Photosynthetica 2018, 56(2):606-615 | DOI: 10.1007/s11099-017-0696-1

Effect of iron, zinc and manganese shortage-induced change on photosynthetic pigments, some osmoregulators and chlorophyll fluorescence parameters in lettuce

H. R. Roosta1, A. Estaji1,*, F. Niknam2
1 Department of Horticultural Sciences, Faculty of Agriculture, Vali-E-Asr University of Rafsanjan, Rafsanjan, Iran
2 Department of Agronomy, Faculty of Agriculture, Vali-E-Asr University of Rafsanjan, Rafsanjan, Iran

Although the beneficial role of Fe, Zn, and Mn on many physiological and biochemical processes is well established, effects of each of these elements on chlorophyll (Chl) a fluorescence and photosynthetic pigment contents is not well studied. The objective of this study was to evaluate effects of Fe, Zn, and Mn deficiency in two lettuce cultivars. The parameters investigated could serve also as physiological and biochemical markers in order to identify stress-tolerant cultivars. Our results indicated that microelement shortage significantly decreased contents of photosynthetic pigments in both lettuce cultivars. Chl a fluorescence parameters including maximal quantum yield of PSII photochemistry and performance index decreased under micronutrient deficiency, while relative variable fluorescence at J-step and minimal fluorescence yield of the dark-adapted state increased under such conditions in both cultivars. Micronutrient deficiency also reduced all parameters of quantum yield and specific energy fluxes excluding quantum yield of energy dissipation, quantum yield of reduction of end electron acceptors at the PSI, and total performance index for the photochemical activity. Osmoregulators, such as proline, soluble sugar, and total phenols were enhanced in plants grown under micronutrient deficiency. Fe, Zn, and Mn deficiency led to a lesser production of dry mass. The Fe deficiency was more destructive than that of Zn and Mn on the efficiency of PSII in both lettuce cultivars. Our results suggest that the leaf lettuce, which showed a higher efficiency of PSII, electron transport, quantum yield, specific energy fluxes, and osmoregulators under micronutrient deficiency, was more tolerant to stress conditions than crisphead lettuce.

Keywords: chlorophyll fluorescence transients; micronutrient; Lactuca sativa; quantum yield

Received: July 16, 2016; Accepted: December 1, 2016; Published: June 1, 2018Show citation

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Roosta, H.R., Estaji, A., & Niknam, F. (2018). Effect of iron, zinc and manganese shortage-induced change on photosynthetic pigments, some osmoregulators and chlorophyll fluorescence parameters in lettuce. Photosynthetica56(2), 606-615. doi: 10.1007/s11099-017-0696-1.
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References

