Sulfur Metabolism and Stress Defense Responses in Plants

Tropical Plant Biology - Tập 8 - Trang 60-73 - 2015
Flávia R. Capaldi1, Priscila L. Gratão2, André R. Reis3, Leonardo W. Lima2, Ricardo A. Azevedo1
1Departamento de Genética, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, Piracicaba, Brazil
2Departamento de Biologia Aplicada à Agropecuária, Faculdade de Ciências Agrárias e Veterinárias, UNESP - Univ Estadual Paulista, Jaboticabal, Brazil
3Engenharia de Biossistemas, UNESP - Univ Estadual Paulista, Tupã, Brazil

Tóm tắt

Sulfur management is an important issue in crop plant nutrition. Sulfur has a role in fundamental processes such as electron transport, structure and regulation. It is also associated with photosynthetic oxygen production, abiotic and biotic stress resistance and secondary metabolism. Sulfate uptake, reductive assimilation and integration into cysteine and methionine are the central processes that direct oxidized and reduced forms of organically bound S into their various functions. Sulfur-containing defense compounds that are crucial for plant survival during biotic and abiotic stress include elemental sulfur, hydrogen sulfide, glutathione, phytochelatins, S-rich proteins and various secondary metabolites. Formation of these compounds in plants is closely related to the supply, demand, uptake and assimilation of S. This review will highlight the role of S during the stress response in plants and the relationship between S metabolism and primary S nutrition.

Tài liệu tham khảo

Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249 Al-Whaibi MH, Siddiqui MH, Basalah MO (2012) Salicylic acid and calcium induced protection of wheat against salinity. Protoplasma 249:769–778 Arruda MAZ, Azevedo RA (2009) Metallomics and chemical speciation: towards a better understanding of metal-induced stress in plants. Ann Appl Biol 155:301–307 Azevedo RA, Arruda P, Turner WL, Lea PJ (1997) The biosynthesis and metabolism of the aspartate derived amino acids in higher plants. Phytochemistry 46:395–419 Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase deficient mutant of barley. Physiol Plant 104:280–292 Azevedo RA, Lancien M, Lea PJ (2006) The aspartic acid metabolic pathway, an exciting and essential pathway in plants. Amino Acids 30:143–162 Azevedo RA, Carvalho RF, Cia MC, Gratão PL (2011) Sugarcane under pressure: an overview of biochemical and physiological studies of abiotic stress. Trop Plant Biol 4:42–51 Becher M, Talke IN, Krall L, Kramer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268 Bell L, Wagstaff C (2014) Glucosinolates, myrosinase hydrolysis products, and flavonols found in rocket (Eruca sativa and Diplotaxis tenuifolia). J Agric Food Chem 62:4481–4492 Biswal B, Raval MK, Biswal UC, Joshi P (2008) Response of photosynthetic organelles to abiotic stress: modulation by sulphur metabolism. In: Khan A, Singh S, Umar S (eds) Sulphur assimilation and abiotic stress in plants. Springer-Verlag, Berlin, pp 167–191 Bitrián M, Zarza X, Altabella T, Tiburcio AF, Alcázar R (2012) Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites 2:516–528 Boaretto LF, Carvalho G, Borgo L, Creste S, Landell MGA, Mazzafera P, Azevedo RA (2014) Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes. Plant Physiol Biochem 74:166–175 Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana ABSICISIC ACID-INSENSITIVE8 encodes a novel protein mediating absicisic acid and sugar responses essential for growth. Plant Cell 16:406–421 Buchner P, Takahashi H, Hawkesford M (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long distance transport. J Exp Bot 55:1765–1773 Bulbovas P, Souza SR, Esposito JBN, Moraes RM, Alves ES, Domingos M, Azevedo RA (2014) Assessment of the ozone tolerance of two soybean cultivars (Glycine max cv. Sambaíba and Tracajá) cultivated in Amazonian areas. Environ Sci Pollut Res 21:10514–10524 Bürstenbinder K, Sauter M (2012) Early events in the ethylene biosynthetic pathway – regulation of the pools of methionine and S-adenosylmethionine. Ann Plant Rev 44:19–52 Carfagna S, Vona V, Di Martino V, Esposito S, Rigano C (2011) Nitrogen assimilation and cysteine biosynthesis in barley: evidence for root sulphur assimilation upon recovery from N deprivation. Environ Exp Bot 71:18–24 Carvalho RF, Campos ML, Azevedo RA (2011) The role of phytochrome in stress tolerance. J Integr Plant Biol 53:920–929 Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29 Choppala G, Saifullah Bolan N, Bibi S, Igbal M, Rengel Z, Kunhikrishnan A, Ashwath N (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391 Cia MC, Guimarães ACR, Medici LO, Chabregas SM, Azevedo RA (2012) Antioxidant responses to water deficit by drought-tolerant and - sensitive sugarcane varieties. Ann Appl Biol 161:313–324 Davidian JC, Kopriva S (2010) Regulation of sulphate uptake and assimilation – the same or not the same? Mol Plant Adv 3:314–325 De Bona FD, Fedoseyenko D, von Wirén N, Monteiro FA (2011) Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form. Environ Exp Bot 74:237–244 Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy AS, Poovaiah BW (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158 Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143 Fatma M, Khan MIR, Masood A, Khan NA (2013) Coordinate changes in assimilatory sulfate reduction are correlated to salt tolerance: involvement of phytohormones. Ann Rev Res Biol 3:267–295 Foyer CH, Noctor G (2012) Managing the cellular redox hub in photosynthetic organisms. Plant Cell Environ 35:199–201 Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100 Francois JA, Kumaran S, Jez JM (2006) Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18:3647–3655 Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46 García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984 Gfeller A, Baerenfaller K, Loscos J, Chételat A, Baginsky S, Farmer EE (2011) Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol 156:1797–1807 Ghelfi A, Gaziola SA, Cia MC, Chabregas SM, Falco MC, Kuser-Falcão PR, Azevedo RA (2011) Cloning, expression, molecular modelling and docking analysis of glutathione transferase from Saccharum officinarum. Ann Appl Biol 159:267–280 Gojon A, Nacry P, Davidian JC (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Curr Opin Plant Biol 12:328–338 Gotor C, Laureano-Marin AM, Moreno I, Aroca A, Garcia I, Romero LC (2014) Signaling in plant cytosol: cysteine or sulfide? Amino Acids 14:1–10 Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy-metal stressed plants a little easier. Funct Plant Biol 32:481–494 Gratão PL, Monteiro CC, Antunes AM, Peres LEP, Azevedo RA (2008) Acquired tolerance of tomato (Lycopersicon esculentum cv. Micro-Tom) plants to cadmium-induced stress. Ann Appl Biol 153:321–333 Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissecation of diageotropica and never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96 Gu CS, Liu LQ, Zhao YH, Deng YM, Zhu XD, Huang SZ (2014) Overexpression of Iris. lactea var. Chinensis metallothionein IIMT2a enhances cadmium tolerance in Arabidopsis thaliana. Ecotoxicol Environ Saf 105:22–28 Guo RF, Shen WS, Qian HM, Zhang M, Liu LH, Wang QM (2013) Jasmonic acid and glucose synergistically modulate the accumulation of glucosinolates in Arabidopsis thaliana. J Exp Bot 64:5707–5719 Halkier B, Geshenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333 Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000) β-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1171 Hawkesford MJ (2005) Sulphur. In: Broadley MR, White PJ (eds) Plant nutritional genomics, 1st edn. Dordrecht Hawkesford MJ (2012) Sulfate uptake and assimilation – whole plant regulation. Proc Int Plant Sulfur Workshop 1:11–24 Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395 Hell R, Kruse C (2006) Sulfur in biotic interactions of plants. In: Hawkesford MJ, De Kok JP (eds) Sulfur in plant: an ecological perspective. Springer, 264p Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette MLM, Cuine S, Aurov P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1754–1768 Hesse H, Trachsel N, Suter M, Kopriva S, von Ballooms P, Rennemberg H, Brunold C (2003) Effect of glucose on assimilatory sulfate reduction in roots of Arabidopsis thaliana. J Exp Bot 54:1701–1709 Hossain Z, Komatsu (2013) Contribution of proteomic studies towards understanding plant heavy metal stress responses. Front Plant Sci 3:1–12 Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311 Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient-tobacco plants. Environ Exp Bot 109:201–211 Iqbal N, Masood A, Iqbal M, Khan R, Asgher M, Fatma M, Khan NA (2013) Cross-talk between sulfur assimilation and ethylene signaling in plants. Plant Signal Behav 8:104–112 Jacob C, Anwar A (2008) The chemistry behind redox regulation with focus on sulphur redox systems. Physiol Plant 133:469–480 Jamal A, Fazli IS, Ahmad S, Kim KT, Oh DG, Abdin MZ (2006) Effect of sulfur on nitrate reductase and ATP sulfurylase activities in groundnut (Arachis hypogea L.). J Plant Biol 49:513–517 Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 44:481–486 Jobe TO, Sung DY, Akmakijan G, Pham A, Komives EA, Mendoza-Cózatil DG, Schroeder JI (2012) Feedback inhibition by thiols outranks glutathione depletion: a luciferase-based screen reveals glutathione-deficient γ-ECS and glutathione synthetase mutants impaired in cadmium-induced sulfate assimilation. Plant J 70:783–795 Josefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defences. Int J Mol Sci 13:3145–3175 Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hahnel U, Hansch R, Hartmann T, Kopriva S, Kruse C, Mendel RR, Papenbrock J, Reichel M, Rennenberg H, Schnug E, Schmidt A, Textor S, Tokuhita J, Wachter A, Wirtz M (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulphur-related pathways in Arabidopsis thaliana. Photosynth Res 86:491–508 Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K, Takahashi T, Koptiva S (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876 Khan NA, Mir, Nazar