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Changes in photosynthesis, chlorophyll fluorescence, and antioxidant enzymes of mulberry (Morus ssp.) in response to salinity and high-temperature stress

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Abstract

Photosynthesis, chlorophyll (Chl) fluorescence, and antioxidant enzymes were measured in the mulberry (Morus spp.) cultivars Da 10, Hongguo 2, Anza 1, and Taiwan 72C002, which were subjected to salinity and high-temperature stress (STS; 0.1%, 0.3%, and 0.5% NaCl concentrations, 34.5°C–40.5°C/27.8°C–29.2°C day/night temperatures). Control plants were watered with 1 L of full-strength Hoagland’s nutrient solution with no added NaCl. Net photosynthetic rate (P N), stomatal conductance (g s), and effective quantum yield of photosystem II photochemistry (ΦPSII) increased in Anza 1 and Taiwan 72C002 under 0.1% STS but decreased in Da 10 and Hongguo 2 compared with the control. However, all the above parameters, including Chl content, maximum quantum yield of photosystem II photochemistry (Fv/Fm), nonphotochemical quenching (NPQ), and maximum carboxylation velocity of Rubisco (V cmax, decreased in Taiwan 72C002, Honggua 2, and Da 10 under 0.3% and 0.5% STS, suggesting that photoinhibition occurred under severe STS. Under STS, there were no significant changes in P N, Fv/Fm, ΦPSII, ascorbate peroxidase (APX) activity, superoxide dismutase (SOD) activity, catalase activity, superoxide anion radical (O 2 ) content, malondialdehyde (MDA) content, soluble sugar content (SSC), and leaf biomass in Anza 1 even at 0.5% STS, showing that Anza 1 displays high resistance to STS. In addition, peroxidase activity was significantly higher in Anza 1 than in the other mulberry cultivars. Significant adverse effects of severe salinity on photosynthesis and Chl fluorescence parameters were observed in Da 10. Additionally, SOD, peroxidase, and APX activities were lower in Da 10, whereas O 2 and MDA contents were higher in comparison with the other mulberry cultivars under 0.3% and 0.5% STS, suggesting that Da 10 had low resistance to STS. These results show that 0.1% STS had a positive effect on photosynthesis and Chl fluorescence parameters in Anza 1 and Taiwan 72C002, and higher peroxidase activity can to a certain extent explain the higher STS tolerance in Anza 1. Damages to DSM photosystems might be related to lower SOD, POD, and APX activities, which resulted in the accumulation of reactive oxygen species.

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Abbreviations

APX:

ascorbate peroxidase

AQY:

apparent quantum yield

C a :

atmospheric CO2 concentration

CE:

carboxylation efficiency

C i :

intercellular CO2 concentration

Chl:

chlorophyll

E :

transpiration rate

F0 :

minimum fluorescence level

Fm :

maximum fluorescence level

Fv/Fm :

maximum quantum yield of photosystem II photochemistry

FS :

steady-state yield of PSII fluorescence in the light

g s :

stomatal conductance

Ls :

stomatal limitation value

MDA:

malondialdehyde

NPQ:

non-photochemical quenching

O 2 :

superoxide anion radical

PAR:

photosynthetically active radiation

P N :

net photosynthetic rate

PPBS:

potassium phosphate buffer solution

PSII:

photosystem II

ΦPSII :

effective quantum yield of photosystem II photochemistry

qp :

photochemical quenching coefficient

ROS:

reactive oxygen species

SOD:

superoxide dismutase

SSC:

soluble sugar content

STS:

salinity and high-temperature stress

V cmax :

maximum carboxylation velocity of Rubisco

References

  • Aebi H. 1974. Catalase, pp. 673–677. In: Bergmeyer H.U. (ed.), Methods of Enzymatic Analysis, Academic Press, New York.

    Chapter  Google Scholar 

  • Almeselmani M., Deshmukh P.S., Sairam R.K., Kushwaha S.R. & Singh T.P. 2006. Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 171: 382–388.

    Article  PubMed  CAS  Google Scholar 

  • Arnon D.I. 1949. Copper enzymes in isolated chloroplasts: Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24: 1–15.

    Article  PubMed  CAS  Google Scholar 

  • Bates L.S., Waldren R.P. & Teare I.D. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39: 205–207.

    Article  CAS  Google Scholar 

  • Cardini C.E., Leloir L.F. & Chiriboga J. 1955. The biosynthesis of sucrose. J. Biol. Chem. 214: 149–155.

    PubMed  CAS  Google Scholar 

  • Chance B. & Maehly A.C. 1955. Assay of catalases and peroxidases. Method. Enzymol. 2: 746–755.

