Limited sulfur resource forces Arabidopsis thaliana to shift towards non-sulfur tolerance under cadmium stress

Environmental and Experimental Botany

Volumn 94, Issue , 2013, Pages 19-32

  Bashir, Humayra ^a   Ahmad, Javed ^a   Bagheri, Rita ^a   Nauman, M ^a   Qureshi, M Irfan ^a  

^a JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

Author keywords

Antioxidants; Arabidopsis thaliana; Cadmium; Proline; Sulfur

Indexed keywords

ANTIOXIDANT; BIOACCUMULATION; BIOMASS; CADMIUM; DEFENSE BEHAVIOR; ENVIRONMENTAL STRESS; GEOGRAPHICAL REGION; GROWTH RESPONSE; HERB; HYDROGEN PEROXIDE; PHOTOSYNTHESIS; POLLUTION EFFECT; POLLUTION EXPOSURE; SULFUR; TOLERANCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84881232410     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2012.05.004     Document Type: Article

References (114)

1. Aebi H. Catalase. Methods of Enzymatic Analysis 1983, vol. 3:273-277. Verlag Chemie, Weinheim.
2. Anderson M.E. Determination of glutathione disulphides in biological samples. Methods in Enzymology 1985, 113:548-570.
3. Andrade J.L., Larque S.A., Trejo C.L. Proline accumulation in leaves of four cultivars of Phaseolus vulgaris L. with different drought resistance. Phyton Beunas Aires 1995, 57:149-1557.
4. Angelone M., Bini C. Trace element concentration in the soil and plants of Western Europe. Biogeochemistry of Trace Metal 1992, 19-670. Lewis Publishers, Boca Raton, Florida. D.C. Adriano (Ed.).
5. Anjum N., Umar S., Ahmad A., Iqbal M., Khan N. Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regulation 2008, 54:271-279.
6. Anjum N.A., Ahmad I., Mohmooda I., Pacheco M., Duarte A.C., Pereira E. Modulation of glutathione and its related enzymes in plants' responses to toxic metals and metalloids-a review. Environmental and Experimental Botany 2012, 75:307-324.
7. Arnon D.I. Copper enzymes in isolated chloroplasts. Polyphenoloxidases in Beta vulgaris. Plant Physiology 1949, 24:1-15.
8. Ashraf M., Foolad M.R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 2007, 59:206-216.
9. Astolfi S., Zuchi S., Hubberten H-M., Pinton R., Hoefgen R. Supply of sulphur to S-deficient young barley seedlings restores their capability to cope with iron shortage. Journal of Experimental Botany 2010, 61:799-806.
10. Astolfi S., Zuchi S., Neumann G., Cesco S., Sanità di Toppi L., Pinton R. Response of barley plants to Fe deficiency and Cd contamination as affected by S starvation. Journal of Experimental Botany 2012, 63:1241-1250.
11. Astolfi S., Zuchi S., Passera C. Role of sulphur availability on cadmium-induced changes of nitrogen and sulphur metabolism in maize (Zea mays L.) leaves. Journal of Plant Physiology 2004, 161:795-802.
12. Azpilicueta C.E., Benavides M.P., Tomaro M.L., Gallego S.M. Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiology and Biochemistry 2007, 45:589-595.
13. Bailey-Serres J., Mittler R. The roles of reactive oxygen species in plant cells. Plant Physiology 2006, 141:311.
14. Barcelò J., Poschenrieder C. Plant-water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 1990, 13:1-37.
15. Baryla A., Carrier P., Franck F., Coulomb C., Sahut C., Havaux M. Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 2001, 212:696-709.
16. Baszynski T., Wajda L., Krol M., Wolinska D., Krupa Z., Tukendorf A. Photosynthetic activities of cadmium treated tomato plants. Physiologia Plantarum 1980, 48:365-370.
17. Bates L.S., Walderen R.D., Taere I.D. Rapid determination of free proline for water stress studies. Plant Soil 1973, 39:205-207.
18. Baudet J., Huet J-C., Jolivet E., Christine E.J. Changes in accumulation of seed nitrogen compounds in maize under conditions of sulphur deficiency. Physiologia Plantarum 1986, 68:608-614.
19. Bowler C., VanMontagu M., Inzé D. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 1992, 43:83-116.
20. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
21. Chaoui A., Mazhoudi S., Ghorbal M.H., El Ferjani E. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Science 1997, 127:139-147.
22. Cho U.-H., Seo N.-H. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Science 2005, 168:113-120.
23. Chu C.-C., Lee W.-C., Guo W.-Y., Pan S.-M., Chen L.-J., Li H.-M., Jinn T.-L. A copper chaperone for superoxide dismutase that confers three types of Copper/Zinc superoxide dismutase activity in Arabidopsis. Plant Physiology 2005, 139:425-436.
24. Cobbett C.S., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 2002, 53:159-182.
25. Dhingra A., Portis A.R., Daniell H. Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:6315-6320.
26. Dixit V., Pandey V., Shyam R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). Journal of Experimental Botany 2001, 52:1101-1109.
27. Dixon D.P., Lapthorn A., Edwards R. Plant glutathione transferases. Genome Biology 2002, 3:3004. 1-3004.10.
28. Edwards R., Dixon D.P., Walbot V. Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends in Plant Science 2000, 5:193-198.
29. Fagioni M., D'Amici G.M., Timperio A.M., Zolla L. Proteomic analysis of multiprotein complexes in the thylakoid membrane upon cadmium treatment. Journal of Proteome Research 2009, 8:310-326.
30. Gadapati W.R., Macfie S.M. Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Science 2006, 170:471-480.
31. Gaitonde M.K. A spectrophotometric method for the direct measurement of cysteine in the presence of other naturally occurring amino acids. Biochemical Journal 1967, 104:627-633.
32. Gao K.H., Ge Y., Zhang C.H. Effects of sulfur starvation on the non-protein thiol content and glutathione S-transferase activity of rice seedlings under cadmium stress. Ying Yong Sheng Tai Xue Bao 2011, 22:1796-1802.
33. Gill S.S., Tuteja N. Cadmium stress tolerance in crop plants - probing the role of sulfur. Plant Signaling Behavior 2011, 6:215-222.
34. Gomes-Junior R.A., Moldes C.A., Delite F.S., Pompeu G.B., Gratão P.L., Mazzafera P., Lea P.J., Azevedo R.A. Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 2006, 65:1330-1337.
35. Grill D., Tausz M., De Kok L.J. Significance of glutathione in plant adaptation to the environment. Handbook of Plant Ecophysiology 2001, vol. 2. Kluwer, Dordrecht.
36. Grossmann S., Leshem Y. Lowering of endogenous lipoxyenase activiyt in Pisum sativum foliage by cytokinin as related to senescence. Physiologia Plantarum 1978, 43L:359-362.
37. Guo W.D., Liang J., Yang X.E., Chao Y.E., Feng Y. Response of ATP sulfurylase and serine acetyltransferase towards cadmium in hyperaccumulator Sedumalfredii Hance. Journal of Zhejiang University. Science B 2009, 10:251-257.
38. Habig W.H., Jacoby W.B. Methods in Enzymology 1981, Academic Press, New York. S.P. Colowick, N.O. Kaplan (Eds.).
39. Harada E., Yamaquchi Y., Koizumi N., Sano H. Cadmium stress induces production of thiol compounds that transcript for enzymes involved in sulphur assimilation pathway in Arabidopsis. Journal of Plant Physiology 2002, 154:445-448.
40. Hardulak L.A., Preuss M.L., Jez J.M. Sulfur metabolism as a support system for plant heavy metal tolerance. Detoxification of Heavy Metals, Soil Biology 2011, vol. 30:289-301. Springer, Berlin, Heidelberg.
41. Hasan S.A., Hayat S., Ali B., Ahmad A. 28-Homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. Environmental Pollution 2008, 151:60-66.
42. Heath R.L., Packer L. Photoperoxidation in isolated chloroplasts: I Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 1968, 125:189-198.
43. Hervieu F., Dily F.L., Billard J.P., Huault C. Effect of water stress on proline content and ornithine aminotransferase activity of radish cotyledons. Plant Cell Environment 1994, 18:205-210.
