Biologia plantarum 64:519-528, 2020 | DOI: 10.32615/bp.2020.075
Different responses of the halophyte Carex pumila to salt stress
- 1 Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, P.R. China
- 2 University of Chinese Academy of Sciences, Beijing 100049, P.R. China
- 3 Collage of Life Sciences, Shangrao Normal University, Shangrao, Jiangxi 334001, P.R. China
- 4 Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, Hubei 430074, P.R. China
- 5 The Institute of Advanced Studies in Coastal Ecology, Ludong University, Yantai 264000, P.R. China
Salt stress is one of the most important stresses that affect coastal vegetation. A halophyte Carex pumila plays a crucial role in the maintenance of fragile ecosystems in coastal areas. Thus, understanding the mechanism of C. pumila responses to salt stress is a prerequisite for the conservation and utilization of this species. After treatment with 200, 300, 400, 500 mM NaCl for 60 h, C. pumila leaves displayed a decline in the relative water content and an increase in salt injury index. Osmolyte accumulation, as a function of osmotic adjustment, and antioxidant enzyme activities were maintained under salinity, even at a high NaCl concentration. High NaCl concentrations severely affected the photosystem II, the JIP-test indicated a significant decrease in performance indexes and quantum efficiencies and an increase in phenomenological fluxes. Metabolic analyses showed the changes of 39 metabolites, including 16 kinds of organic acids, 9 kinds of amino acids, 9 kinds of sugars, 3 kinds of sugar alcohols, and 2 amines. The identified metabolites were mainly involved in the glycolysis, pentose phosphate pathway, and tricarboxylic acids cycle.
Keywords: antioxidant enzymes, chlorophyll a fluorescence, metabolites, NaCl, osmotic adjustment.
Received: February 28, 2020; Revised: April 29, 2020; Accepted: May 18, 2020; Published online: July 29, 2020 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Supplementary files
| Download file | Wang6441_Suppl.pdf File size: 267.61 kB |
References
- Aghaleh, M., Niknam, V., Ebrahimzadeh, H., Razavi, K.: Salt stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. - Biol. Plant. 53: 243-248, 2009.
Go to original source... - Ahmad, P., Kumar, A., Ashraf, M., Akram, N.A.: Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). - Afr. J. Biotechnol. 11: 2694-2703, 2012.
Go to original source... - Allakhverdiev, S.I., Sakamoto, A., Nishiyama, Y., Inaba, M., Murata, N.: Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. - Plant Physiol. 123: 1047-1056, 2000.
Go to original source... - Alscher, R.G., Erturk, N., Heath, L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. - J. exp. Bot. 53: 1331-1341, 2002.
Go to original source... - Amjad, M., Akhtar, S.S., Yang, A., Akhtar, J., Jacobsen, S.E.: Antioxidative response of quinoa exposed to iso-osmotic, ionic and non-ionic salt stress. - J. Agron. Crop Sci. 201: 452-460, 2015.
Go to original source... - Bela, K., Riyazuddin, R., Horváth, E., Hurton, Á., Gallé, Á., Takács, Z., Zsigmond, L., Szabados, L., Tari, I., Csiszár, J.: Comprehensive analysis of antioxidant mechanisms in Arabidopsis glutathione peroxidase-like mutants under salt-and osmotic stress reveals organ-specific significance of the AtGPXL's activities. - Environ. exp. Bot. 150: 127-140, 2018.
Go to original source... - Bi, A., Fan, J., Hu, Z., Wang, G., Amombo, E., Fu, J., Hu, T.: Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. - Front. Plant Sci. 7: 453-453, 2016.
Go to original source... - Bose, J., Rodrigo-Moreno, A., Shabala, S.: ROS homeostasis in halophytes in the context of salinity stress tolerance. - J. exp. Bot. 65: 1241-1257, 2014.
Go to original source... - Burgess, R.E.: The life history strategy of Carex pumila Thunb. (Cyperaceae), a rhizomatous perennial pioneer species on the sand plains of the dune system of coastal Manawatu. - Dissertations & Theses, Massey University, Palmerston North 1984.
- Chen, C., Liu, H., Wang, C., Liu, Z., Liu, X., Zou, L., Zhao, H., Yan, Y., Shi, J., Chen, S.: Metabolomics characterizes metabolic changes of Apocyni Veneti folium in response to salt stress. - Plant Physiol. Biochem. 144: 187-196, 2019.
Go to original source... - Chen, K., Chen, L., Fan, J., Fu, J.: Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. - Photosynth. Res. 1: 21-31, 2013.
Go to original source... - Chen, T.H., Murata, N.: Glycinebetaine: an effective protectant against abiotic stress in plants. - Trends Plant Sci. 13: 499-505, 2008.
Go to original source... - Corney, H.J., Sasse, J.M., Ades, P.K.: Assessment of salt tolerance in eucalypts using chlorophyll fluorescence attributes. - New Forest. 26: 233-246, 2003.
