moreno-Sánchez R..
Interaction of chromium with microorganisms and plants.
FEMS Microbiology Reviews.
(2001);
25
335-347
8
Frias I., Caldeira M. T., Perez-Castineira J. R., Navarro-Avino J. P., Culianez-Macia F. A.,
Kuppinger O., Stransky H., Pages M., Hager A., Serrano R..
A major isoform of the maize plasma membrane H+ -ATPase: characterization and induction by auxin in coleoptiles.
Plant Cell.
(1996);
8
1533-1544
9
Gardea-Torresdey J. L., De la Rosa G., Peralta-Videa J. R., Montes M., Cruz-Jimenez G.,
Cano-Aguilera I..
Differential uptake and transport of trivalent and hexavalent chromium by Tumbleweed
(Salsola kali) .
Archives of Environmental Contamination and Toxicology.
(2005);
48
225-232
10
Hawkesford M. J..
Plant response to sulphur deficiency and the genetic manipulation of the sulfate transporters
to improve S-utilization efficiency.
Journal of Experimental Botany.
(2000);
51
131-138
11
Hell R., Hillebrand H..
Plant concepts for mineral acquisition and allocation.
Current Opinion in Biotechnology.
(2001);
12
161-168
12
Hirai M. Y., Saito K..
Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur
deficiency.
Journal of Experimental Botany.
(2004);
55
1871-1879
13
Hopkins L., Parmar S., Bouranis D. L., Howarth J. R., Hawkesford M. J..
Coordinated expression of sulfate uptake and components of the sulfate assimilatory
pathway in maize.
Plant Biology.
(2004);
6
408-414
14
Hopkins L., Parmar S., Blaszczyk A., Hesse H., Hoefgen R., Hawkesford M. J..
O -Acetylserine and the regulation of expression of genes encoding components for sulfate
uptake and assimilation in potato.
Plant Physiology.
(2005);
138
433-440
15
Kaszycki P., Gabry H., Appenroth K. J., Jaglarz A., Sedziwy S., Walczak T., Koloczek H..
Exogenously applied sulphate as a tool to investigate transport and reduction of chromate
in the duckweed Spirodela polyrhiza .
Plant, Cell and Environment.
(2005);
28
260-268
16
Kim Y. J., Kim J. H., Lee C. E., Mok Y. G., Choi J. S., Shin H. S., Hwanga S..
Expression of yeast transcriptional activator MSN1 promotes accumulation of chromium
and sulfur by enhancing sulfate transporter level in plants.
FEBS Letters.
(2006);
580
206-210
17
Kleiman I. D., Cogliatti D. H..
Uptake of chromate in sulfate deprived wheat plants.
Environmental Pollution.
(1997);
97
131-135
18
Kotas J., Stasicka Z..
Chromium occurrence in the environment and methods of its speciation.
Environmental Pollution.
(2000);
107
263-283
19
Lappartient A. G., Touraine B..
Glutathione-mediated regulation of ATP sulfurylase activity, SO4
2- uptake, and oxidative stress response in intact canola roots.
Plant Physiology.
(1997);
114
177-183
20
Lindblom S. D., Abdel-Ghany S. E., Hanson B. R., Hwang S., Terry N., Pilon-Smits E. A. H..
Constitutive expression of a high-affinity sulfate transporter in Brassica juncea affects metal tolerance and accumulation.
Journal of Environmental Quality.
(2006);
35
726-733
21
Murphy A., Taiz L..
A new vertical mesh transfer technique for metal-tolerance studies in Arabidopsis (ecotypic variation and copper-sensitive mutants).
Plant Physiology.
(1995);
108
29-38
22
Nocito F. F., Pirovano L., Cocucci M., Sacchi G. A..
Cadmium induced sulfate uptake in maize roots.
Plant Physiology.
(2002);
129
1872-1879
23
Nocito F. F., Lancilli C., Crema B., Fourcoy P., Davidian J.-C., Sacchi G. A..
Heavy metal stress and sulfate uptake in maize roots.
Plant Physiology.
(2006);
141
1138-1148
24
Pilon-Smits E. A. H., Pilon M..
Phytoremediation of metals using transgenic plants.
Critical Reviews in Plant Sciences.
(2002);
21
439-456
25
Pilon-Smits E. A. H..
Phytoremediation.
Annual Review of Plant Biology.
(2005);
56
15-39
26
Quaggiotti S., Abrahamshon C., Malagoli M., Ferrari G..
Physiological and molecular aspects of sulphate uptake in two maize hybrids in response
to S-deprivation.