    Google Scholar 

  • Chen S., Li J., Wang T., Wang S., Polle A. & Hüttermann A. 2002. Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar. J. Plant Growth Regul. 21: 224–233.

    Article  CAS  Google Scholar 

  • Dat J.F., Lopez-Delgado H., Foyer C.H. & Scott I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116: 1351–1357.

    Article  PubMed  CAS  Google Scholar 

  • Elboutahiri N., Thami Alami I., Ibriz M. & Alfaiz C. 2008. The effect of salinity and high temperature on biomass production of some alfalfa landraces. Options Méditerranéennes Série A 79: 293–297.

    Google Scholar 

  • Elstner E.F. & Heupel A. 1976. Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal. Biochem. 70: 616–620.

    Article  PubMed  CAS  Google Scholar 

  • Epstein E., Norlyn J.D., Rush D.W., Kingsbury R.W., Kelley D.B., Cunningham G.A. & Wrona A.F. 1980. Saline culture of crops: A genetic approach. Science 210: 399–404.

    Article  PubMed  CAS  Google Scholar 

  • Esfandiari E., Shekari F., Shekari F. & Esfandiari M. 2007. The effect of salt stress on antioxidant enzymes’ activity and lipid peroxidation on the wheat seedling. Not. Bot. Hort. Agrobot. Cluj. 35: 48–56.

    CAS  Google Scholar 

  • Giannopolitis C.N. & Ries S.K. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 59: 309–314.

    Article  PubMed  CAS  Google Scholar 

  • Harinasut P., Poonsopa D., Roengmongkol K. & Charoensataporn R. 2003. Salinity effects on antioxidant enzymes in mulberry cultivar. Science Asia 29: 109–113.

    Article  CAS  Google Scholar 

  • Harinasut P., Srisunak S., Pitukchaisopol S. & Charoensataporn R. 2000. Mechanisms of adaptation to increasing salinity of mulberry: Proline content and ascorbate peroxidase activity in leaves of multiple shoots. Science Asia 26: 207–211.

    Article  CAS  Google Scholar 

  • Henley W.J., Major K.M. & Hironaka J.L. 2002. Response to salinity and heat stress in two halotolerant chlorophyte algae. J. Phycol. 38: 757–766.

    Article  Google Scholar 

  • Hichem H., El Naceur A. & Mounir D. 2009. 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.

    Article  CAS  Google Scholar 

  • Hodges D.M., DeLong J.M., Forney C.F. & Prange R.K. 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604–611.

    Article  CAS  Google Scholar 

  • Jia Z.S., Tang M.C., Wu J.M. 1999. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem. 64: 555–559

    Article  Google Scholar 

  • Knight H. & Knight M.R. 2001. Abiotic stress signalling pathways: Specificity and cross-talk. Trends Plant Sci. 6: 262–267.

    Article  PubMed  CAS  Google Scholar 

  • Koca H., Bor M., Özdemir F. & Türkan I. 2007. The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ. Exp. Bot. 60: 344–351.

    Article  CAS  Google Scholar 

  • Li Z.G. & Gong M. 2005. Improvement of measurement method for superoxide anion radical in plant. Acta Bot. Yunnan. 27: 211–216.

    CAS  Google Scholar 

  • Lu C., Qiu N., Wang B. & Zhang J. 2003. Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J. Exp. Bot. 54: 851–860.

    Article  PubMed  CAS  Google Scholar 

  • Lu C.M., Qiu N.W., Lu Q.T., Wang B.S. & Kuang T.Y. 2002. Does salt stress lead to increased susceptibility of photosystem II to photoinhibition and changes in photosynthetic pigment composition in halophyte Suaeda salsa grown outdoors? Plant Sci. 163: 1063–1068.

    Article  CAS  Google Scholar 

  • Maricle B.R., Lee R.W., Hellquist C.E., Kiirats O. & Edwards G.E. 2007. Effects of salinity on chlorophyll fluorescence and CO2 fixation in C4 estuarine grasses. Photosynthetica 45: 433–440.

    Article  CAS  Google Scholar 

  • Masojídek J., Torzillo G., Kopecky J., Koblížek M., Nidiaci L., Komenda J., Lukavská A. & Sacchi A. 2000. Changes in chlorophyll fluorescence quenching and pigment composition in the green alga Chlorococcum sp. grown under nitrogen deficiency and salinity stress. J. Appl. Phycol. 12: 417–426.

    Article  Google Scholar 

  • McMurtrie R.E. & Wang Y.P. 1993. Mathematical models of the photosynthetic responses of tree stands to rising CO2 concentrations and temperatures. Plant Cell Environ. 16: 1–13.

