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Photosynthetica

, Volume 52, Issue 4, pp 484–492 | Cite as

Effects of salinity on temperature-dependent photosynthetic parameters of a native C3 and a non-native C4 marsh grass in the Yangtze Estuary, China

  • Z. -M. Ge
  • L. -Q. Zhang
  • L. Yuan
  • C. Zhang
Original Papers

Abstract

The invasion of Spartina alterniflora along the coasts of China has allowed this C4 grass to outcompete often much of the native, salt marsh vegetation, such as Phragmites australis (C3 grass), in the Yangtze Estuary. In this study, native grass, P. australis, and non-native grass, S. alterniflora, were grown in fresh and saline water (moderate salinity of 15‰ and high salinity of 30‰) to compare the effects of salinity on photosynthetic and biochemical parameters in combination with measurement temperatures. The C4 grass, S. alterniflora, showed a greater CO2 assimilation rate than P. australis, across the tested temperatures. The net photosynthetic rate declined significantly with increasing salinity as a result of inhibited stomatal conductance together with a greater decrease in the maximum rate of electron transport (J max). In P. australis, salt treatments shifted the optimum temperatures for the maximum rate of carboxylation by Rubisco (V cmax) and J max to lower temperatures. S. alterniflora showed a greater salt tolerance to moderate stress than that of the native grass, with lower sensitivity of V cmax, J max, and the maximum rate of phosphoenolpyruvate carboxylation. Both moderate and high stress decreased significantly stomatal conductance of S. alterniflora; high salinity reduced significantly photosynthetic efficiency and J max. Our findings indicated that the combination of stomatal conductance, enzyme activity, and electron transport affected the photosynthetic performance of the plants in response to salt treatments. The success of S. alterniflora could be probably attributed to its C4 photosynthetic pathway and the tolerance to moderate salinity. In this study, a modified parameterization of the photosynthetic model was suggested to support a more reasonable simulation of photosynthesis under salt stress.

Additional key words

carboxylation efficiency coastal wetlands gas exchange invasive species 

Abbreviations

Ca

ambient CO2 concentration

Cc

chloroplast CO2 concentration

Ci

intercellular CO2 concentration

Cm

CO2 concentration in the mesophyll cell

Cs

CO2 concentration at the carboxylation site of Rubisco in the bundle-sheath

gbs

bundle sheath cell conductance

gm

mesophyll conductance

gs

light-saturated stomatal conductance

Ha

enthalpy of activation

Hd

enthalpy of deactivation

HS

high salinity

J, Jt

rate of electron transport for C3 and C4 plants

Jmax

maximum rate of electron transport

Kc, Ko

Rubisco Michaelis constants for CO2 and O2

Kp

Michaelis-Menten constants for PEP carboxylation

MS

moderate salinity

O

O2 concentration

PEP

phosphoenolpyruvate

PEPC

phosphoenolpyruvate carboxylase

PN

net photosynthetic rate

PNsat

light-saturated net photosynthetic rate

R

molar gas constant

RD

dark respiration

RH

relative humidity

Rm

mitochondrial respiration in the mesophyll

RuBP

ribulose-1,5-bisphosphate

ΔS

entropy of the desaturation equilibrium

Sc/o

reciprocal of Rubisco specificity

TL

the leaf temperature

Vc

rate of Rubisco carboxylation

Vcmax

maximum rate of carboxylation by Rubisco

Vp

rate of PEP carboxylation

Vpmax

maximum rate of PEP carboxylation

α

quantum efficiency

α1

photosynthetically active irradiance absorbed by PSII

γ*

half of S c/o

θ

curvature of the light response curve

Γ*

CO2 compensation point (absence of dark respiration)