44. Hesse H., Hoefgen R. Molecular aspects of methionine biosynthesis. Trends in Plant Science 2003, 8:259-262.
45. Hiscox J.D., Israelstam G.F. A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 1979, 57:1332-1334.
46. Hogland D.R., Arnon D.I. The water culture method for growing plants without soil. Colorado Agricultural Experiment Station circular 1950, 347:1-32.
47. Honsel A., Kojima M., Haas R., Frank W., Sakakibara H., Herschbach C., Rennenberg H. Sulphur limitation and early sulphur deficiency responses in poplar: significance of gene expression, metabolites, and plant hormones. Journal of Experimental Botany 2012, 63:1873-1893.
48. Jimenez A., Hernandez J.A., del Rio L.A., Sevilla F. Evidence for the presence of the sscorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiology 1997, 114:275-284.
49. Kastori R., Plesnicar M., Arsenijevic-Maksimovic I., Petrovic N., Pankovic D., Sakac Z. Photosynthesis chlorophyll fluorescence, and water relations in young sugar beet plants as affected by sulfur supply. Journal of Plant Nutrition 2000, 23:1037-1049.
50. Kato M., Shimizu S. Chlorophyll metabolism in higher plants. VI Involvement of peroxidase in chlorophyll degradation. Plant Cell Physiology 1985, 26:1291-1301.
51. Khan T.A., Mazid M. Nutritional significance of sulphur in pulse cropping system. Biology and Medicine 2011, 3:114-133.
52. Kim Y., Yang Y.Y., Lee Y. Pb and Cd uptake in rice toots. Physiologia Plantarum 2002, 116:368-372.
53. Kishor P.B.K., Hong Z., Miao G.H., Hu C.A.A., Verma D.P.S., Hong Z.L., Miao G.H. Overexpression of delta-1 pyroline 5'-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plant. Plant Physiology 1995, 108:1387-1394.
54. Kramer U. The dilemma of controlling heavy metal accumulation in plants. New Phytologist 2009, 181:3-5.
55. Krupa Z., Baszynski T. Some aspect of heavy metals toxicity towards photosynthetic apparatus - direct and indirect effects on light and dark reactions. Acta Physiologiae Plantarum 1995, 177-190.
56. Lee B.-R., Jin Y.-L., Jung W.-J., Avice J.-C., Morvan-Bertrand A., Ourry A., Park C.-W., Kim T.-H. Water-deficit accumulates sugars by starch degradation-not by de novo synthesis-in white clover leaves (Trifolium repens). Physiologia Plantarum 2008, 134:403-411.
57. Lee S., Leustek T. The effect of cadmium on sulphate assimilation enzyme in Brassica juncea. Plant Science 1999, 141:201-207.
58. Leustek T. Sulfate metabolism. The Arabidopsis Book 2002, American Society of Plant Biologists, Rockville, MD. C.A. Somerville, E.M. Meyerowitz (Eds.).
59. Leustek T., Martin M.N., Bick J.A., Davies J.P. Pathways and regulations of sulphur metabolism revealed through molecular and genetic studies. Annual Review of Plant Physiology and Plant Molecular Biology 2000, 51:141-165.
60. Leustek T., Saito K. Sulfate transport and assimilation in plants. Plant Physiology 1999, 120:637-643.
61. Liu Y., Wang X., Zeng G., Qu D., Gu J., Zhou M., Chai L. Cadmium-induced oxidative stress and response of the ascorbate-glutathione cycle in Bechmeria nivea (L.) Gaud. Chemosphere 2007, 69:99-107.
62. Lunde C., Zygadlo A., Simonsen H.T., Nielsen P.L., Blennow A., Haldrup A. Sulfur starvation in rice: the effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. Physiologia Plantarum 2008, 134:508-521.
63. Marrs K.A. The functions and regulation of glutathione S transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 1996, 47:127-158.
64. Matsubayashi Y., Ogawa M., Morita A., Sakagami Y. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 2002, 296:1470-1472.
65. Michele R.D., Vurro E., Rigo C., Costa A., Elviri L., Di Valentin M., Careri M., Zottini M., Sanità di Toppi L., Lo Schiavo F. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiology 2009, 150:217-228.