    Article  CAS  Google Scholar 

  • Mishra R.K. & Singhal G.S. 1993. Photosynthetic activity and peroxidation of thylakoid lipids during photoinhibition and high temperature treatment of isolated wheat chloroplasts. J. Plant Physiol. 141: 286–292.

    Article  CAS  Google Scholar 

  • Nagesh Babu R. & Devaraj V.R. 2008. High temperature and salt stress response in French bean (Phaseolus vulgaris). Aust. J. Crop Sci. 2: 40–48

    Google Scholar 

  • Nakano Y. & Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22: 867–880.

    CAS  Google Scholar 

  • Norlyn J.D. & Epstein E. 1984. Variability in salt tolerance of four triticale lines at germination and emergence. Crop Sci. 24: 1090–1092.

    Article  Google Scholar 

  • Pospíšil P. 2009. Production of reactive oxygen species by photosystem II. BBA-Bioenergetics 1787: 1151–1160.

    Article  PubMed  Google Scholar 

  • Qin J., Dong W.Y., He K.N., Chen J., Liu J. & Wang Z.L. 2010. Physiological responses to salinity in Silver buffaloberry (Shepherdia argentea) introduced to Qinghai high-cold and saline area, China. Photosynthetica 48: 51–58.

    Article  Google Scholar 

  • Qin L.Q., Li L., Bi C., Zhang Y.L., Wan S.B., Meng J.J., Meng Q.W. & Li X.G. 2011. Damaging mechanisms of chilling- and salt stress to Arachis hypogaea L. leaves. Photosynthetica 49: 37–42.

    Article  CAS  Google Scholar 

  • Qiu N. & Lu C. 2003. Enhanced tolerance of photosynthesis against high temperature damage in salt-adapted halophyte Atriplex centralasiatica plants. Plant Cell Environ. 26: 1137–1145.

    Article  Google Scholar 

  • Rizhsky L., Liang H.J., Shuman J., Shulaev V., Davletova S. & Mittler R. 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134: 1683–1696.

    Article  PubMed  CAS  Google Scholar 

  • Roháček K. 2002. Chlorophyll fluorescence parameters: The definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40: 13–29.

    Article  Google Scholar 

  • Stoeva N. & Kaymakanova M. 2008. Effect of salt stress on the growth and photosynthesis rate of bean plants (Phaseolus vulgaris L.). J. Centr. Eur. Agr. 9: 385–391.

    Google Scholar 

  • Sui N., Li M., Li K., Song J. & Wang B.S. 2010. Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48: 623–629.

    Article  CAS  Google Scholar 

  • Tiwari A. & Pospíšil P. 2009. Superoxide oxidase and reductase activity of cytochrome b559 in photosystem II. BBA-Bioenergetics 1787: 985–994.

    Article  PubMed  CAS  Google Scholar 

  • Tsugane K., Koboyashi K., Niwa Y., Ohba Y., Wada K. & Kobayashi H. 1999. A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11: 1195–1206.

    PubMed  CAS  Google Scholar 

  • Wang R.G., Chen S.L., Deng L., Fritz E., Hüttermann A. & Polle A. 2007. Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees-Struct. Funct. 21: 581–591.

    Article  CAS  Google Scholar 

  • Xu H.L., Wang R., Gauthier L. & Gosselin A. 1999. Tomato leaf photosynthetic responses to humidity and temperature under salinity and water deficit. Pedosphere 9: 105–112.

    Google Scholar 

  • Xu Z.Z. & Zhou G.S. 2006. Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. Planta 224: 1080–1090.

    Article  PubMed  CAS  Google Scholar 

  • Yin C.Y., Berninger F. & Li C.Y. 2006. Photosynthetic responses of Populus przewalski subjected to drought stress. Photosynthetica 44: 62–68.

    Article  Google Scholar 

  • Zheng Y.H., Xu X.B., Wang M.Y., Zheng X.H., Li Z.J. & Jiang G.M. 2009. Responses of salt-tolerant and intolerant wheat genotypes to sodium chloride: Photosynthesis, antioxidants activities, and yield. Photosynthetica 47: 87–94.

    Article  CAS  Google Scholar 

  • Zhu J.K. 2001a. Plant salt tolerance. Trends Plant Sci. 6: 66–71.

    Article  PubMed  CAS  Google Scholar 

  • Zhu J.K. 2001b. Cell signaling under salt, water and cold stresses. Curr. Opin. Plant Biol. 4: 401–406.

    Article  PubMed  CAS  Google Scholar 

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Yu, C., Huang, S., Hu, X. et al. Changes in photosynthesis, chlorophyll fluorescence, and antioxidant enzymes of mulberry (Morus ssp.) in response to salinity and high-temperature stress. Biologia 68, 404–413 (2013). https://doi.org/10.2478/s11756-013-0167-5

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