R, Singh S (2008) The application of ethephon (an ethylene releaser) increases growth, photosynthesis and nitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. Plant Biol 10:534–538 Khorshidi MB, Yarnia M, Hassanpanah D (2009) Salinity effects on nutrients accumulation in alfafa shoots in hydroponic condition. J Food Agric Environ 7:787–790 Klein M, Papenbrock J (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J Exp Bot 55:1809–1820 Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495 Kopriva S, Rennenberg H (2004) Control of sulfate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842 Koprivova A, Kopriva S (2014) Molecular mechanisms of regulation of sulphate assimilation: first steps on a long road. Front Plant Sci 5:1–11 Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746 Koralewska A, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2008) Regulation of sulfate uptake, expression of the sulfate transporters Sultr1;1 and Sultr1;2, and APS reductase in Chinese cabbage (Brassica pekinensis) as affected by atmospheric H2S nutrition and sulfate deprivation. Funct Plant Biol 35:318–327 Krischan J, Makaruk A, Harasek M (2012) Design and scale-up of an oxidative scrubbing process for the selective removal of hydrogensulfide from biogas. J Hazard Mater 215:49–56 Kruse J, Kopriva S, Hansch R, Krauss GJ, Mendel RR, Rennemberg H (2007) Interaction of sulfur and nitrogen nutrition in tobacco (Nicotiana tabacum) plants: significance of nitrogen source and root nitrate reductase. Plant Biol 9:638–646 Leung SCS, Smith D, Chen R, McCallum JA, McKenzie M, McManus MT (2006) Characterization of adenosine 5′-phospho-sulfate kinase (APSK) genes from higher plants. In: De Kok LJ, Rennenber H, Hawkesford J (eds) Sulfur metabolism in plants, pp 67–70 Lewandowska M, Sirko A (2008) Recent advances in understanding plant response to sulphur-deficiency stress. Acta Biochim Pol 55:457–471 Li ZG, Gong M, Xie H, Yang L, Li J (2012) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185:185–189 Li H, Yan SH, Zhao L, Tan JJ, Zhang Q, Gao F, Wang P, Hou HL, Li LJ (2014) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 105:1–14 Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935 Lisjak M, Teklic T, Wilson ID, Wood ME, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6:1444–1446 Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616 Lunde C, Zygadlo A, Simonsen HT, Nielsen PL, Blennow A, Haldrup A (2008) Sulphur starvation in rice: the effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. Physiol Plant 133:508–521 Ma XL, Wang ZL, Qi YC, Zhao YX, Zhang H (2003) Isolation of S-adenosylmethionine synthase gene from Suadea salsa and its differential expression under NaCl stress. Acta Bot Sin 45:1359–1365 Magrath R, Mithen R (1993) Maternal effects on the expression of individual aliphatic glucosinolates in seed and seedlings of Brassica napus. Plant Breed 111:249–252 Majic DB, Samardzic JT, Milisavljevic MD, Krstic AM, Maksimovic VR (2008) Two metallothionein gene family members in buckwheat: expression analysis in flooding stress using Real Time RT-PCR technology. Arch Biol Sci 60:77–82 Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Yamaya T, Takahashi H (2004) Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol 45:340–345 Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314 Mazid M, Khan TM, Mohammad F (2011) Response of crop plants under sulphur stress tolerance. J Stress Physiol Biochem 7:25–57 Medici LO, Reinert F, Carvalho DF, Kozak M, Azevedo RA (2014) What about keeping plants well watered? Environ Exp Bot 99:38–42 Mendoza-Cozatl D, Loza-Tavera H, Hernandez-Navarro A, Moreno-Sanchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671 Mera R, Torres E, Abalde J (2014) Sulphate more than a nutrient protects the microalga Chlamydomonas moewusii from cadmium toxicity. Aquat Toxicol 148:92–103 Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezotto T, Medici LO, Peres LEP, Azevedo RA (2011) Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses. Environ Exp Bot 71:306–320 Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R, Gigolashvili T, Flugge UI, Wasternack C, Gershenzon J, Hell R, Saito K, Kopriva S (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfate secondary metabolites. Plant Cell 21:910–927 Mugford SG, Mattewman CA, Hill L, Kopriva S (2010) Adenosine-5′-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett 584:119–123 Muneer S, Lee BR, Kim KY, Park SH, Zhang Q, Kim TH (2014) Involvement of sulphur nutrition in modulating iron deficiency responses in photosynthetic organelles of oilseed rape (Brassica napus L.). Photosynth Res 119:319–329 Na G, Salt DE (2011) The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Environ Exp Bot 72:18–25 Nazar R, Iqbal N, Syeed S, Khan NA (2011a) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815 Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011b) Understanding the significance of sulfur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87 Negishi