352
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Baseline hydroponic study for biofortification of bread wheat genotypes with iron and zinc under salinity: growth, ionic, physiological and biochemical adjustments

, , &
Pages 743-764 | Received 14 Jul 2021, Accepted 15 Feb 2022, Published online: 26 Apr 2022

References

  • Aftab, M., M. Haq, J. Akhtar, and E. A. Waraich. 2015. Salinity and boron tolerance in cotton (Gossypium hirsutum) varieties: A short-term hydroponic study. International Journal of Agriculture and Biology 17 (4):797–802. doi: 10.17957/IJAB/14.0020.
  • Ahmad, P., K. R. Hakeem, A. Kumar, M. Ashraf, and N. A. Akram. 2012. Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). African Journal of Biotechnology 11:2694–703.
  • Alloway, B. J. 2009. Soil factors associated with zinc deficiency in crops and humans. Environmental Geochemistry and Health 31 (5):537–48. doi: 10.1007/s10653-009-9255-4.
  • Alpaslan, M., A. Inal, A. Gunes, V. Cikili, and H. Ozcan. 1999. Effect of zinc treatment on the alleviation of sodium and chloride injury in tomato (Lycopersicum esculentum L.) grown under salinity. Turkish Journal of Botany 23:1–6.
  • Arinola, O. G. 2008. Essential trace elements and metal binding proteins in Nigerian consumers of alcoholic beverages. Pakistan Journal of Nutrition 7 (6):763–5. doi: 10.3923/pjn.2008.763.765.
  • Aroca, R., J. M. Ruiz-Lozano, A. M. Zamarreno, J. A. Paz, J. M. Garcia-Mina, M. J. Pozo, and J. A. Lopez-Raez. 2013. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. Journal of Plant Physiology 170 (1):47–55. doi: 10.1016/j.jplph.2012.08.020.
  • Ashraf, M., and Q. Ali. 2008. Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environmental and Experimental Botany 63 (1–3):266–73. doi: 10.1016/j.envexpbot.2007.11.008.
  • Ashraf, M. Y., and G. Sarwar. 2002. Salt tolerance potential in some members of Brassicaceae physiological studies on water relations and mineral contents. In Prospects for saline agriculture, 237–45. Dordrecht: Springer.
  • Ashraf, M., H. R. Athar, P. Harris, and T. R. Kwon. 2008. Some prospective strategies for improving crop salt tolerance. Advances in Agronomy 97:45–110.
  • Ashraf, M., S. M. Shahzad, M. Imtiaz, M. S. Rizwan, and M. M. Iqbal. 2017. Ameliorative effects of potassium nutrition on yield and fiber quality characteristics of cotton (Gossypium hirsutum L.) under NaCl stress. Soil and Environment 36 (01):51–8. doi: 10.25252/SE/17/31054.
  • Ashraf, M. A., M. Ashraf, and Q. Ali. 2010. Response of two genetically diverse wheat cultivars to salt stress at different growth stages: Leaf lipid peroxidation and phenolic contents. Pakistan Journal of Botany 421:559–65.
  • Bouis, H. E., C. Hotz, B. McClafferty, J. V. Meenakshi, and W. H. Pfeiffer. 2011. Biofortification: A new tool to reduce micronutrient malnutrition. Food and Nutrition Bulletin 32 (1_suppl1):S31–S540. doi: 10.1177/15648265110321S105.
  • Braun, H. J. G. Atlin, and T. Payne. 2010. Multi-location testing as a tool to identify plant response to global climate change. In Climate change and crop production, edited by M. P. Reynolds, 115–38. Oxford, UK: CABI Press.
  • Cakmak, I. 2008. Enrichment of cereal grains with zinc: Agronomic or genetic biofortification. Plant and Soil 302 (1–2):1–17. doi: 10.1007/s11104-007-9466-3.