χ

partitioning factor of electron transport

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References

  1. Agastian, P., Kingsley, S.J., Vivekanandan, M.: Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes. — Photosynthetica 38: 287–290, 2000.CrossRefGoogle Scholar
  2. Bernacchi, C.J., Singsaas, E.L., Pimentel, C. et al.: Improved temperature response functions for models of Rubisco-limited photosynthesis. — Plant Cell Environ. 24: 253–259, 2001.CrossRefGoogle Scholar
  3. Bernacchi, C.J., Portis, A.R., Nakano, H. et al.: Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. — Plant Physiol. 130: 1992–1998, 2002.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Burdick, D.M., Buchsbaum, R., Holt, E.: Variation in soil salinity associated with expansion of Phragmites australis in salt marshes. — Environ. Exp. Bot. 46: 247–261, 2001.CrossRefGoogle Scholar
  5. Centritto, M., Loreto, F., Chartzoulakis, K.: The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. — Plant Cell Environ. 26: 585–594, 2003.CrossRefGoogle Scholar
  6. Chambers, R.M., Mozdzer, T.J., Ambrose, J.C.: Effects of salinity and sulfide on the distribution of Phragmites australis and Spartina alterniflora in a tidal saltmarsh. — Aquat. Bot. 62: 161–169, 1998.CrossRefGoogle Scholar
  7. Cousins, A.B., Ghannoum, O., von Caemmerer, S., Badger, M.R.: Simultaneous determination of Rubisco carboxylase and oxygenase kinetic parameters in Triticum aestivum and Zea mays using membrane inlet mass spectrometry. — Plant Cell Environ. 33: 444–452, 2010.PubMedCrossRefGoogle Scholar
  8. Crafts-Brandner, S.J., Salvucci, M.E.: Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. — Plant Physiol. 129: 1773–1780, 2002.PubMedCentralPubMedCrossRefGoogle Scholar
  9. Dadkhah, A.: Effect of salinity on growth and leaf photosynthesis of two sugar beet (Beta vulgaris L.) cultivars. — J. Agr. Sci. Tech. 13: 1001–1012, 2011.Google Scholar
  10. Deng, Ch., Zhang, G., Pan, X.: Photosynthetic responses in Reed (Phragmites australis (CAV.) TRIN. ex Steud.) seedlings induced by different salinity-alkalinity and nitrogen levels. — J. Agr. Sci. Tech. 13: 687–699, 2011.Google Scholar
  11. Desingh, R., Kanagaraj, G.: Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. — Gen. Appl. Plant Physiol. 33: 221–234, 2007.Google Scholar
  12. Farquhar, G.D., von Caemmerer, S., Berry, J.A.: A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. — Planta 149: 78–90, 1980.PubMedCrossRefGoogle Scholar
  13. Farquhar, G.D., von Caemmerer, S.: Modelling of photosynthetic responses to environmental conditions. — In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (ed.): Physiological Plant Ecology. II. Encyclopedia of Plant Physiology. New Series. Vol. 12B. Pp. 548–577. Springer-Verlag, Berlin 1982.Google Scholar
  14. Farquhar, G.D., Wong, S.C.: An empirical model of stomatal conductance. — Aust. J. Plant. Physiol. 11: 191–209, 1984.CrossRefGoogle Scholar
  15. Farquhar, G.D., von Caemmerer, S., Berry, J.A.: Models of photosynthesis. — Plant Physiol. 125: 42–45, 2001.PubMedCentralPubMedCrossRefGoogle Scholar
  16. Flowers, T.J., Troke, P.F., Yeo, A.R.: The mechanism of salt tolerance in halophytes. — Annu. Rev. Plant Phys. 28: 89–121, 1977.CrossRefGoogle Scholar
  17. Ge, Z.M., Zhou, X., Wang, K. et al.: [Research methodology on carbon pool dynamics in the typical wetland of Yangtze River estuary.] — Acta Ecolog. Sin. 30: 1097–1108, 2010. [In Chinese]Google Scholar
  18. Ge, Z.M., Zhou, X., Kellomäki, S. et al.: Acclimation of photosynthesis in a boreal grass (Phalaris arundinacea L.) under different temperature, CO2, and soil water regimes. — Photosynthetica 50: 141–151, 2012.CrossRefGoogle Scholar
  19. He, X.J., Chen, J.Q., Zhang, Z.G. et al.: Identification of saltstress responsive genes in rice (Oryza sativa L.) by cDNA array. — Sci. China Ser B 45: 477–484, 2002.CrossRefGoogle Scholar
  20. He, Y., Yu, C.L., Zhou, L. et al.: Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max) under salt stress. — Plant Physiol. Bioch. 74: 118–124, 2014.CrossRefGoogle Scholar
  21. Hichem, H., Naceur, El A., Mounir, D.: Effects of salt stress on photosynthesis, PSII photochemistry and thermal energy dissipation in leaves of two corn (Zea mays L.) varieties. — Photosynthetica 47: 517–526, 2009.CrossRefGoogle Scholar
  22. Huang, H.M., Zhang, L.Q.: A study on the population dynamics of Spartina alterniflora at Jiuduansha Shoals, Shanghai, China. — Ecol. Eng. 29: 164–172, 2007.CrossRefGoogle Scholar