66. Mobin M., Khan N.A. Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. Journal of Plant Physiology 2007, 164:601-610.
67. Murashige T., Skoog F.A. Revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiology 1962, 15:473-497.
68. Na G., Salt D.E. The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Environmental and Experimental Botany 2011, 72:18-25.
69. Nagel K., Adelmeier U., Voight J. Subcellular 601 distribution of cadmium in the unicellular green alga Chlamydomonas reinhardii. Journal of Plant Physiology 1996, 149:86-90.
70. Nikiforova V., Freitag J., Kempa S., Adamik M., Hesse H., Hoefgen R. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant Journal 2003, 33:633-650.
71. Nikiforova V.J., Kopka J., Tolstikov V., Fiehn O., Hopkins L., Hawkesford M.J., Hesse H., Hoefgen R. Systems rebalancing of metabolism in response to sulfur deprivation as revealed by metabolome analysis of Arabidopsis plants. Plant Physiology 2005, 138:304-318.
72. Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 1998, 49:249-279.
73. Noctor G., Gomez L.A., Vanacker H., Foyer C.H. Interactions between biosynthesis, comparmentation and transport in the control of glutathione homeostasis and signaling. Journal of Experimental Botany 2002, 53:1283-1304.
74. Noctor G., Queval G., Mhamdi A., Chaouch S., Foyer C.H. Glutathione. The Arabidopsis Book 2011, American Society of Plant Biologists, Rockville, MD. 10.1199/tab.0142.
75. Novitskaya L., Trevanion S.J., Driscoll S., Foyer C.H., Noctor G. How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis. Plant, Cell and Environment 2002, 25:821-835.
76. Ogren W.L. Affixing the O to Rubisco: discovering the source of photorespiratory glycolate and its regulation. Photosynthesis Research 2003, 76:53-63.
77. Osslund T., Chandler C., Segel I.H. ATP sulfurylase from higher plants. Purification and preliminary kinetics studies on the cabbage leaf enzyme. Plant Physiology 1982, 70:39-45.
78. Palmer C.M., Guerinot M.L. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nature Chemical Biology 2009, 5:333-340.
79. Park J., Song W.-Y., Ko D., Eom Y., Hansen T.H., Schiller M., Lee T.G. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant Journal 2012, 69:278-288.
80. Perfus-Barbeoch L., Leonhardt N., Vavasseur A., Forestier C. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant Journal 2002, 32:539-548.
81. Pietrini F., Iannelli M.A., Pasqualini S., Massacci A. Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.). Trin. Ex Steudel. Plant Physiology 2003, 133:829-837.
82. Qadir S., Qureshi M.I., Javed S., Abdin M.Z. Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Science 2004, 167:1171-1181.
83. Qureshi M., Abdin M., Qadir S., Iqbal M. Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biologia Plantarum 2007, 51:121-128.
84. Qureshi M.I., D'Amici G.M., Fagioni M., Rinalducci S., Zolla L. Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. Journal of Plant Physiology 2010, 167:761-770.
85. Rascio N., Dalla Vecchia F., La Rocca N., Barbato R., Pagliano C., Raviolo M., Gonnelli C., Gabbrielli R. Metal accumulation and damage in rice (cv Vialone nano) seedlings exposed to cadmium. Environmental and Experimental Botany 2008, 62:267-278.
86. Rodríguez-Serrano M., Romero-Puertas M.C., Sparkes I., Hawes C., del Río L.A., Sandalio L.M. Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radical Biology and Medicine 2009, 47:1632-1639.
87. Romero-Puertas M.C., Corpas F.J., Rodri{dotless}guez-Serrano M., Gomez M., del Ri{dotless}o L.A., Sandalio L.M. Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. Journal of Plant Physiology 2007, 164:1346-1357.
88. 2 in pea leaves. Plant Cell Environment 2004, 27:1122-1134.
89. Ryan K.C., Johnson O.E., Cabelli D.E., Brunold T.C., Maroney M.J. Nickel superoxide dismutase: structural and functional roles of Cys2 and Cys6. Journal of Biological Chemistry 2010, 15:795-807.