  • Cakmak, I. 2009. Enrichment of fertilizers with zinc: An excellent investment for humanity and crop production in India. Journal of Trace Elements in Medicine and Biology: Organ of the Society for Minerals and Trace Elements (GMS) 23 (4):281–9. doi: 10.1016/j.jtemb.2009.05.002.
  • Cakmak, I., D. Strbac, and H. Marschner. 1993. Activities of hydrogen peroxide-scavenging enzymes in germinated wheat seeds. Journal of Experimental Botany 44 (1):127–32. doi: 10.1093/jxb/44.1.127.
  • Cakmak, I., L. Ozturk, S. Eker, B. Torun, H. I. Kalfa, and A. Yilmaz. 1997. Concentration of zinc and activity of Cu/Zn superoxide dismutase in leaves of rye and wheat cultivars differing in sensitivity to zinc deficiency. Journal of Plant Physiology 151:91–5. doi: 10.1016/S0176-1617(97)80042-9.
  • Cakmak, I., M. Kalayci, Y. Kaya, A. Torun, N. Aydin, Y. Wang, Z. Arisoy, H. Erdem, A. Yazici, A. Gokmen, et al. 2010. Biofortification and localization of zinc in wheat grain. Journal of Agricultural and Food Chemistry 58 (16):9092–910. doi: 10.1021/jf101197h.
  • Cantrell, I. C., and R. G. Linderman. 2001. Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant and Soil 233 (2):269–81. doi: 10.1023/A:1010564013601.
  • Chance, B., and A. C. Maehly. 1955. Assay of catalase and peroxidases. Methods in Enzymology 2:764–75. [Database][Mismatch
  • Clemens, S. 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212 (4):475–86. doi: 10.1007/s004250000458.
  • Curie, C., and J. F. Briat. 2003. Iron transport and signaling in plants. Annual Review of Plant Biology 54:183–206. doi: 10.1146/annurev.arplant.54.031902.135018.
  • Daneshbakhsh, B., A. H. Khoshgoftarmanesh, H. Shariatmadari, and I. Cakmak. 2013. Effect of zinc nutrition on salinity-induced oxidative damages in wheat genotypes differing in zinc deficiency tolerance. Acta Physiologiae Plantarum 35 (3):881–9. doi: 10.1007/s11738-012-1131-7.
  • Delfine, S., A. Alvino, M. C. Villani, and F. Loreto. 1999. Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiology 119 (3):1101–6. doi: 10.1104/pp.119.3.1101.
  • Dogan, M., R. Tipirdamaz, and Y. Demir. 2010. Salt resistance of tomato species grown in sand culture. Plant, Soil and Environment 56 (11):499–507. doi: 10.17221/24/2010-PSE.
  • Fahad, S., S. Hussain, A. Bano, S. Saud, S. Hassan, D. Shan, F. A. Khan, F. Khan, Y. Chen, C. Wu, et al. 2015. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: Consequences for changing environment. Environmental Science and Pollution Research International 22 (7):4907–21. doi: 10.1007/s11356-014-3754-2.
  • FAO. 2005. Global network on integrated soil management for sustainable use of salt-affected soils. In Food and agriculture organization, land plant nutrition management service. Rome, Italy: FAO.
  • Flexas, J., A. Diaz-Espejo, J. Galmes, R. Kaldenhoff, H. Medrano, and M. Ribas-Carbo. 2007. Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell and Environment 30 (10):1284–98. doi: 10.1111/j.1365-3040.2007.01700.x.
  • Foyer, C. H., and G. Noctor. 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell 17 (7):1866–75. doi: 10.1105/tpc.105.033589.
  • Ghogdi, E. A., A. Izadi-Darbandi, and A. Borzoue. 2012. Effects of salinity on some physiological traits in wheat (Triticum aestivum L.) cultivars. Indian Journal of Science and Technology 5 (1):1–1906. doi: 10.17485/ijst/2012/v5i1.23.
  • Gong, H., X. Zhu, K. Chen, S. Wang, and C. Zhang. 2005. Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Science 169 (2):313–21. doi: 10.1016/j.plantsci.2005.02.023.