  1. Aravind P., Prasad M.N.V.: Zinc protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte. - Plant Sci. 166: 1321-1327, 2004. Go to original source...
  2. Arias-Baldrich C., Bosch N., Begines D. et al.: Proline synthesis in barley under iron deficiency and salinity. - J. Plant Physiol. 183: 121-129, 2015. Go to original source...
  3. Barker A.V., Pilbeam D.J.: Handbook of Plant Nutrition. Pp. 392-457. CRC Press, New York 2015. Go to original source...
  4. Beauchemin R., Gauthier A., Harnois J. et al.: Spermine and spermidine inhibition of photosystem II: disassembly of the oxygen evolving complex and consequent perturbation in electron donation from Tyr Z to P680+ and the quinone acceptors QA to QB. - BBA-Bioenergetics 1767: 905-912, 2007. Go to original source...
  5. Bertamini M., Nedunchezhian N., Borghi B.: Effect of iron deficiency induced changes on photosynthetic pigments, ribulose-1,5-bisphosphate carboxylase, and photosystem activities in field grown grapevine (Vitis vinifera L. cv. Pinot noir) leaves. - Photosynthetica 39: 59-65, 2001. Go to original source...
  6. Bityutskii N., Pavlovic J., Yakkonen K. et al.: Contrasting effect of silicon on iron, zinc and manganese status and accumulation of metal-mobilizing compounds in micronutrient-deficient cucumber. - Plant Physiol. Bioch. 74: 205-211, 2014. Go to original source...
  7. Breštič M., Živčák M., Kunderlíková K. et al.: Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. - Photosynth. Res. 125: 151-166, 2015. Go to original source...
  8. Cesco S., Neumann G., Tomasi N. et al.: Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. - Plant Soil 329: 1-25, 2010. Go to original source...
  9. Chaves M.M., Maroco J.P., Pereira J.S.: Understanding plant responses to drought. - from genes to the whole plant. - Funct. Plant Biol. 30: 239-264, 2003. Go to original source...
  10. Ciompi S., Gentili E., Guidi L. et al.: The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. - Plant Sci. 118: 177-184, 1996. Go to original source...
  11. Donnini S., Guidi L., Degl'Innocenti E. et al.: Image changes in chlorophyll fluorescence of cucumber leaves in response to iron deficiency and resupply. - J. Plant Nutr. Soil Sci. 176: 734-742, 2013. Go to original source...
  12. Duysens L., Sweers H.: Mechanism of two photochemical reactions in algae as studied by means of fluorescence. - In: Japanese Society of Plant Physiologists (ed.): Studies on Microalgae and Photosynthetic Bacteria. Pp. 353-372. Univ. of Tokyo Press, Tokyo 1963.
  13. Evans J.R., Terashima I.: Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. - Funct. Plant Biol. 14: 59-68, 1987. Go to original source...
  14. Fu C., Li M., Zhang Y. et al.: Morphology, photosynthesis, and internal structure alterations in field apple leaves under hidden and acute zinc deficiency. - Sci. Hortic.-Amsterdam 193: 47-54, 2015.
  15. Hajiboland R., Amirazad F.: Growth, photosynthesis and antioxidant defense system in Zn-deficient red cabbage plants. - Plant Soil Environ. 56: 209-217, 2010 Go to original source...
  16. Hayat S., Hayat Q., Alyemeni M.N. et al.: Role of proline under changing environments: a review. - Plant Signal. Behav. 7: 1456-1466, 2012. Go to original source...
  17. Heidari M., Sarani S.: Growth, biochemical components and ion content of chamomile (Matricaria chamomilla L.) under salinity stress and iron deficiency. - J. Saudi Society Agri. Sci. 11: 37-42, 2012. Go to original source...
  18. Henriques F.S.: Loss of blade photosynthetic area and of chloroplasts photochemical capacity account for reduced CO2 assimilation rates in zinc-deficient sugar beet leaves. - J. Plant Physiol. 158: 915-919, 2001. Go to original source...
  19. Isfendiyaroglu M., Ozeker E.: The relation between phenolic compound and seed dormancy in pistachios and almond. - Cahiers Opt. Mediterr. 56: 232-277, 2002
  20. Izaguirre-Mayoral M., Sinclair T.: Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. - Ann. Bot.-London 96: 149-158, 2005. Go to original source...
  21. Jamalomidi M., Esfahani M., Carapetian J.: Zinc and salinity interaction on agronomical traits, chlorophyll and proline content in lowland rice (Oryza sativa L.) genotypes. - Pak. J. Biol. Sci. 9: 1315-1319, 2006.
  22. Kalaji H.M. Loboda T.: Photosystem II of barley seedlings under cadmium and lead stress. - Plant Soil Environ. 53: 511-516, 2007.
  23. Kalaji H.M., Oukarroum A., Alexandrov V. et al.: Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. - Plant Physiol. Bioch. 81: 16-25, 2014. Go to original source...
  24. Kautsky H., Hirsch A.: [New experiments on carbonic acid assimilation.]. - Naturwissenschaften 19: 964-964, 1931. [In German] Go to original source...
  25. Khan M.I.R., Khan N.A.: Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PSII activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. - Protoplasma 251: 1007-1019, 2014. Go to original source...
  26. Lichtenthaler R.: Chlorophylls and carotenoids. - pigments of photosynthetic biomembranes. - Methods Enzymol. 148: 350-382, 1987. Go to original source...
  27. Machold O., Stephan U.: The function of iron in porphyrin and chlorophyll biosynthesis. - Phytochemistry 8: 2189-2192, 1969. Go to original source...
