Indian Journal of Plant Physiology

, Volume 23, Issue 1, pp 118–127 | Cite as

Biomass partitioning and morphological parameters of Trigonella foenum-graecum submitted to sulfur deficiency

  • Mariame Houhou
  • Khalid Amrani Joutei
  • Chaimae Rais
  • Lahsen Elghadraoui
  • Said Louahlia
Original Article


In last decade several studies showed a serious reduction of sulfur content of agronomical crops associated to the decrease of the concentrations of sulfur in the atmosphere. This adverse situation would impact seriously the growth and the quality of numerous economically important plants like medicinal and aromatic species. Fenugreek (Trigonella foenum-graecum) is one of the most widely used aromatic and medicinal herbs in the world. The effect of sulfur deprivation in Fenugreek was investigated in plants grown on nutrient solution containing 1 mol m−3 S for control and 0.05 mol m−3 S for S-deficient plants. The experiment was conducted during 75 days after sowing. When compared to the control plants, the total sulfur and sulfate levels were lower in the leaves of S-deficient plants and total dry matter of the plant decreased by 32%. The most important reduction of biomass was recorded in the aerial part. The Chlorophyll content in leaves was reduced by 59% in S-deficient plants as compared to control. Partitioning of biomass and the plant morphology were also affected by S-deficiency. When compared to control, the leaf area and the LWR decreased by 37.7 and 35.3% respectively, but the LAR did not show any significant change. The leaves of S-deficient plants became thinner as result to the increase recorded in SLA value (+ 23.3%).


Sulfur deficiency Trigonella foenum-graecum Leaf area ratio Specific leaf area Leaf weight ratio 