Journal of Plant Physiology.
(2003);
160
167-173
27
Raskin I., Salt D. E., Smith R. D..
Phytoremediation.
Plant Molecular Biology.
(1998);
49
643-668
28 Sambrook J., Fritsch E. F., Maniatis T.. Molecular Cloning: A Laboratory Manual,
2nd ed. Cold Spring Harbor; Cold Spring Harbor Laboratory Press (1989)
29
Sanger F., Nicklen S., Coulson A. R..
DNA sequence with chain-terminating inhibitors.
Proceedings of the National Academy of Sciences of the USA.
(1977);
74
5463-5467
30
Santi S., Locci G., Monte R., Pinton R., Varanini Z..
Induction of nitrate uptake in maize roots: expression of a putative high-affinity
nitrate transporter and plasma membrane H+ -ATPase isoforms.
Journal of Experimental Botany.
(2003);
54(389)
1851-1864
31
Schachtman D. P., Reid R. J., Ayling S. M..
Phosphorus uptake by plants: from soil to cell.
Plant Physiology.
(1998);
116
447-453
32
Serrano R..
Structure and function of plasma membrane H+ -ATPase.
Annual Review in Plant Physiology and Plant Molecular Biology.
(1989);
40
61-94
33
Sharma D. C., Sharma C. P., Tripathi R. D..
Phytotoxic lesion of chromium in maize.
Chemosphere.
(2003);
51
63-68
34
Shewry P. R., Peterson P. J..
The uptake and transport of chromium by barley seedlings (Hordeum vulgare L.).
Journal of Experimental Botany.
(1974);
25
785-797
35
Skeffington R. A., Shewry P. R., Peterson P. J..
Chromium uptake and transport in barley seedlings (Hordeum vulgare L.)
Planta.
(1976);
132
209-214
36
Smith I. K., Kendall A. C., Keys A. J., Turner J. C., Lea P. J..
Increased levels of glutathione in a catalase-deficient mutant of barley (Hordeum vulgar e L.).
Plant Science Letters.
(1984);
37
29-33
37
Smith F. W., Rae A. L., Hawkesford M. J..
Molecular mechanisms of phosphate and sulphate transport in plants.
Biochimica et Biophysica Acta.
(2000);
1465
236-245
38
Takahashi H., Yamazaki M., Sasakura N., Watanabe A., Leustek T., De Almeida Engler J.,
Engler G., Van Montagu M., Saito K..
Regulation of sulfur assimilation in higher plants: a sulfate transporter induced
in sulfate starved roots plays a central role in Arabidopsis thaliana .
Proceedings of the National Academy of Sciences of the USA.
(1997);
94
11102-11107
39
Vajpayee P., Tripathi R. D., Rai U. N., Ali M. B., Singh S. N..
Chromium (VI) accumulation reduces chorophyll biosynthesis, nitrate reductase activity
and protein content in Nynphaea alba L.
Chemosphere.
(2000);
41
1075-1082
40
Vauclare P., Kopriva S., Fell D., Suter M., Sticher L., von Ballmoos P., Krahenbühl U.,
den Camp R. O., Brunold C..
Flux control of sulphate assimilation in Arabidopsis thaliana : adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase
to negative control by thiols.
The Plant Journal.
(2002);
31
729-740
41
Vázquez M. D., Poschenrieder C. H., Barceló J..
Chromium (VI) induced structural and ultrastructural changes in bush bean plants (Phaseolus vulgaris L.)
Annals of Botany.
(1987);
59
427-438
42
Wirtz M., Droux M., Hell R..
O -acetylserine (thiol)lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited
in Arabidopsis thaliana .
Journal of Experimental Botany.
(2004);
55
1785-1798
43
Zaccheo P., Cocucci M., Cocucci S..
Effects of Cr on proton extrusion, potassium uptake and transmembrane electric potential
in maize root segments.
Plant, Cell and Environment.
(1985);
8
721-726
44
Zayed A. M., Lytle C. M., Qian J. H., Terry N..
Chromium accumulation, translocation and chemical speciation in vegetable crops.
Planta.
(1998);
206
293-299
45
Zayed A. M., Terry N..
Chromium in the environment: factors affecting biological remediation.
Plant and Soil.
(2003);
249
139-156
M. Malagoli
Department of Agricultural Biotechnologies University of Padua
Agripolis
35020 Legnaro (Padua)
Italy
eMail: mario.malagoli@unipd.it
Guest Editor: T. Rausch