, Volume 51, Issue 1, pp 115–126 | Cite as

Effect of inland salt-alkaline stress on C4 enzymes, pigments, antioxidant enzymes, and photosynthesis in leaf, bark, and branch chlorenchyma of poplars



The effects of soil salt-alkaline (SA) stress on leaf physiological processes are well studied in the laboratory, but less is known about their effect on leaf, bark and branch chlorenchyma and no reports exist on their effect on C4 enzymes in field conditions. Our results demonstrated that activities of C4 enzymes, such as phospholenolpyruvate carboxylase (PEPC), NADP-malic enzyme (NADP-ME), pyruvate orthophosphate dikinase (PPDK), and NADP-dependent malate dehydrogenase (NADP-MDH), could also be regulated by soil salinity/alkalinity in poplar (Populus alba × P. berolinensis) trees, similarly as the already documented changes in activities of antioxidative enzymes, such as superoxide dismutase (SOD), catalase (CAT), and glutathione reductase (GR), pigment composition, photosynthesis, and respiration. However, compared with 50–90% changes in a leaf and young branch chlorenchyma, much smaller changes in malondialdehyde (MDA), antioxidative enzymes, and C4 enzymatic activities were observed in bark chlorenchyma, showing that the effect of soil salinity/alkalinity on enzymatic activities was organ-dependent. This suggests that C4 enzymatic ratios between nonleaf chlorenchyma and leaf (the commonly used parameter to discern the operation of the C4 photosynthetic pathway in nonleaf chlorenchyma), were dependent on SA stress. Moreover, much smaller enhancement of these ratios was seen in an improved soil contrary to SA soil, when the fresh mass (FM) was used as the unit compared with a calculation on a chlorophyll (Chl) unit. An identification of the C4 photosynthesis pathway via C4 enzyme difference between chlorenchyma and leaf should take this environmental regulation and unit-based difference into account.

Additional key words

NADP-dependent malate dehydrogenase NADP-dependent malic enzyme phosphoenolpyruvate carboxylase photosynthetic pathway discrimination pyruvate orthophosphate dikinase woody chlorenchyma 