  1. Abdallah, M., Dubousset, L., Meuriot, M., Etienne, P., Avice, J. C., & Ourry, A. (2010). Effect of mineral sulfur availability on nitrogen and sulfur uptake and remobilization during the vegetative growth of Brassica napus L. Journal of Experimental Botany, 61(10), 2635–2646.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akiko, M. N., Yumiko, N., Akiko, W. T., Eri, I., Tomoyuki, Y., & Hideki, T. (2005). Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant Journal, 42, 305–314.CrossRefGoogle Scholar
  3. Anjum, N. A., Ahmad, I., Mohmood, I., Pacheco, M., Duarte, A. C., & Pereira, E. (2012). Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids. A review. . Environmental and Experimental Botany, 75, 307–324.Google Scholar
  4. Anjum, N. A., Umar, S., Ahmad, A., Iqbal, M., & Khan, N. A. (2008). Sulfur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regulation, 54, 271–279.CrossRefGoogle Scholar
  5. Arnon, D. I. (1949). Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1–15.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Astolfi, S., & Zuchi, S. (2013). Adequate S supply protects barley plants from adverse effects of salinity stress by increasing thiol contents. Acta PhysiologiaePlantarum, 35(1), 175–181.Google Scholar
  7. Bardsley, C. E., & Lancaster, J. D. (1960). Determination of reserves sulphur and solublesulfate in soil. Proceedings of Soil Sociey of America Proceeding, 24, 265–268.CrossRefGoogle Scholar
  8. Bell, C. I., Clarkson, D. T., & John Cram, W. (1995). Partitioning and redistribution of sulphur during S-stress in Macroptilium atropurpureum cv. Siratro. Journal of Experimental Botany, 46(282), 73–81.CrossRefGoogle Scholar
  9. Blake-Kalff, M. M. A., Harrison, K. R., Hawkesford, M. J., Zhao, F. J., & McGrath, S. P. (1998). Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth. Plant Physiology, 118(4), 1337–1344.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brouwer, R. (1963). Some aspects of the equilibrium between overground and underground plant parts. Meded Inst Biol Scheik Onderz Landb Gewas, 213, 31–39.Google Scholar
  11. Burke, J. J., Holloway, P., & Dalling, M. J. (1966). The effect of sulfur deficiency on the organization and photosynthetic capability of wheat leaves. Journal of Plant Physiology, 125, 371–375.CrossRefGoogle Scholar
  12. Casieri, L., Gallardo, K., & Wipf, D. (2012). Transcriptional response of Medicago truncatula sulfate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta, 235, 1431–1447.CrossRefPubMedGoogle Scholar
  13. Ceccotti, S. (1996). Plant nutrient sulphur-a review of nutrient balance, environmental impact and fertilizers. Fertilizers and Environment, 66, 185–193.CrossRefGoogle Scholar
  14. Clarkson, D. T., Smith, F. W., & Vanden Berg, P. J. (1983). Regulation of sulfate transport in a tropical legume, Macroptilium atropurpureum, cv. Sirato. Journal of Experimental Botany, 34, 1463–1483.CrossRefGoogle Scholar
  15. Cram, W. J. (1990). Uptake and transport of sulphate. In H. Rennenberg (Ed.), Sulphur nutrition and assimilation in higher plants (pp. 3–11). The Hague: SPB Acadmic Publishing.Google Scholar
  16. Dan, H., Yang, G., & Zheng, Z. L. (2007). A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana. Plant Molecular Biology, 63, 221–235.CrossRefPubMedGoogle Scholar
  17. Davidian, J. C., & Kopriva, S. (2010). Regulation of sulfate uptake and assimilation-the same or not the same? Molecular Plant, 3, 314–325.CrossRefPubMedGoogle Scholar
  18. Droux, M. (2004). Sulfur assimilation and the role of sulfur in plant metabolism: A survey. Photosynthesis Research, 79, 331–348.CrossRefPubMedGoogle Scholar
  19. Erice, G., Louahlia, S., Irigoyen, J. J., Sanchez-Diaz, M., & Avice, J. C. (2010). Biomass partitioning, morphology and water status of four alfalfa genotypes submitted to progressive drought and subsequent recovery. Journal of Plant Physiology, 167, 114–120.CrossRefPubMedGoogle Scholar
  20. Fatma, M., Asgher, M., Masood, A., & Khan, N. A. (2014). Excess sulfur supplementation improves photosynthesis and growth in mustard under salt stress through increased production of glutathione. Environmental and Experimental Botany, 107, 55–63.CrossRefGoogle Scholar
  21. Fatma, M., Khan, M. I. R., Masood, A., & Khan, N. A. (2013). Coordinate changes in assimilatory sulfate reduction are correlated to salt tolerance: Involvement of phytohormones. Annual Review & Research in Biology, 3, 267–295.Google Scholar
