MECHANISM OF SALT TOLERANCE IN Vitex trifolia linn. var. simplicifolia Cham: ION HOMEOSTASIS, OSMOTIC BALANCE, ANTIOXIDANT CAPACITY AND PHOTOSYNTHESIS

DeJie Yin

Shandong Jianzhu University, Jinan, 250101, China

FengQin Bu

Shandong Jianzhu University, Jinan, 250101, China

YanFang Xu

Shandong Jianzhu University, Jinan, 250101, China

DeYu Mu

Shandong Jianzhu University, Jinan, 250101, China

Qiang Chen

Shandong Jianzhu University, Jinan, 250101, China

Jie Zhang

Shandong Jianzhu University, Jinan, 250101, China

Jia Guo

National Engineering Research Center for Floriculture, Beijing Forestry University, Beijing, 10083, China


Abstract

Vitex trifolia Linn. var. simplicifolia Cham is a medicinal aromatic plant and perennial halophyte growing in the coastal areas around the Bohai Sea in China. The aim of this study was to investigate the salt tolerance mechanisms of V. trifolia when subjected to different concentrations of NaCl (0, 90, 180, 270, 360 and 450 mM) by measuring growth parameters, ion contents, proline, soluble sugar, soluble protein, malondialdehyde (MDA), photosynthetic pigment contents, chlorophyll fluorescence parameters and antioxidant enzyme activities. The plants died when the NaCl concentration reached 450 mM 20 days after salt stress. Biomass and shoot growth were inhibited by increasing salinity, while root growth was promoted at a NaCl concentration ranging from 90 to 270 mM. Na+ and Cl accumulation was markedly promoted in both leaves and roots with increasing salinity, while no significant changes were observed in the K+ concentration and K+/Na+ ratio in the leaves. Proline, soluble sugar and soluble protein contents increased significantly with increasing salinity. In order to eliminate the reactive oxygen species (ROS) produced by salt-induced oxidative stress, the activities of peroxidase (POD), catalase (CAT) and ascorbate peroxidase (APX) were enhanced. Photosynthetic pigment contents and PSII activity did not significantly decrease under salt stress. The results indicate that the mechanism of salt tolerance in V. trifolia are by ion homeostasis, osmotic balance, antioxidant enzyme induction and photosynthesis adjustment.

Keywords:

antioxidant enzymes, ion homeostasis, osmotic balance, photosynthesis, salt tolerance

Aebi, H. (1984). Catalase in vitro. In: Methods in enzymology, Fleischer, S., Fleischer, B. (eds.). Academic Press, Salt Lake City, pp. 121–126.

Amor, N.B., Hamed, K.B., Debez, A., Grignon, C., Abdelly, C. (2005). Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity. Plant Sci., 168(4), 889–899. https://doi.org/10.1016/j.plantsci.2004.11.002

Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., Wang, L.C. (2017). Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front. Plant Sci., 8, 69. https://doi.org/10.3389/fpls.2017.00069

Ashraf, U., Hussain, S., Anjum, S.A., Abbas, F., Tanveer, M., Noor, M.A., Tang, X. (2017). Alterations in growth, oxidative damage, and metal uptake of five aromatic rice cultivars under lead toxicity. Plant Physiol. Biochem., 115, 461–471. https://doi.org/10.1016/j.plaphy.2017.04.019

Azri, W., Barhoumi, Z., Chibani, F., Borji, M., Bessrour, M., Mliki, A. (2016). Proteomic responses in shoots of the facultative halophyte Aeluropus littoralis (Poaceae) under NaCl salt stress. Funct. Plant Biol., 43(11), 1028–1047. https://doi.org/10.1071/FP16114

Bates, L.S., Waldren, R.P., Teare, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil, 39(1), 205–207.

Becker, V.I., Goessling, J.W., Duarte, B., Caçador, I., Liu, F., Rosenqvist, E., Jacobsen, S.E. (2017). Combined effects of soil salinity and high temperature on photosynthesis and growth of quinoa plants (Chenopodium quinoa). Funct. Plant Biol., 44(7), 665–678. https://doi.org/10.1071/FP16370

Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72(1–2), 248–254. https://doi.org/10.1006/abio.1976.9999

Bueno, M., Lendínez, M.L., Aparicio, C., Cordovilla, M.P. (2015). Effect of salinity on polyamines and ethylene in Atriplex prostrata and Plantago coronopus. Biol. Plantarum, 59(3), 596–600. https://doi.org/10.1007/s10535-015-0510-5

Chaves, M.M., Flexas, J., Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. – London, 103(4), 551–560. https://doi.org/10.1093/aob/mcn125