electrical conductivity


fresh mass


glutathione reductase




NADP-dependent malate dehydrogenase


NADP-dependent malic enzyme


net photosynthetic rate


phosphoenolpyruvate carboxylase


pyruvate orthophosphate dikinase


photosystem II




superoxide dismutase


dark respiration rate


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  1. Berveiller, D., Damesin, C.: Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. — Trees 22: 149–157, 2008.CrossRefGoogle Scholar
  2. Berveiller, D., Vidal, J., Degrouard, J. et al.: Tree stem phosphoenolpyruvate carboxylase (PEPC): lack of biochemical and localization evidence for a C4-like photosynthesis system. — New Phytol. 176: 775–781, 2007.PubMedCrossRefGoogle Scholar
  3. Brown, N.J., Palmer, B.G., Stanley, S. et al.: C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. — Plant J. 61: 122–133, 2010.PubMedCrossRefGoogle Scholar
  4. Dickson, R.E., Isebrands, J.G.: Leaves as regulators of stress response. — In: Mooney, H.A., Winner, W.E., Pell, E.J., Chu, E. (ed.): Response of Plants to Multiple Stresses. Pp. 3–34. Acad. Press, San Diego 1991.CrossRefGoogle Scholar
  5. Doubnerová, V., Ryšlavá, H.: What can enzymes of C4 photosynthesis do for C3 plants under stress? — Plant Sci. 180: 575–583, 2011.PubMedCrossRefGoogle Scholar
  6. Gonzalez, D.H., Iglesias, A.A., Andreo, C.S.: On the regulation of phosphoenolpyruvate carboxylase activity from maize leaves by L-malate: Effect of pH. — J. Plant Physiol. 116: 425–429, 1984.PubMedCrossRefGoogle Scholar
  7. Han, M., Yang, L., Zhang, Y., Zhou, G.: [Biomass of C3 and C4 plant function groups in Leymus chinensis communities and their response to environmental change along NE China.] — Acta Ecol. Sin. 26: 1825–1832, 2006.[In Chin.]Google Scholar
  8. Hatch, M.D., Slack, C.R.: Pyruvate, Pi dikinase from leaves. — Methods Enzymol. 42: 212–219, 1975.CrossRefGoogle Scholar
  9. Hibberd, J.M., Quick, W.P.: Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. — Nature 415: 451–454, 2002.Google Scholar
  10. HLJTR (Hei-Long-Jiang-Tu-Rang editing committee): [Soil of Heilongjiang Province.] — China Agr. Press, Beijing 1993 [In Chin.]Google Scholar
  11. Ivanov, A., Krol, M., Sveshnikov, D. et al.: Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine. — Planta 223:1165–1177, 2006.PubMedCrossRefGoogle Scholar
  12. Johnson, H.S., Hatch, M.D.: Properties and regulation of leaf NADP malate dehydrogenase and malic enzyme in plants with C4-carboxylic pathway of photosynthesis. — Biochem. J. 119: 273–280, 1970.Google Scholar
  13. Lao, J.: [Soil Agrochemistry Analysis Manual.] — China Agr. Press, Beijing 1988. [In Chin.]Google Scholar
  14. Lin, N., Tang, J.: [Quaternary environmental evolution and desertification in north China.] — J. Jilin Univ. (Earth Sci. Ed.) 33: 183–191, 2003.[In Chin.]Google Scholar
  15. Munns, R., Termaat, A.: Whole plant response to salinity. — Aust. J. Plant Physiol. 13: 143–160, 1986.CrossRefGoogle Scholar
  16. Osmond, C.B., Winter, K., Ziegler, H.: Functional significance of different pathways of CO2 fixation in photosynthesis. — In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (ed.): Physiological Plant Ecology II. Water Relations and Carbon Assimilation. Pp. 479–547. Springer-Verlag, Berlin — Heidelberg — New York 1982.CrossRefGoogle Scholar
  17. Pan, R.Z.: [Plant Physiology.] 5th Ed. — Higher Education Press, Beijing 2004. [In Chin.]Google Scholar
  18. Parida, A.K. and Das, A.B.: Salt tolerance and salinity effects on plants: a review. — Ecotoxicol. Environ. Safety 60: 324–349, 2005.PubMedCrossRefGoogle Scholar
  19. Pyankov, V., Voznesenskaya, E., Kuzmin, A. et al.: Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species. — Photosynth. Res. 63: 69–84, 2000.PubMedCrossRefGoogle Scholar
  20. Sage, R. F.: The evolution of C4 photosynthesis. — New Phytol. 161: 341–370, 2004.Google Scholar
  21. Sayre, R.T., Gonzalez, R.A.: Photosynthetic enzyme actives and localization in Mollugo verticillata populations differing in the levels of C3 and C4 cycle operation. — Plant Physiol. 64: 293–299, 1979.PubMedCrossRefGoogle Scholar
  22. Schaedle, M., Brayman, A.: Ribulose-1,5-bisphosphate carboxylase activity of Populus tremuloides Michx. bark tissues. — Tree Physiol. 1: 53–56, 1986.PubMedCrossRefGoogle Scholar
  23. Sofo, A., Dichio, B., Xiloyannis, C., Masia, A.: Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree. — Plant Sci. 166: 293–302, 2004.CrossRefGoogle Scholar
  24. Tang, H., Liu, S.: [The list of C4 plants in Neimongol area.] — Acta Sci. Natur. Univ. Neimongol 32: 431–438, 2001. [In Chin.]Google Scholar
  25. Urban, M.A., Nelson, D M., Jiménez-Moreno, G. et al.: Isotopic evidence of C4 grasses in southwestern Europe during the Early Oligocene — Middle Miocene. — Geology 38: 1091–1094, 2010.CrossRefGoogle Scholar
  26. Voznesenskaya, E., Franceschi, V., Kiirats, O. et al.: Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. — Nature 414: 543–546, 2001.PubMedCrossRefGoogle Scholar
  27. Wang, W., Guan, Y., Zu, Y., Zhao, X., Yang, L., Xu, H., Yu, X.: [The dynamics of soil alkali-salinity and growth status of several herbal plants after krilium addition in heavy soda saline-alkali soil in field.] — Acta Ecol. Sin. 29: 2835–2844, 2009.[In Chin.]Google Scholar
  28. Wang, W., He, H., Zu, Y. et al.: Addition of HPMA affects seed germination, plant growth and properties of heavy salinealkali soil in northeastern China: comparison with other agents and determination of the mechanism. — Plant Soil. 339: 177–191, 2011.CrossRefGoogle Scholar
  29. Wang, W., Zu, Y., Wang, H.: Review on the photosynthetic function of non-photosynthetic woody organs of stem and branches. — Acta Ecol. Sin. 27: 1583–1595, 2007.CrossRefGoogle Scholar
  30. Wellburn, A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. — Plant Physiol. 144: 307–313, 1994.Google Scholar
  31. Wild, A.: Soils, Land and Food: Managing the Land during the twenty-first Century. — Cambridge Univ. Press, Cambridge 2003.CrossRefGoogle Scholar
  32. Yan, Y., Wang, W., Zhu, H. et al.: [Effect of saline-alkali stress on photosynthetic characteristics of Qingshan poplar.] — J. NE Agr. Univ. 41: 31–38, 2010. [In Chin.]Google Scholar
  33. Yan, Y., Wang, W., Zhu, H. et al.: [Growth and physiological adaptability of three hybrid poplars planted in different salinealkali soil.] — Bull. Bot. Res. 29: 433–438, 2009. [In Chin.]Google Scholar
  34. Yang, C. W., Wang, P., Li, C.Y. et al.: Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. — Photosynthetica 46: 107–114, 2008.CrossRefGoogle Scholar
  35. Zhang, A., Jiang, M., Zhang, J. et al.: Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. — New Phytol. 175: 36–50, 2007.PubMedCrossRefGoogle Scholar
  36. Zhang, Y., Yin, B.: [Influences of salt and alkali mixed stresses on antioxidative activity and MDA content of Medicago sativa at seedling stage.] — Acta Prataculturae Sin. 18: 46–50, 2009. [In Chin.]Google Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Key Laboratory of Forest Plant Ecology, Ministry of EducationNortheast Forestry UniversityHarbinChina

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