  22. Gao, Y., Li, X., Tiana, Q. Y., Wanga, B. L., & Zhanga, W. H. (2015). Sulfur deficiency had different effects on MedicagoTruncatula ecotypes A17 and R108 in terms of growth, root morphology and nutrient contents. Journal Plant Nutrition, 39, 301–314.CrossRefGoogle Scholar
  23. Garnier, E., Salager, J. L., Laurent, G., & Sonie, L. (1999). Relationships between photosynthesis, nitrogen and leaf structure in 14 grass species and their dependence on the basis of expression. New Phytologist, 143, 119–129.CrossRefGoogle Scholar
  24. Grant, C., & Hawkesford, M. J. (2015). Sulfur. In A. V. Barker & D. J. Pilbeam (Eds.), Handbook of plant nutrition (2nd ed., pp. 261–301). New York: Taylor and Francis Group.Google Scholar
  25. Guendouz, A., Semcheddine, N., Moumeni, L., & Hafsi, M. (2016). The effect of supplementary irrigation on leaf area, specific leaf weight, grain yield and water use efficiency in durum wheat (Triticum durum Desf.) cultivars. Journal of Crop Breeding and Genetics, 2(1), 82–89.Google Scholar
  26. Han, Y., Chaouch, S., Mhamdi, A., Queval, G., Zechmann, B., & Noctor, G. (2013). Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxidants Redox Signaling, 18, 2106–2121.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Haneklaus, S., Bloem, E., & Schnug, E. (2008). History of sulfur deficiency in crops. In J. Jez (Ed.), Sulfur: A missing link between soils, crops, and nutrition (pp. 45–58). Madison, WI: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America.Google Scholar
  28. Haneklaus, S., Bloem, E., Schnug, E., De Kok, L. J., & Stulen, I. (2007). Sulfur. In A. V. Barker & D. J. Pilbeam (Eds.), Handbook of plant nutrition (pp. 183–238). New York: Taylor and Francis Group.Google Scholar
  29. Hawkesford, M. J. (2000). Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. Journal of Experimental Botany, 51(342), 131–138.CrossRefPubMedGoogle Scholar
  30. Hawkesford, M. J., & De kok, L. J. (2006). Managing sulphur metabolism in plants. Plant, Cell and Environment, 29, 382–395.CrossRefPubMedGoogle Scholar
  31. Hermans, C., Hammond, J. P., White, P. J., & Verbruggen, N. (2006). How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science, 11(12), 610–617.CrossRefPubMedGoogle Scholar
  32. Hiscox, J., & Israelstam, D. G. F. (1949). A method for the extraction of chlorophyll from leaf tissue without maceration. Review. Canadian botany, 57, 1332–1334.CrossRefGoogle Scholar
  33. Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil (2nd Ed., pp. 1–32). California Agricultural Experiment Station (347).Google Scholar
  34. Hoefgen, R., & Nikiforova, V. J. (2008). Metabolomics integrated with transcriptomics: Assessing systems response to sulfur-deficiency stress. Physiologia Plantarum, 132, 190–198.CrossRefPubMedGoogle Scholar
  35. Iqbal, N., Khan, N. A., Khan, M. I. R., Nazar, R., Masood, A., & Syeed, S. (2012). Sulfur in the alleviation of cadmium-induced oxidative stress in plants. In P. Ahmad & M. N. V. Prasad (Eds.), Environmental adaptations and stress tolerance of plants in the era of climate change (pp. 429–446). New York: Springer.CrossRefGoogle Scholar
  36. Iqbal, N., Masood, A., Khan, M. I. R., Asgher, M., Fatma, M., & Khan, N. A. (2013). Cross-talk between sulfur assimilation and ethylene signaling in plants. Plant Signaling and Behaviour, 8, e-22478.CrossRefGoogle Scholar
  37. Juszczuk, I. M., & Ostaszewska, M. (2011). Respiratory activity, energy and redox status in sulphur-deficient bean plants. Environmental and Experimental Botany, 74, 245–254.CrossRefGoogle Scholar
  38. Kassem, A. S., Mohammed, H. F. A., & EL-Sayed, S. A. A. (2015). Influence of sulfur deprivation on biomass allocation, mineral composition and fruit quality of tomato plants. Middle East Journal of Agriculture Research, 4, 42–48.Google Scholar
  39. Kaviarasan, S., Naik, G. H., Gangabhagirathi, R., Anuradha, C. V., & Priyadarsini, K. I. (2007). In vitro studies on antiradical and antioxidant activities of fenugreek (Trigonella foenum-graecum) seeds. Food Chemistry, 103, 31–37.CrossRefGoogle Scholar
  40. Khan, N. A., Anjum, N. A., Nazar, R., & Iqbal, N. (2009a). Increased activity of ATP-sulfurylase and increased contents of cysteine and glutathione reduce high cadmium-induced oxidative stress in mustard cultivar with high photosynthetic potential. Russian Journal of Plant Physiology, 56, 670–677.CrossRefGoogle Scholar