  • Graham, R. D., R. M. Welch, and H. E. Bouis. 2001. Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: Principles, perspectives and knowledge gaps. Advances in Agronomy 70:77–142.
  • Grattan, S. R., and C. M. Grieve. 1992. Mineral element acquisition and growth response of plants grown in saline environments. Agriculture, Ecosystems and Environment 38 (4):275–300. doi: 10.1016/0167-8809(92)90151-Z.
  • Hajiboland, R. 2000. Zinc efficiency in rice plants., PhD. Thesis., Univ. Hohenheim, Verlag Grauer. Stuttgart.
  • Hajiboland, R. 2012. Effect of micronutrient deficiencies on plants stress responses. In Abiotic stress responses in plants: Metabolism, productivity and sustainability, edited by P. Ahmad and M. Prasad, 283–329. New York: Springer.
  • Hajiboland, R., and N. Becairamzadeh. 2008. Growth, gas exchange and function of antioxidant defense system in two contrasting rice genotypes under Zn and Fe deficiency and hypoxia. Acta Biologica Szegediensis 52:283–94.
  • Hao, B., J. Ma, L. Jiang, X. Wang, Y. Bai, C. Zhou, S. Ren, C. Li, and Z. Wang. 2021. Effects of foliar application of micronutrients on concentration and bioavailability of zinc and iron in wheat landraces and cultivars. Scientific Reports 11 (1):22782. doi: 10.1038/s41598-021-02088-3.
  • Hayat, S., B. A. Mir, A. S. Wani, S. A. Hasan, M. Irfan, and A. Ahmad. 2011. Screening of salt tolerant genotypes of Brassica juncea based on photosynthetic attributes. Journal of Plant Interactions 6 (1):53–60. doi: 10.1080/17429145.2010.521592.
  • Heidari, M. 2012. Effects of salinity stress on growth, chlorophyll content and osmotic components of two basil (Ocimum basilicum L.) genotypes. African Journal of Biotechnology 2012:379–84.
  • Hoagland, D. R., and D. J. Arnon. 1950. The water culture method for growing plants without soil. California Agricultural Experiment Station Circular 347:1–32.
  • Hussein, M. M., H. Mehanna, and H. N. Abou-Baker. 2012. Growth, photosynthetic pigments and mineral status of cotton plants as affected by salicylic acid and salt stress. Journal of Applied Science and Research 8:5476–84.
  • Imtiaz, M., B. J. Alloway, K. H. Shah, S. H. Siddiqui, M. Y. Memon, M. Aslam, and P. Khan. 2003. Zinc nutritious of wheat: I: Growth and zinc uptake. Asian Journal of Plant Sciences 2 (2):152–5. doi: 10.3923/ajps.2003.152.155.
  • Iqbal, M. M., G. Murtaza, T. Naz, W. Javed, S. Hussain, M. Ilyas, M. A. Anjum, S. M. Shahzad, M. Ashraf, and Z. Iqbal. 2017a. Uptake, translocation of Pb and chlorophyll contents of Oryza sativa as influenced by soil applied amendments under normal and salt-affected Pb-spiked soil conditions. Asian Journal of Agriculture and Biology 5:15–25.
  • Iqbal, M. M., G. Murtaza, S. M. Mehdi, T. Naz, A. Rehman, O. Farooq, M. Ali, M. Sabir, M. Ashraf, G. Sarwar, et al. 2017b. Evaluation of phosphorus and zinc interaction effects on wheat grown in saline–sodic soil. Pakistan Journal of Agricultural Sciences 54 (03):531–7. doi: 10.21162/PAKJAS/17.4983.
  • Iqbal, M. M., T. Naz, A. Rehman, N. Sarwar, G. Murtaza, R. Ahmad, G. Sarwar, O. Farooq, M. Ali, and M. W. Khan. 2016. Assessment of P–Zn interactive effects on growth, P and Zn uptake by wheat in salt-affected soil. Pakistan Journal of Life and Social Sciences 14:144–50.
