Photosynthetica, 2013 (vol. 51), issue 1

Photosynthetica 2013, 51(1):115-126 | DOI: 10.1007/s11099-013-0008-3

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

H. M. Wang1, W. J. Wang1,*, H. Z. Wang1, Y. Wang1, H. N. Xu1, Y. G. Zu1,*
1 Key Laboratory of Forest Plant Ecology, Ministry of Education, Northeast Forestry University, Harbin, China

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.

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

Received: February 13, 2012; Accepted: November 21, 2012; Published: March 1, 2013Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Wang, H.M., Wang, W.J., Wang, H.Z., Wang, Y., Xu, H.N., & Zu, Y.G. (2013). Effect of inland salt-alkaline stress on C4 enzymes, pigments, antioxidant enzymes, and photosynthesis in leaf, bark, and branch chlorenchyma of poplars. Photosynthetica51(1), 115-126. doi: 10.1007/s11099-013-0008-3.
Download citation

References

  1. Berveiller, D., Damesin, C.: Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. - Trees 22: 149-157, 2008. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  5. Doubnerová, V., Ryšlavá, H.: What can enzymes of C4 photosynthesis do for C3 plants under stress? - Plant Sci. 180: 575-583, 2011. Go to original source...
  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. Go to original source...
  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.]
  8. Hatch, M.D., Slack, C.R.: Pyruvate, Pi dikinase from leaves. - Methods Enzymol. 42: 212-219, 1975. Go to original source...
  9. Hibberd, J.M., Quick, W.P.: Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. - Nature 415: 451-454, 2002. Go to original source...
  10. HLJTR (Hei-Long-Jiang-Tu-Rang editing committee): [Soil of Heilongjiang Province.] - China Agr. Press, Beijing 1993 [In Chin.]
  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. Go to original source...
  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. Go to original source...
  13. Lao, J.: [Soil Agrochemistry Analysis Manual.] - China Agr. Press, Beijing 1988. [In Chin.]
  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.]
  15. Munns, R., Termaat, A.: Whole plant response to salinity. - Aust. J. Plant Physiol. 13: 143-160, 1986. Go to original source...
  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. Go to original source...
  17. Pan, R.Z.: [Plant Physiology.] 5th Ed. - Higher Education Press, Beijing 2004. [In Chin.]
  18. Parida, A.K. and Das, A.B.: Salt tolerance and salinity effects on plants: a review. - Ecotoxicol. Environ. Safety 60: 324-349, 2005. Go to original source...
  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. Go to original source...
  20. Sage, R. F.: The evolution of C4 photosynthesis. - New Phytol. 161: 341-370, 2004. Go to original source...
  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. Go to original source...
  22. Schaedle, M., Brayman, A.: Ribulose-1,5-bisphosphate carboxylase activity of Populus tremuloides Michx. bark tissues. - Tree Physiol. 1: 53-56, 1986. Go to original source...
  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. Go to original source...
  24. Tang, H., Liu, S.: [The list of C4 plants in Neimongol area.] - Acta Sci. Natur. Univ. Neimongol 32: 431-438, 2001. [In Chin.]
  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. Go to original source...
  26. Voznesenskaya, E., Franceschi, V., Kiirats, O. et al.: Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. - Nature 414: 543-546, 2001. Go to original source...
  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.]
  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. Go to original source...
  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.
  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. Go to original source...
  31. Wild, A.: Soils, Land and Food: Managing the Land during the twenty-first Century. - Cambridge Univ. Press, Cambridge 2003. Go to original source...
  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.]
  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.]
  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. Go to original source...
  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. Go to original source...
  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.]