  41. Khan, M. I. R., Asgher, M., Iqbal, N., & Khan, N. A. (2012). Potentiality of sulfur-containing compounds in salt tolerance. In P. Ahmad & M. N. V. Prasad (Eds.), Ecophysiology and responses of plants under salt stress (pp. 443–472). New York: Springer.Google Scholar
  42. Khan, N. A., Khan, M. I. R., Asgher, M., Fatma, M., Masood, A., & Syeed, S. (2014). Salinity tolerance in plants: Revisiting the role of sulfur metabolites. Journal of Plant Biochemistry and Physiology, 1, 120.Google Scholar
  43. Khan, N. A., Nazar, R., & Anjum, N. A. (2009b). Growth, photosynthesis and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in ATP-sulfurylase activity under salinity stress. Scientia Horticulturare, 122, 455–460.CrossRefGoogle Scholar
  44. Khan, M. I. R., Nazir, F., Asgher, M., Per, T. S., & Khan, N. A. (2015). Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. Journal of Plant Physiology, 173, 9–18.CrossRefPubMedGoogle Scholar
  45. Khan, N. A., Singh, S., & Nazar, R. (2007). Activities of antioxidative enzymes, sulfur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. Journal of Agronomy and Crop Science, 193, 435–444.CrossRefGoogle Scholar
  46. Klimont, Z., Smith, S. J., & Cofala, J. (2013). The last decade of global anthropogenic sulfur dioxide: 2000–2011 emissions. Environmental Research Letters, 8(1), 014003.CrossRefGoogle Scholar
  47. Koester, R. P., Skoneczka, J. A., Cary, T. R., Diers, B. W., & Ainsworth, E. A. (2014). Historical gains in soybean (Glycine max Merr.) seed yield are driven by linear increases in light interception, energy conversion, and partitioning efficiencies. Journal of Experimental Botany, 65(12), 3311–3321.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kutz, A., Muller, A., Hennig, P., Kaiser, W. M., Piotrowski, M., & Weiler, E. W. (2002). A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant Journal, 30, 95–106.CrossRefPubMedGoogle Scholar
  49. Leustek, T., Martin, M. N., Bick, J. A., & Davies, J. P. (2000). Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annual Review of Plant Physiology, 51, 141–165.CrossRefGoogle Scholar
  50. Leustek, T., & Saito, K. (1999). Sulfate transport and assimilation in plants. Plant Physiology, 120(3), 637–643.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lopez-Bucio, J., Cruz-Ramırez, A., & Herrera-Estrella, L. (2003). The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology, 6, 280–287.CrossRefPubMedGoogle Scholar
  52. Lunde, C., Zygadlo, A., Simonsen, H. T., Nielsen, P. L., Blennow, A., & Haldrup, A. (2008). Sulfur starvation in rice: The effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. Physiologia Plantarum, 134, 508–521.CrossRefPubMedGoogle Scholar
  53. Masood, A., Iqbal, N., & Khan, N. A. (2012). Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant, Cell and Environment, 35, 524–533.CrossRefPubMedGoogle Scholar
  54. Mills, H. A., & Jones J. B. Jr. (1996). Plant analysis handbook II: a practical sampling, preparation, analysis, and interpretation guide. Athens, GA: MicroMacro Publishing, Inc. ISBN: 1878148052.Google Scholar
  55. Na, G., & Salt, D. E. (2011). The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Journal of Experimental Botany, 72, 18–25.CrossRefGoogle Scholar
  56. Nazar, R., Iqbal, N., Masood, A., Syeed, S., & Khan, N. A. (2011). Understanding the significance of sulfur in improving salinity tolerance in plants. Journal of Experimental Botany, 70, 80–87.CrossRefGoogle Scholar
  57. Nazar, R., Khan, N. A., & Anjum, N. A. (2008). ATP-sulfurylase activity, photosynthesis and shoot dry mass of mustard (Brassica juncea L.) cultivars differing in sulfur accumulation capacity. Photosynthetica, 46, 279–282.CrossRefGoogle Scholar
  58. Nielsen, S. L., Enriquez, S., Duarte, C. M., & Sand-jensent, K. (1996). Scaling maximum growth rates across photosynthetic organism. Functional Ecology, 10, 167–175.CrossRefGoogle Scholar
  59. Nikiforova, V. J., Daub, C. O., Hesse, H., Willmitze, L., & Hoefgen, R. (2005). Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. Journal of Experimental Botany, 56(417), 1887–1896.CrossRefPubMedGoogle Scholar
  60. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., & Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: Interlacing of biosynthetic pathways provides response specificity. Plant Journal, 33, 633–650.CrossRefPubMedGoogle Scholar
  61. Nikiforova, V. J., Gakiere, B., Kempa, S., Adamik, M., Willmitzer, L., Hesse, H., et al. (2004). Towards dissecting nutrient metabolism in plants: A systems biology case study on sulphur metabolism. Journal of Experimental Botany, 55, 1861–1870.CrossRefPubMedGoogle Scholar