  • Iyengar, E., and M. P. Reddy. 1996. Photosynthesis in highly salt-tolerant plants. In Handbook of Photosynthesis, edited by M. Pessaraki, 897–909. New York: Marcel Dekker.
  • Joshi, A. K., I. Crossa, B. Arun, R. Chand, R. Trethowan, M. Vargas, and I. Ortiz-Monasterio. 2010. Genotype environment interaction for zinc and iron concentration of wheat grain in Eastern Gangetic plains of India. Field Crops Research 116 (3):268–77. doi: 10.1016/j.fcr.2010.01.004.
  • Jumberi, A., M. Yamada, S. Yamada, and H. Fujiyama. 2001. Salt tolerance of grain crops in relation to ionic balance and ability to absorb microelements. Soil Science and Plant Nutrition 47 (4):657–64. doi: 10.1080/00380768.2001.10408430.
  • Khoshgoftarmanesh, A. H., R. Schulin, R. L. Chaney, B. Daneshbakhsh, and M. Afyuni. 2010. Micronutrient-efficient genotypes for crop yield and nutritional quality in sustainable agriculture. A review. Agronomy for Sustainable Development 30 (1):83–107. doi: 10.1051/agro/2009017.
  • Latef, A., and H. Chaoxing. 2011. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Horticulturae 127 (3):228–33. doi: 10.1016/j.scienta.2010.09.020.
  • Lauchli, A., and S. R. Grattan. 2007. Plant growth and development under salinity stress. In Advances in molecular breeding toward drought and salt tolerant crops, 1–32. The Netherlands: Springer: Dordrecht.
  • Marschner, H. 1995. Mineral nutrition of higher plants. 2nd ed., 889. San Diego: Academic Press.
  • Marschner, H., and V. Romheld. 1994. Strategies of plants for acquisition of iron. Plant and Soil 165 (2):261–74. doi: 10.1007/BF00008069.
  • Masood, S., T. Naz, M. T. Javed, I. Ahmed, H. Ullah, and M. Iqbal. 2014. Effect of short-term supply of farmyard manure on maize growth and soil parameters in pot culture. Archives of Agronomy and Soil Science 60 (3):337–47. doi: 10.1080/03650340.2013.792990.
  • Munns, R. 2002. Comparative physiology of salt and water stress. Plant, Cell and Environment 25 (2):239–50.
  • Munns, R., and M. Tester. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59:651–81. doi: 10.1146/annurev.arplant.59.032607.092911.
  • Munns, R., D. P. Schachtman, and A. G. Condon. 1995. The significance of a two-phase growth response to salinity in wheat and barley. Functional Plant Biology 22 (4):561–9. doi: 10.1071/PP9950561.
  • Munns, R., R. A. James, and A. Lauchli. 2006. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57 (5):1025–43. doi: 10.1093/jxb/erj100.
  • Munns, R., S. Husain, A. R. Rivelli, A. J. Richard, A. G. Condon, P. L. Megan, S. L. Evans, D. P. Schachtman, and R. A. Hare. 2002. Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant and Soil 247 (1):93–105. doi: 10.1023/A:1021119414799.
  • Naz, T. J., Akhtar, M. Anwar-Ul-Haq, and M. Shahid. 2015. Genetic variability in wheat genotypes for salt tolerance, growth and physiological responses. Soil and Environment 34:187–99.
  • Naz, T., J. Akhtar, M. A. Haq, M. Saqib, M. M. Iqbal, and M. Shahid. 2018. Interaction of salinity and boron in wheat affects physiological attributes, growth and activity of antioxidant enzymes. Pakistan Journal of Agricultural Sciences 55 (02):339–47. doi: 10.21162/PAKJAS/18.5549.
  • Naz, T., J. Akhtar, M. M. Iqbal, M. Anwar-ul-Haq, G. Murtaza, N. K. Niazi, Atique-ur-Rehman, O. Farooq, M. Ali, and B. Dell. 2019. Assessment of gas exchange attributes, chlorophyll contents, ionic composition and antioxidant enzymes of bread wheat genotypes in boron toxic, saline and boron toxic–saline soils. International Journal of Agriculture and Biology 21:1271–8.