M, Pedersen LG, Petrotchenko E, Shevtsov S, Gorokhov A, Kakuta Y, Pedersen LC (2001) Structure and function of sulfotransferases. Arch Biochem Biophys 390:149–157 Noctor G (2006) Metabolic signaling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425 Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484 Nogueirol RC, Monteiro FA, Gratão PL, Borgo L, Azevedo RA (2015) Tropical soils with high aluminum concentrations cause oxidative stress in two tomato genotypes. Environ Monit Assess 187:73 Paiva LB, de Oliveira JG, Azevedo RA, Ribeiro DR, da Silva MG, Vitoria AP (2009) Ecophysiological responses of water hyacinth exposed to Cr3+ and Cr6+. Environ Exp Bot 65:403–409 Pál M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defence mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246 Pál M, Kovács V, Szalai G, Soós V, Ma X, Liu H, Mei H, Janda T (2014) Salicylic acid and abiotic stress responses in rice. J Agron Crop Sci 200:1–11 Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295 Qureshi MI, Qadir S, Zolla L (2007) Proteomics-based dissection of stress-responsive pathways in plants. J Plant Physiol 164:1239–1260 Rahoui S, Ben C, Chaoui A, Martinez Y, Yamchi A, Rickauer M, Gentzbittel L, Ferjani EE (2014) Oxidative injury and antioxidant genes regulation in cadmium-exposed radicles of six contrasted Medicago truncatula genotypes. Environ Sci Pollut Res 21:8070–8083 Rausch T, Watcher A (2005) Sulphur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509 Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci U S A 95:7805–7812 Rennenberg H, Herschbach C (2012) Sulphur compounds in multiple compensation reactions of abiotic stress responses. Sulphur Metabolism in Plants. Proc Int Plant Sulphur Workshop 1:203–215 Riemenschneider A, Wegele R, Schimidt A, Papenbrock J (2005) Isolation and characterization of a D-cysteine desulphydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304 Roy M, Wu R (2002) Overexpression of S-adenosylmethionine descarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992 Ruiz JM, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969 Salvagiotti F, Castellarín JM, Miralles DJ, Pedrol HM (2009) Sulfur fertilization improves nitrogen use efficiency in wheat by increasing nitrogen uptake. Field Crop Res 113:170–177 Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamita K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668 Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69 Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346 Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139 Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14 Shulaev V, Cortesa D, Millerb G, Mittlerb R (2008) Metabolomics for plant stress response. Physiol Plant 132:199–208 Siddiqui MH, Mohammad F, Khan MN, Khan MNA (2008) Cumulative effect of soil and foliar application of nitrogen, phosphorus and sulfur on growth, physico-biochemical parameters, yield attributes and fatty acid composition in oil of erucic acid-free rapeseed-mustard genotypes. J Plant Nutr 31:1284–1298 Siddiqui MH, Mohammad F, Masrooor M, Khan M, Al-Whaibi M (2012) Cumulative effects of nitrogen and sulfur on Brassica juncea L. genotypes under NaCl stress. Protoplasma 249:139–153 Srivastava S, Srivastava AK, Suprasanna P, D’Souza SF (2013) Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. J Exp Bot 64:303–315 Stulen I, De Kok LJ (2012) Foreword: exploring interactions between sulfate and nitrate uptake at a whole plant level. Proc Int Plant Sulfur Workshop 1:1–8 Su Y, Liu J, Lu Z, Wang X, Zhang Z, Shi G (2014) Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. Environ Exp Bot 97:40–48 Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184 Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu SH (2012) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:1–9 Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710 Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734 Wang SC, Frey P (2007) S-adenosylmethionine as an oxidant: the radical SAM superfamily. Trends Biochem Sci 32:101–110 Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151 Weber M, Harada E, Vess C, von Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential hyperaccumulation factors. Plant J 37:269–281 Yadav SK (2010) Heavy metal toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179 Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:377–388 Youssefian S, Nakamura M, Orudgev E, Kondo N (2001) Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine(thiol) lyase modifies plant responses to oxidative stress. Plant Physiol 126:1001–1011 Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432 Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–1901 Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminium toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567 Zhang B, Pasini R, Dan H, Joshi N, Zhao YH, Leustek T, Zheng ZL (2014) Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulphate transporter in response to sulphur nutrient status. Plant J 77:185–197