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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Iron deficiency induces sulfate uptake and modulates redistribution of reduced sulfur pool in barley plants

Stefania Astolfi A E , Sabrina Zuchi A , Stefano Cesco B , Luigi Sanità di Toppi C , Daniela Pirazzi A , Maurizio Badiani D , Zeno Varanini B and Roberto Pinton B
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A Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, via S. C. de Lellis, 01100 Viterbo, Italy.

B Dipartimento di Scienze Agrarie e Ambientali, Università di Udine, Viale delle Scienze 208, 33100 Udine, Italy.

C Dipartimento di Biologia Evolutiva e Funzionale, Università di Parma, Viale delle Scienze 11 / A, 43100 Parma, Italy.

D Dipartimento di Biotecnologie per il Monitoraggio Agro-alimentare ed Ambientale, Università Mediterranea di Reggio Calabria, Loc. Feo di Vito, 89129 Reggio Calabria, Italy.

E Corresponding author. Email: sastolfi@unitus.it

Functional Plant Biology 33(11) 1055-1061 https://doi.org/10.1071/FP06179
Submitted: 19 July 2006  Accepted: 4 September 2006   Published: 1 November 2006

Abstract

We studied the possibility that the sulfur (S) assimilatory pathway might be modulated by iron (Fe) starvation in barley, as a consequence of plant requirement for an adequate amount of reduced S to maintain methionine and, in turn, phytosiderophore biosynthesis. Barley seedlings were grown with or without 100 µm FeIII–EDTA, at three S levels in the nutrient solution (S2 = 1200, S1 = 60, and S0 = 0 µm sulfate) in order to reproduce conditions of optimal supply, latent and severe deficiency, respectively. Fe deprivation increased root cysteine content irrespective of the S supply. However, this increase was not associated with either higher rates of 35SO42– uptake or increased expression of the gene for the high-affinity sulfate transporter, HvST1, and these roots failed to increase their activities of ATP sulfurylase (ATPS) and O-acetylserine(thiol) lyase (OASTL). We observed a significant increase in 35SO42– uptake rate (+76%) only in Fe-deficient S1 plants and we found an increase in root ATPS activity only in S0 plants. We observed an increase of ATPS enzyme activity in leaves of S1 and S2 plants, most likely suggesting increased S assimilation followed by translocation of thiols (Cys) to the root. Taken together, our results suggest that Fe deficiency affects the partitioning from the shoot to the root of the reduced S pool within the plant and can affect SO42– uptake under limited S supply.

Keywords: iron deficiency, iron uptake, phytosiderophores, Strategy II, sulfur deficiency, thiols.


Acknowledgments

Research was supported by grants from Italian M.I.U.R.-COFIN 2004.


References


Astolfi S, Zuchi S, Passera C, Cesco S (2003) Does the sulfur assimilation pathway play a role in the response to Fe deficiency in maize (Zea mays L.) plants? Journal of Plant Nutrition 26, 2111–2121.
Crossref | GoogleScholarGoogle Scholar | open url image1

Astolfi S, Zuchi S, Cesco S, Varanini Z, Pinton R (2004) Influence of iron nutrition on sulfur uptake and metabolism in maize (Zea mays L.) roots. Soil Science and Plant Nutrition 50, 1079–1083. open url image1

Astolfi S, Cesco S, Zuchi S, Neumann G, Roemheld V (2006) Sulfur starvation reduces phytosiderophores release by Fe-deficient barley plants. Soil Science and Plant Nutrition 52, 80–85. open url image1

Bardsley CE, Lancaster JD (1960) Determination of reserve sulfur and soluble sulfate in soils. Soil Science Society American Proceedings 24, 265–268. open url image1

Bouranis DL, Chorianopoulou SN, Protonotarios VE, Siyannis VF, Hopkins L, Hawkesford MJ (2003) Leaf response of young iron-inefficient maize plants to sulfur deprivation. Journal of Plant Nutrition 26, 1189–1202.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buchner P, Stuiver EE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiology 136, 3396–3408.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

De Knecht JA, Van Dillen M, Koevoets PLM, Schat H, Verkleij JAC, Ernst WHO (1994) Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris: chain length distribution and sulphide incorporation. Plant Physiology 104, 255–261.
PubMed |
open url image1