Chen, P., Yan, K., Shao, H., Zhao, S. (2013). Physiological mechanisms for high salt tolerance in wild soybean (Glycine soja) from yellow river delta, China: photosynthesis, osmotic regulation, ion flux and antioxidant capacity. Plos One., 8(12), e83227. https://doi.org/10.1371/journal.pone.0083227

Duarte, B., Santos, D., Marques, J.C., Caçador, I. (2013). Ecophysiological adaptations of two halophytes to salt stress: photosynthesis, PS II photochemistry and anti-oxidant feedback-implications for resilience in climate change. Plant Physiol. Biochem., 67, 178–188. https://doi.org/10.1016/j.plaphy.2013.03.004

Flowers, T.J., Colmer, T.D. (2008). Salinity tolerance in halophytes. New Phytol., 945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x

Genty, B., Briantais, J.M., Baker, N.R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen. Subjects, 990(1), 87–92. https://doi.org/10.1016/S0304-4165(89)80016-9

Guo, Y., Tan, J. (2015). Recent advances in the application of chlorophyll a fluorescence from photosystem II. Photochem. Photobiol., 91(1), 1–14. https://doi.org/10.1111/php.12362

Hamdani, F., Derridj, A., Rogers, H.J. (2017). Multiple mechanisms mediate growth and survival in young seedlings of two populations of the halophyte Atriplex halimus (L.) subjected to long single-step salinity treatments. Funct. Plant Biol., 44(8), 761–773. https://doi.org/10.1071/FP17026

Hoffmann, W.A., Poorter, H. (2002). Avoiding bias in calculations of relative growth rate. Ann. Bot. – London, 90(1), 37–42. https://doi.org/10.1093/aob/mcf140

Huchzermeyer, B., Flowers, T. (2013). Putting halophytes to work-genetics, biochemistry and physiology. Funct. Plant Biol., 40, V-VIII. https://doi.org/10.1071/FPv40n9_FO

Joseph, B., Jini, D., Sujatha, S. (2011). Development of salt stress-tolerant plants by gene manipulation of antioxidant enzymes. Asian J. Agric. Res., 5(1), 17–27. https://doi.org/10.3923/ajar.2011.17.27

Li, H.S., Sun, Q., Zhao, S.J., Zhang, W.H. (2000). Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing, pp. 195–197.

Lichtenthaler, H.K., Wellburn, A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. T., 11, 591–592.

Liu, X., Duan, D., Li, W., Tadano, T., Khan, M.A. (2008). A comparative study on responses of growth and solute composition in halophytes Suaeda salsa and Limonium bicolor to salinity. In: Ecophysiology of high salinity tolerant plants. Springer, Dordrecht, pp. 135–143. https://doi.org/10.1007/1-4020-4018-0_9

Llanes, A., Masciarelli, O., Ordoñez, R., Isla, M.I., Luna, V. (2014). Differential growth responses to sodium salts involve different abscisic acid metabolism and transport in Prosopis strombulifera. Biol. Plant., 58(1), 80–88. https://doi.org/10.1007/s10535-013-0365-6

Mansour, M.M.F., Ali, E.F. (2017). Evaluation of proline functions in saline conditions. Phytochemistry, 140, 52–68. https://doi.org/10.1016/j.phytochem.2017.04.016

Megdiche, W., Amor, N.B., Debez, A., Hessini, K., Ksouri, R., Zuily-Fodil, Y., Abdelly, C. (2007). Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiol. Plant., 29(4), 375–384. https://doi.org/10.1007/s11738-007-0047-0

Muchate, N.S., Nikalje, G.C., Rajurkar, N.S., Suprasanna, P., Nikam, T.D. (2016). Physiological responses of the halophyte Sesuvium portulacastrum to salt stress and their relevance for saline soil bio-reclamation. Flora, 224, 96–105. https://doi.org/10.1016/j.flora.2016.07.009

Nakano, Y., Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol., 22(5), 867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Oukarroum, A., Bussotti, F., Goltsev, V., Kalaji, H.M. (2015). 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. https://doi.org/10.1016/j.envexpbot.2014.08.005

Percey, W.J., McMinn, A., Bose, J., Breadmore, M.C., Guijt, R.M., Shabala, S. (2016). Salinity effects on chloroplast PSII performance in glycophytes and halophytes. Funct. Plant Biol., 43(11), 1003–1015. https://doi.org/10.1071/FP16135

Percey, W.J., Shabala, L., Wu, Q., Su, N., Breadmore, M.C., Guijt, R.M. (2016). Potassium retention in leaf mesophyll as an element of salinity tissue tolerance in halophytes. Plant Physiol. Biochem., 109, 346–354. https://doi.org/10.1016/j.plaphy.2016.10.011