  • Naz, T., M. M. Iqbal, M. Tahir, M. M. Hassan, M. I. Rehmani, M. I. Zafar, U. Ghafoor, M. A. Qazi, A. E. Sabagh, and M. I. Sakran. 2021. Foliar application of potassium mitigates salinity stress conditions in spinach (Spinacia oleracea L.) through reducing NaCl toxicity and enhancing the activity of antioxidant enzymes. Horticulturae 7 (12):566. doi: 10.3390/horticulturae7120566.
  • Nikolic, M., and V. Romheld, V. 2002. Does high bicarbonate supply to roots change availability of iron in the leaf apoplast? Plant and Soil 241 (1):67–74. doi: 10.1023/A:1016029024374.
  • Nikolic, M., and R. Kastori. 2000. Effect of bicarbonate and Fe supply on Fe nutrition of grapevine. Journal of Plant Nutrition 23 (11–12):1619–27. doi: 10.1080/01904160009382128.
  • Norhaizan, M. E., and N. Ain. 2009. Determination of phytate, iron, zinc, calcium contents and their molar ratios in commonly consumed raw and prepared food in Malaysia. Malasiyan Journal of Nutrition 15:213–22.
  • Ozkutlu, F., B. Torun, and I. Cakmak. 2006. Effect of zinc humate on growth of soybean and wheat in zinc deficient calcareous soil. Communications in Soil Science and Plant Analysis 37 (15–20):2769–78. doi: 10.1080/00103620600832167.
  • Page, A. L., A. C. Chang, and D. C. Adriano. 1990. Deficiencies and toxicities of trace elements. Agricultural salinity assessment and management. Ch. 7, ASCE Manuals and Reports on Engineering Practice (71):138–60.
  • Palmer, C. M., and M. L. Guerinot. 2009. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nature Chemical Biology 5 (5):333–40. doi: 10.1038/nchembio.166.
  • Palmgren, M. G., S. Clemens, L. E. Williams, U. Krämer, S. Borg, J. K. Schjørring, and D. Sanders. 2008. Zinc biofortification of cereals: Problems and solutions. Trends in Plant Science 13 (9):464–73. doi: 10.1016/j.tplants.2008.06.005.
  • Parida, A. K., and A. B. Das. 2005. Salt tolerance and salinity effects on plants: A review. Ecotoxicology and Environmental Safety 60 (3):324–49. doi: 10.1016/j.ecoenv.2004.06.010.
  • Prasad, R. 2010. Zinc biofortification of food grains in relation to food security and alleviation of zinc malnutrition. Current Science 98:1300–4.
  • Prentice, A. 2008. Vitamin D deficiency: A global perspective. Nutrition Reviews 66:S153–S164. doi: 10.1111/j.1753-4887.2008.00100.x.
  • Ramzani, P., M. Khalid, M. Naveed, R. Ahmad, and M. Shahid. 2016. Iron biofortification of wheat grains through integrated use of organic and chemical fertilizers in pH affected calcareous soil. Plant Physiology and Biochemistry : PPB 104:284–93. doi: 10.1016/j.plaphy.2016.04.053.
  • Rosegrant, M. W., and M. Agcaoili. 2010. Global food demand, supply and price prospects to 2010. Washington, DC, USA: International Food Policy Research Institute.
  • Saeidnejad, A. H., and M. Kafi. 2013. Alleviative effects of Zinc on physiological properties and antioxidants activity of maize plants under salinity stress. International Journal of Agriculture and Crop Science 5:529–37.
  • Santi, S., and W. Schmidt. 2009. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. The New Phytologist 183 (4):1072–84. doi: 10.1111/j.1469-8137.2009.02908.x.