Ferretti M, Ghisi R, Merlo L, Dalla Vecchia F, Passera C (1993) Effect of cadmium on photosynthetic sulfate and nitrate assimilation. Photosynthetica 29, 49–54. open url image1

Hawkesford MJ (2003) Transporter gene families in plants: the sulfate transporter gene family — redundancy or specialization? Physiologia Plantarum 117, 155–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hawkesford MJ , Smith FW (1997) Molecular biology of higher plant sulfate transporters. In ‘Sulfur metabolism in higher plants’. (Eds WJ Cram, LJ De Kok, I Stulen, C Brunold, H Rennenberg) pp. 13–25. (Backhuys Publishers: Leiden)

Hawkesford MJ, Wray JL (2000) Molecular genetics of sulfur assimilation. Advances in Botanical Research 33, 159–223. open url image1

Herschbach C, Pilch B, Tausz M, Rennenberg H, Grill D (2002) Sulfate uptake and xylem loading of young pea (Pisum sativum L.). Plant and Soil 242, 227–233.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hesse H, Hoefgen R (2003) Molecular aspects of methionine biosynthesis. Trends in Plant Science 8, 259–262.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. The Plant Cell 16, 2693–2704.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kuwajima K , Kawai S (1997) Relationship between sulfur metabolism and biosynthesis of phytosiderophores in barley roots. In ‘Plant nutrition for sustainable food production and environment’. (Eds T Ando, K Fujita, T Mae, H Matsumoto, S Mori, J Sekiya) pp. 285–286. (Kluwer Academic Publishers: The Netherlands)

Ma JF, Shinada T, Matsuda C, Kyosuke NJ (1995) Biosynthesis of phytosiderophores, mugineic acid, associated with methionine cycle. Biological Chemistry 270, 16549–16554.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marschner H, Römheld V (1994) Strategies of plant acquisition of iron. Plant and Soil 165, 261–274.
Crossref | GoogleScholarGoogle Scholar | open url image1

McGrath SP, Zhao FJ (1995) A risk assessment of sulfur deficiency in cereals using soil and atmospheric deposition data. Soil Use and Management 11, 110–114. open url image1

Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in Gramineae plants. Plant & Cell Physiology 28, 1081–1092. open url image1

Nakanishi H, Bughio N, Matsuhashi S, Ishioka NS, Uchida H, Tsuji A, Osa A, Sekine T, Kume T, Mori S (1999) Visualizing real time [11C] methionine translocation in Fe-sufficient and Fe-deficient barley using a positron emitting tracer imaging system (PETIS). Journal of Experimental Botany 50, 637–643.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neves-Piestun BG, Bernstein N (2005) Salinity-induced changes in the nutritional status of expanding cells may impact leaf growth inhibition in maize. Functional Plant Biology 32, 141–152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ravanel S, Gakière B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proceedings of the National Academy of Sciences USA 95, 7805–7812.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytologist 127, 635–674.
Crossref | GoogleScholarGoogle Scholar | open url image1

Romera FJ, Alcantara E (2004) Ethylene involvement in the regulation of Fe-deficiency stress responses by Strategy I plants. Functional Plant Biology 31, 315–328.
Crossref | GoogleScholarGoogle Scholar | open url image1

Römheld V (1987) Different strategies for iron acquisition in higher plants. Physiologia Plantarum 70, 231–234.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schmutz D, Brunold C (1982) Rapid and simple measurement of ATP sulfurylase activity in crude plant extracts using an ATP meter for bioluminescence determination. Analytical Biochemistry 121, 151–155.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher AR, Warrilow AGS (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter. The Plant Journal 12, 875–884.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith FW , Cybinski D , Rae AL (1999) Regulation of expression of genes encoding phosphate transporters in barley roots. In ‘Plant nutrition — molecular biology and genetics’. (Eds G Gissel-Nielsen, A Jensen) pp. 145–150. (Kluwer Academic Publishers: Dordrecht)

Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant and Soil 248, 71–83.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhang FS, Römheld V, Marschner H (1991) Role of the root apoplasm for iron acquisition by wheat plants. Plant Physiology 97, 1302–1305.
PubMed |
open url image1