  62. Pagani, A., & Echeverría, H. E. (2012). Influence of sulfur deficiency on chlorophyll-meter readings of corn leaves. Journal of Plant Nutrition and Soil Science, 175, 604–613.CrossRefGoogle Scholar
  63. Prosser, I. M., Purves, J. V., Saker, L. R., & Clarkson, D. T. (2001). Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. Journal of Experimental Botany, 52, 113–121.CrossRefPubMedGoogle Scholar
  64. Rais, L., Masood, A., Inam, A., & Khan, N. A. (2013). Sulfur and nitrogen co-ordinately improve photosynthetic efficiency, growth and proline accumulation in two cultivars of mustard under salt stress. Journal of Plant Biochemistry & Physiology, 1, 101.CrossRefGoogle Scholar
  65. Rausch, T., & Wachter, A. (2005). Sulfur metabolism: A versatile platform for launching defence operations. Trends in Plant Sciences, 10, 503–509.CrossRefGoogle Scholar
  66. Ross, J. V., & Koppel, A. (2000). Estimation of leaf area and its vertical distribution during growth period. Agricultural and Forest Meteorology, 101, 237–246.CrossRefGoogle Scholar
  67. Saito, K. (2004). Sulfur assimilatory metabolism, the long and smelling road. Plant Physiology, 136, 2443–2450.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Scherer, H. W. (2001). Sulphur in crop production. European Journal of Agronomy, 14, 81–111.CrossRefGoogle Scholar
  69. Scherer, H. W. (2009). Sulfur in soils. Journal of Plant Nutrition. Soil Science, 172, 326–335.CrossRefGoogle Scholar
  70. Scherer, H. W., Pacyna, S., Spoth, K. R., & Schulz, M. (2008). Low levels of ferredoxin, ATP and leghemoglobin contribute to limited N2 fixation of peas (Pisumsativum L.) and alfalfa (Medicago sativa L.) under S deficiency conditions. Biology and Fertility of Soils, 44, 909–916.CrossRefGoogle Scholar
  71. Snehlata, H. S., & Payal, D. R. (2012). Fenugreek (Trigonella foenum-graecum L.): An overview. International Journal of Current Pharmaceutical Review and Research, 2(4), 169–187.Google Scholar
  72. Syvertsen, J. P., Lloyd, J., Meconchie, C., Kriedbmann, P. E., & Garquhar, G. D. (1995). On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell and Environment, 18, 149–157.CrossRefGoogle Scholar
  73. Tewari, R. K., Kumar, P., & Sharma, P. N. (2010). Morphology and oxidative physiology of sulfur-deficient mulberry plants. Environmental and Experimental Botany, 68, 301–308.CrossRefGoogle Scholar
  74. Thomas, S. G., Bilsborrow, P. E., Hocking, T. J., & Bennett, J. (2000). Effect of sulphur deficiency on the growth and metabolism of sugar beet (Beta vulgaris cv. Druid). Journal of the Science of Food and Agriculture, 80, 2057–2062.CrossRefGoogle Scholar
  75. Varin, S., Cliquet, J. B., Personeni, E., Avice, J. C., & Lemauviel-Lavenant, S. (2010). How does sulphur availability modify N acquisition of white clover (Trifoliumrepens L.)? Journal of Experimental Botany, 61, 225–234.CrossRefPubMedGoogle Scholar
  76. Weijers, D., & Jürgens, G. (2004). Funneling auxin action: Specificity in signal transduction. Current Opinion in Plant Biology, 7, 687–693.CrossRefPubMedGoogle Scholar
  77. Weraduwage, S. M., Chen, J., Anozie, F. C., Morales, A., Weise, E., & Sharkey, T. D. (2015). The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. Frontiers in Plant Sciences, 6, 167.Google Scholar
  78. Xu, H. L., Lopez, J., Rachidi, F., Tremblay, N., Gauthier, L., Desjardins, Y., et al. (1996). Effect of sulphate on photosynthesis in greenhouse-grown tomato plants. Physiologia Plantarum, 96, 722–726.CrossRefGoogle Scholar
  79. Zhao, F. J., Wood, A. P., & McGrath, S. P. (1999). Effects of sulphur nutrition on growth and nitrogen fixation of pea (Pisum sativum L.). Plant and Soil, 212, 207–217.CrossRefGoogle Scholar

Copyright information

© Indian Society for Plant Physiology 2018

Authors and Affiliations

  • Mariame Houhou
    • 1
    • 2
  • Khalid Amrani Joutei
    • 2
  • Chaimae Rais
    • 3
  • Lahsen Elghadraoui
    • 3
  • Said Louahlia
    • 1
  1. 1.Laboratoire des Ressources Naturelles et Environnement, Multidisciplinary Faculty of TazaSidi Mohamed Ben Abdellah UniversityTazaMorocco
  2. 2.Laboratoire des Molécules BioactivesSidi Mohamed Ben Abdellah UniversityFezMorocco
  3. 3.Laboratoire Ecologie Fonctionnelle et EnvironnementSidi Mohamed Ben Abdellah UniversityFezMorocco

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