  • Saqib, M., C. Zorb, and S. Schubert. 2006. Salt-resistant and salt-sensitive wheat genotypes show similar biochemical reaction at protein level in the first phase of salt stress. Journal of Plant Nutrition and Soil Science 169 (4):542–8. doi: 10.1002/jpln.200520557.
  • Saqib, Z. J., Akhtar, M. A. Haq, I. Ahmad, and H. F. Bakhat. 2012. Rationality of using various physiological and yield related traits in determining salt tolerance in wheat. African Journal of Biotechnology 11:3558–68.
  • Schachtman, D. P., R. Kumar, J. I. Schroeder, and E. L. Marsh. 1997. Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. Proceedings of the National Academy of Sciences of the United States of America 94 (20):11079–84. doi: 10.1073/pnas.94.20.11079.
  • Steel, R. J., H. Torrie, and D. A. Dickey. 1997. Principles and procedures of statistics: A biometrical approach, 352–8. 3rd ed. New York, USA: McGraw Hill book Co. Inc.
  • Stewart, C. P., K. G. Dewey, and P. Ashorn. 2010. The undernutrition epidemic: An urgent health priority. The Lancet 375 (9711):282. doi: 10.1016/S0140-6736(10)60132-8.
  • Szabo, G., S. Chavan, P. Mandrekar, D, and Catalano, D. 1999. Acute alcohol consumption attenuates interleukin-8 (IL-8) and monocyte chemoattractant peptide-1 (MCP-1) induction in response to ex vivo stimulation. Journal of Clinical Immunology 19 (1):67–76. doi: 10.1023/A:1020518703050.
  • Taiz, L., and E. Zeiger. 2002. Plant physiology, 690, 3rd ed. UK: Publisher Sinauer. Sunderland.
  • Turan, M. A., V. Katkat, and S. Taban. 2007. Variations in proline, chlorophyll and mineral elements contents of wheat plants grown under salinity stress. Journal of Agronomy 6:137–41.
  • US Salinity Lab. Staff. 1954. Diagnosis and improvement of saline and alkali soils. Washington, DC, USA: United States Department of Agriculture, Handbook. No. 60.
  • White, P. J., and M. R. Broadley. 2011. Physiological limits to zinc biofortification of edible crops. Frontiers in Plant Science 2:80.
  • WHO. 2012. Trends in maternal mortality: 1990 to 2010. WHO, UNICEF, UNFPA and the World Bank estimates. Geneva, Switzerland: WHO Press, World Health Organization. ISBN 978 92 4 150363 1, Printedin France.
  • Witzel, K., A. Weidner, G. K. Surabhi, A. Borner, and H. P. Mock. 2009. Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. Journal of Experimental Botany 60 (12):3545–57. doi: 10.1093/jxb/erp198.
  • Xu, L. H., W. Y. Wang, J. J. Guo, J. Qin, D. Q. Shi, Y. L. Li, and J. Xu. 2014. Zinc improves salt tolerance by increasing reactive oxygen species scavenging and reducing Na + accumulation in wheat seedlings. Biologia Plantarum 58 (4):751–7. doi: 10.1007/s10535-014-0442-5.
  • Yousfi, S., H. Houmani, F. Zribi, C. Abdelly, and M. Gharsalli. 2012. Physiological responses of wild and cultivated barley to the interactive effect of salinity and iron deficiency. ISRN Agronomy 2012:1–8. doi: 10.5402/2012/121983.
  • Zhang, J., Q. Z. Zhao, G. L. Duan, and Y. C. Huang. 2011. Influence of sulphur on arsenic accumulation and metabolism in rice seedlings. Environmental and Experimental Botany 72 (1):34–40. doi: 10.1016/j.envexpbot.2010.05.007.
  • Zhu, J. K. 2001. Plant salt tolerance. Trends in Plant Science 6 (2):66–71. doi: 10.1016/S1360-1385(00)01838-0.
  • Zhu, Z. J., G. Q. Wei, J. Li, Q. Q. Qian, and J. Q. Yu. 2004. Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Science 167 (3):527–33. doi: 10.1016/j.plantsci.2004.04.020.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.