90. Saito K. Sulphur assimilatory metabolism. The long and smelling road. Plant Physiology 2004, 136:2443-2450.
91. Sandalio L.M., Dalura H.C., Gomez M., Romero-Puertas M.C., del Rio L.A. Cadmium induced changes in the growth and oxidative metabolism of pea plant. Journal of Experimental Botany 2001, 52:2114-2126.
92. Sandmann G., Böger P. Copper meidated lipid peroxidation process in photosynthetic membranes. Plant Physiology 1980, 36:1291-1301.
93. Sanità di Toppi L., Gabbrielli R. Responses to cadmium in higher plants: a review. Environmental and Experimental Botany 1999, 41:105-130.
94. Sappl P.G., Onate-Sanchez L., Singh K.B., Millar A.H. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Molecular Biology 2004, 54:205-219.
95. Schnug E., Ernst W.H.O., Kraztz S., Knolle F., Haneklaus S. Aspects of ecotoxicology of sulphur in the Harz region-a guided excursion. Landbauforschung Voelkenrode 2004, 54:129-143.
96. Sekhar K., Priyanka B., Reddy V.D., Rao K.V. Metallothionein 1 (CcMT1) of pigeonpea (Cajanus cajan, L.) confers enhanced tolerance to copper and cadmium in Escherichia coli and Arabidopsis thaliana. Environmental and Experimental Botany 2011, 72:131-139.
97. Shigeoka S., Ishikawa T., Tamoi M., Miyagawa Y., Takeda T., Yabuta Y., Yoshimura K. Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany 2002, 53:1305-1319.
98. Siedow J.N., Day D.A. Respiration and photorespiration. Biochemistry and Molecular Biology of Plants 2000, 676-728. American Society of Plant Physiologists, Rockville, MD. B.B. Buchanan, W. Gruissem, R.L. Jones (Eds.).
99. Somashekaraiah B.V., Padmaja K., Prasad A.R.K. Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxides in chlorphyll degradation. Physiologia Plantarum 1992, 85:85-89.
100. Spreitzer R.J., Salvucci M.E. Rubisco: structure regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology 2002, 53:449-475.
101. Stochs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biology and Medicine 1995, 18:321-336.
102. Tausz M., Sircelj H., Grill D. The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid?. Journal of Experimental Botany 2004, 55:1955-1962.
103. Trovato M., Mattioli R., Costantino P. Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei 2008, 19:325-346.
104. Van Assche F., Clijsters H. Effects of metals on enzyme activity in plants. Plant Cell Environment 1990, 13:195-206.
105. Vitória A.P., Lea P.J., Azevedo R.A. Antioxidant enzyme responses to cadmium in radish tissue. Phytochemistry 2001, 57:701-710.
106. Wagner G.J. Accumulation of cadmium in crop plants and its consequences to human health. Advances in Agronomy 1993, 51:173-212.
107. Weckx J.E.J., Clijsters H.M.M. Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiologia Plantarum 1996, 96:506-512.
108. Wilson, Bandurski L.G. Enzymatic reaction involving sulphate, sulphite, selenate and molybdate. Journal of Biological Chemistry 1958, 233:975-981.
109. Xu J., Yin H.X. Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Reports 2009, 28:325-333.
110. Yu B., Benning C. Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant Journal 2003, 36:762-770.
111. Zenk M.H. Heavy metal detoxification in higher plants: a review. Gene 1996, 179:21-30.
112. Zhang F.Q., Shi W.Y., Jin Z.X., Shen Z.G. Response of antioxidative enzymes in cucumber chloroplast to cadmium toxicity. Journal of Plant Nutrition 2003, 26:1779-1788.
113. Zhang Z.-C., Chen B.-X., Qiu B.-S. Phytochelatin synthesis plays a similar role in shoots of the cadmium hyperaccumulator Sedum alfredii as in non-resistant plants. Plant Cell Environment 2010, 33:1248-1255.
114. Zhao F.J., Hawkesford M.J., McGrath S.P. Sulphur assimilation and effects on yield and quality of wheat. Journal of Cereal Science 1999, 30:1-17.