  28. Mahmoudi H., Ksouri R., Gharsalli M. et al.: Differences in responses to iron deficiency between two legumes: lentil (Lens culinaris) and chickpea (Cicer arietinum). - J. Plant Physiol. 162: 1237-1245, 2005. Go to original source...
  29. Marschner H.: Marschner's Mineral Nutrition of Higher Plants. Pp. 191-243. Academic Press, London 2011.
  30. Milner M.J., Seamon J., Craft E. et al.: Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. - J. Exp. Bot. 64: 369-381, 2013. Go to original source...
  31. Morales F., Abadía A., Abadía J.: Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. - Plant Physiol. 97: 886-893, 1991. Go to original source...
  32. Osório J., Osório M.L., Correia P.J. et al.: Chlorophyll fluorescence imaging as a tool to understand the impact of iron deficiency and resupply on photosynthetic performance of strawberry plants. - Sci. Hortic.-Amsterdam 165: 148-155, 2014. Go to original source...
  33. Oukarroum A., Bussotti F., Goltsev V. et al.: Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. - Environ. Exp. Bot. 109: 80-88, 2015 Go to original source...
  34. Pavlovic J., Samardzic J., Maksimović V. et al.: Silicon alleviates iron deficiency in cucumber by promoting mobilization of iron in the root apoplast. - New Phytol. 198: 1096-1107, 2013. Go to original source...
  35. Percival G., Henderson A.: An assessment of the freezing tolerance of urban trees using chlorophyll fluorescence. - J. Hortic. Sci. Biotech. 78: 254-260, 2003. Go to original source...
  36. Pestana M., Correia P.J., Saavedra T. et al.: Development and recovery of iron deficiency by iron resupply to roots or leaves of strawberry plants. - Plant Physiol. Bioch. 53: 1-5, 2012. Go to original source...
  37. Petrazzini L.L., Souza G.A., Rodas C.L. et al.: Nutritional deficiency in crisphead lettuce grown in hydroponics. - Hortic. Bras. 32: 310-313, 2014. Go to original source...
  38. Qu C., Gong X., Liu C. et al.: Effects of manganese deficiency and added cerium on photochemical efficiency of maize chloroplasts. - Biol. Trace. Elem. Res. 146: 94-100, 2012. Go to original source...
  39. Roháček K., Barták M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. - Photosynthetica 37: 339-363, 1999.
  40. Roosta H.R., Schjoerring J.K.: Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants. - J. Plant Nutr. 30: 1933-1951, 2007.
  41. Roosta H.R., Mohsenian Y.: Effects of foliar spray of different Fe sources on pepper (Capsicum annum L.) plants in aquaponic system. - Sci. Hortic.-Amsterdam 146: 182-191, 2012.
  42. Saradhi P.P., Alia, Vani B.: Inhibition of mitochondrial electron transport is the prime cause behind proline accumulation during mineral deficiency in Oryza sativa. - Plant Soil 155: 465-468, 1993. Go to original source...
  43. Shangguan Z., Shao M., Dyckmans J.: Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. - J. Plant Physiol. 156: 46-51, 2000. Go to original source...
  44. Sinclair S.A., Krämer U.: The zinc homeostasis network of land plants. - BBA-Mol. Cell. Biol. L. 1823: 1553-1567, 2012.
  45. Singh P., Misra A., Srivastava N.K.: Influence of Mn deficiency on growth, chlorophyll content, physiology, and essential monoterpene oil(s) in genotypes of spearmint (Mentha spicata L.). - Photosynthetica 39: 473-476, 2001. Go to original source...
  46. Sperotto R.A., Ricachenevsky F.K., Fett, J.P.: Iron deficiency in rice shoots: identification of novel induced genes using RDA and possible relation to leaf senescence. - Plant Cell Rep. 26: 1399-1411, 2007. Go to original source...
  47. Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. - In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445-483, Taylor and Francis, London 2000.
  48. Strasser R.J., Tsimilli-Michael M., Qiang S. et al.: Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. - BBABioenergetics 1797: 1313-1326, 2010. Go to original source...
  49. Suzuki M., Bashir K., Inoue H. et al.: Accumulation of starch in Zn-deficient rice. - Rice 5: 9, 2012. Go to original source...
  50. Terry N., Abadía J.: Function of iron in chloroplasts. - J. Plant Nutr. 9: 609-646, 1986. Go to original source...
  51. Timperio A.M., D'Amici G.M., Barta C. et al.: Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. - J. Exp. Bot. 58: 3695-3710, 2007. Go to original source...
  52. Tuba Z., Saxena D.K., Srivastava K. et al.: Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping. - Curr. Sci. 98: 1505-1508, 2010.
  53. Valentinuzzi F., Pii Y., Vigani G. et al.: Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria × ananassa. - J. Exp. Bot. 66: 6483-6495, 2015. Go to original source...
  54. Weng J.K., Li X., Bonawitz N.D. et al.: Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. - Curr. Opin. Biotech. 19: 166-172, 2008. Go to original source...
  55. Xue H., Aziz R.M., Sun N. et al.: Inhibition of cellular transformation by berry extracts. - Carcinogenesis 22: 351-356, 2001. Go to original source...
  56. Zhao A.Q., Bao Q.L., Tian X.H. et al.: Combined effect of iron and zinc on micronutrient levels in wheat (Triticum aestivum L.). - J. Env. Biol. 32: 235-239, 2011.