Pérez-López, U., Robredo, A., Lacuesta, M., Sgherri, C., Muñoz-Rueda, A., Navari-Izzo, F., Mena-Petite, A. (2009). The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2. Physiol. Plant., 135(1), 29–42. https://doi.org/10.1111/j.1399-3054.2008.01174.x

Qi, B.J., Wang, J.D., Zhang, Y.C. (2013). Comparison and validation of different methods for determination of chloride in sweet potatoes (Ipomoea batatas L.) different in cultivar. Acta Pedol. Sin., 50, 584–590. https://doi.org/10.1007/s13197-017-2510-2

Qiu, N., Lu, Q., Lu, C. (2003). Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica. New Phytol., 159(2), 479–486. https://doi.org/10.1046/j.1469-8137.2003.00825.x

Rajaravindran, M., Natarajan, S. (2012). Effects of salinity stress on growth and biochemical constituents of the halophyte Sesuvium portulacastrum. Int. J. Res. Biol. Sci., 2(1), 18–25.

Ramani, B., Reeck, T., Debez, A., Stelzer, R., Huchzermeyer, B., Schmidt, A., Papenbrock, J. (2006). Aster tripolium L. and Sesuvium portulacastrum L.: two halophytes, two strategies to survive in saline habitats. Plant Physiol. Biochem., 44(5–6), 395–408. https://doi.org/10.1016/j.plaphy.2006.06.007

Schreiber, U., Schliwa, U., Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res., 10(1–2), 51–62. https://doi.org/10.1007/BF00024185

Sekmen, A.H., Türkan, I., Takio, S. (2007). Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol. Plant., 131(3), 399–411. https://doi.org/10.1111/j.1399-3054.2007.00970.x

Shabala, S. (2013). Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot. – London, 112(7), 1209–1221. https://doi.org/10.1093/aob/mct205

Shabala, S., Mackay, A. (2011). Ion transport in halophytes. In: Advances in botanical research., Callow, J.A. (eds.). Academic Press, Salt Lake City, pp. 151–199. https://doi.org/10.1016/B978-0-12-387692-8.00005-9

Singh, M., Kumar, J., Singh, S., Singh, V.P., Prasad, S.M. (2015). Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev. Environ. Sci. Biotechnol., 14(3), 407–426. https://doi.org/10.1007/s11157-015-9372-8

Slama, I., Abdelly, C., Bouchereau, A., Flowers, T., Savoure, A. (2015). Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. – London, 115(3), 433–447. https://doi.org/10.1093/aob/mcu239

Van Kooten, O., Snel, J.F. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res., 25(3), 147–150. https://doi.org/10.1007/BF00033156

Xu, L.H., Wang, W.Y., Guo, J.J., Qin, J., Shi, D.Q., Li, Y.L., Xu, J. (2014). Zinc improves salt tolerance by increasing reactive oxygen species scavenging and reducing Na+ accumulation in wheat seedlings. Biol. Plant., 58(4), 751–757. https://doi.org/10.1007/s10535-014-0442-5

Yıldıztugay, E., Sekmen, A.H., Turkan, I., Kucukoduk, M. (2011). Elucidation of physiological and biochemical mechanisms of an endemic halophyte Centaurea tuzgoluensis under salt stress. Plant Physiol. Bioch., 49(8), 816–824. https://doi.org/10.1016/j.plaphy.2011.01.021

Zhao, K.F., Li, F.Z., Zhang, F.S. (2013). Chinese Halophyte. In: Zhao, K.F., Li, F.Z. (eds.). Science Press, Beijing, pp. 101–105.

Zhou, W., Leul, M. (1999). Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul., 27(2), 99–104. https://doi.org/10.1023/A:1006165603300

Zhu, G.L., Zhong, H.W., Zhang, A.Q. (1990). Plant physiology experiment. Peking University Press, Beijing, pp. 57–61.

Zinnert, J.C., Nelson, J.D., Hoffman, A.M. (2012). Effects of salinity on physiological responses and the photochemical reflectance index in two co-occurring coastal shrubs. Plant Soil, 354(1–2), 45–55. https://doi.org/10.1007/s11104-011-0955-z

Download

Published
2021-08-31



DeJie Yin 
Shandong Jianzhu University, Jinan, 250101, China
FengQin Bu 
Shandong Jianzhu University, Jinan, 250101, China
YanFang Xu 
Shandong Jianzhu University, Jinan, 250101, China
DeYu Mu 
Shandong Jianzhu University, Jinan, 250101, China
Qiang Chen 
Shandong Jianzhu University, Jinan, 250101, China
Jie Zhang 
Shandong Jianzhu University, Jinan, 250101, China
Jia Guo 
National Engineering Research Center for Floriculture, Beijing Forestry University, Beijing, 10083, China



License

 

Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.

The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.