  23. Kubien, D.S., von Caemmerer, S., Furbank, R.T., Sage, R.F.: C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. — Plant Physiol. 132: 1577–1585, 2003.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Leuning, R.: Temperature dependence of two parameters in a photosynthesis model. — Plant Cell Environ. 25: 1205–1210, 2002.CrossRefGoogle Scholar
  25. Li, H.P., Zhang, L.Q., Wang, D.H.: A study on the distribution of an exotic plant Spartina alterniflora in Shanghai. — Biodivers. Sci. 14: 114–120, 2006.CrossRefGoogle Scholar
  26. Li, J.Y., Zhao, C.Y., Li, J. et al.: Growth and leaf gas exchange in Populus euphratica across soil water and salinity gradients. — Photosynthetica 51: 321–329, 2013.CrossRefGoogle Scholar
  27. Long, S.P., Ainsworth, E.H., Rogers, A., Ort, D.R.: Rising atmospheric carbon dioxide: plants face the future. — Annu. Rev. Plant Biol. 55: 591–628, 2004.PubMedCrossRefGoogle Scholar
  28. Maricle, B.R., Lee, R.W., Hellquist, C.E. et al.: Effects of salinity on chlorophyll fluorescence and CO2 fixation in C4 estuarine grasses. — Photosynthetica 45: 433–440, 2007.CrossRefGoogle Scholar
  29. Massad, R.S., Tuzet, A., Bethenod, O.: The effect of temperature on C4-type leaf photosynthesis parameters. — Plant Cell Environ. 30: 1191–1204, 2007.PubMedCrossRefGoogle Scholar
  30. Meinzer, F.C., Zhu, J.: Efficiency of C4 photosynthesis in Atriplex lentiformis under salinity stress. — Aust. J. Plant Physiol. 26: 79–86, 1999.CrossRefGoogle Scholar
  31. Munns, R., Tester, M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.PubMedCrossRefGoogle Scholar
  32. Naz, N., Hameed, M., Ashraf, M. et al.: Relationships between gas-exchange characteristics and stomatal structural modifications in some desert grasses under high salinity. — Photosynthetica 48: 446–456, 2010.CrossRefGoogle Scholar
  33. Rout, N.P., Shaw, B.P.: Salt tolerance in aquatic macrophytes: Ionic relation and interaction. — Biol. Plantarum 55: 91–95, 2001.Google Scholar
  34. Saha, A.K., Saha, S., Sadle, J. et al.: Sea level rise and South Florida coastal forests. — Climatic Change 107: 81–108, 2011.CrossRefGoogle Scholar
  35. Sharkey, T.D., Bernacchi, C.J., Farquhar, G.D., Singsaas, E.L.: Fitting photosynthetic carbon dioxide response curves for C3 leaves. — Plant Cell Environ. 30: 1035–1040, 2007.PubMedCrossRefGoogle Scholar
  36. Sudhir, P., Murthy, S.D.S.: Effects of salt stress on basic processes of photosynthesis. — Photosynthetica 42: 481–486, 2004.CrossRefGoogle Scholar
  37. Vasquez, E.A., Glenn, E.P., Guntenspergen, G.R. et al.: Salt tolerance and osmotic adjustment of Spartina alterniflora (Poaceae) and the invasive M haplotype of Phragmites australis (Poaceae) along a salinity gradient. — Am. J. Bot. 93:1784–1790, 2006.PubMedCrossRefGoogle Scholar
  38. von Caemmerer, S., Furbank, R.T.: Modeling C4 photosynthesis. — In: Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology. Pp. 173–211. Academic Press, Toronto 1999.CrossRefGoogle Scholar
  39. Wang, H.M., Wang, W.J., Wang, H.Z. et al.: Effect of inland saltalkaline stress on C4 enzymes, pigments, antioxidant enzymes, and photosynthesis in leaf, bark, and branch chlorenchyma of poplars. — Photosynthetica 51: 115–126, 2013.CrossRefGoogle Scholar
  40. Wu, Z.H., Yang, C.W., Yang, M.Y.: Photosynthesis, photosystem II efficiency, amino acid metabolism and ion distribution in rice (Oryza sativa L.) in response to alkaline stress. — Photosynthetica 52: 157–160, 2014.CrossRefGoogle Scholar
  41. Yin, X.Y., Sun, Z.P., Struik, P.C. et al.: Using a biochemical C4 photosynthesis model and combined gas exchange and chlorophyll fluorescence measurements to estimate bundle-sheath conductance of maize leaves differing in age and nitrogen content. — Plant Cell Environ. 34: 2183–2199, 2011.PubMedCrossRefGoogle Scholar
  42. Yu, J.B., Wang, X.H., Ning, K. et al.: Effects of salinity and water depth on germination of Phragmites australis in coastal wetland of the Yellow River Delta. — Clean-Soil Air Water. 40: 1154–1158, 2012.CrossRefGoogle Scholar
  43. Zhang, L.G., Xing, D.: Rapid determination of the damage to photosynthesis caused by salt and osmotic stresses using delayed fluorescence of chloroplasts. — Photochem. Photobiol. Sci. 7: 352–360, 2008.PubMedCrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2014

Authors and Affiliations

  1. 1.State Key Laboratory of Estuarine and Coastal ResearchEast China Normal UniversityShanghaiChina
  2. 2.Key Laboratory of Geographic Information Science (Ministry of Education)East China Normal UniversityShanghaiChina

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