Go to original source... - D'Amelia, L., Dell'Aversana, E., Woodrow, P., Ciarmiello, L. F., Carillo, P.: Metabolomics for Crop Improvement against Salinity Stress. (Salinity Responses and Tolerance in Plants. Vol. 2.) - Springer-Verlag, Cham - Berlin - Heidelberg 2018.
Go to original source... - Dahdouh-Guebas, F., Koedam, N.: Coastal vegetation and the Asian tsunami. - Science 311: 37-38, 2006.
Go to original source... - Evelin, H., Kapoor, R., Giri, B.: Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. - Ann. Bot. 104: 1263-1280, 2009.
Go to original source... - Fan, J., Ren, J., Zhu, W., Amombo, E., Fu, J., Chen, L.: Antioxidant responses and gene expression in bermudagrass under cold stress. - J. amer. Soc. hort. Sci. 139: 699-705, 2014.
Go to original source... - Feagin, R.A., Mukherjee, N., Shanker, K., Baird, A.H., Cinner, J., Kerr, A.M., Koedam, N., Sridhar, A., Arthur, R., Jayatissa, L.P.: Shelter from the storm? Use and misuse of coastal vegetation bioshields for managing natural disasters. - Conserv, Lett. 3: 1-11, 2010.
Go to original source... - Ferchichi, S., Hessini, K., Dell'Aversana, E., D'Amelia, L., Woodrow, P., Ciarmiello, L.F., Fuggi, A., Carillo, P.: Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites. - Funct. Plant Biol. 45: 1096-1109, 2018.
Go to original source... - Flowers, T.J., Colmer, T.D.: Plant salt tolerance: adaptations in halophytes. - Ann. Bot. 115: 327-331, 2015.
Go to original source... - Foyer, C.H., Noctor, G.: Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. - Plant Cell Environ. 28: 1056-1071, 2005.
Go to original source... - Franzini, V.I., Azcón, R., Ruiz-Lozano, J.M., Aroca, R.: Rhizobial symbiosis modifies root hydraulic properties in bean plants under non-stressed and salinity-stressed conditions. - Planta 249: 1207-1215, 2019.
Go to original source... - Gao, Y.F., Liu, J.K., Yang, F.M., Zhang, G.Y., Wang, D., Zhang, L., Ou, Y.B., Yao, Y.A.: The WRKY transcription factor WRKY8 promotes resistance to pathogen infection and mediates drought and salt stress tolerance in Solanum lycopersicum. - Physiol. Plant. 168: 98-117, 2020.
Go to original source... - Garg, N., Manchanda, G.: ROS generation in plants: boon or bane? - Plant Biosystem. 143: 81-96, 2009.
Go to original source... - Ghatak, A., Chaturvedi, P., Weckwerth, W.: Metabolomics in plant stress physiology. - Adv. Biochem. Eng. Biotechnol. 164: 187-236, 2018.
Go to original source... - Guo, R., Shi, L., Yan, C., Zhong, X., Gu, F., Liu, Q., Xia, X., Li, H.: Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. - BMC Plant Biol. 1: 1-13, 2017.
Go to original source... - Hagemeyer, J. Ecophysiology of plant growth under heavy metal stress. - In: Hagemeyer, J.: Heavy Metal Stress in Plants. Pp. 201-222. Springer-Verlag, Berlin - Heidelberg 1999.
Go to original source... - Hämmerli, A., Reusch, T.: Inbreeding depression influences genet size distribution in a marine angiosperm. - Mol. Ecol. 12: 619-629, 2003.
Go to original source... - Hasanuzzaman, M., Oku, H., Nahar, K., Bhuyan, M.B., Al Mahmud, J., Baluska, F., Fujita, M.: Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. - Plant Biotechnol. Rep. 12: 77-92, 2018.
Go to original source... - Hernández, J.A., Almansa, M.S.: Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. - Physiol. Plant. 115: 251-257, 2002.
Go to original source... - Hoagland, D.R., Arnon, D.I.: The water-culture method for growing plants without soil. - Circular Calif. Agr. Exp. Sta. 347: 1-39, 1950.
- Hope-Simpson, R.B.J.F.: Downs and dunes: their plant life and its environment.by edward salisbury. - J. Ecol. 43: 311-315, 1955.
Go to original source... - Hossain, M.S., Hasanuzzaman, M., Sohag, M.M.H., Bhuyan, M.B., Fujita, M.: Acetate-induced modulation of ascorbate: glutathione cycle and restriction of sodium accumulation in shoot confer salt tolerance in Lens culinaris Medik. - Physiol. mol. Biol. Plants 25: 443-455, 2019.
Go to original source... - Hu, L., Hu, T., Zhang, X., Pang, H., Fu, J.: Exogenous glycine betaine ameliorates the adverse effect of salt stress on perennial ryegrass. - J. amer. Soc. hort. Sci. 137: 38-46, 2012.
Go to original source... - Hu, Z., Fan, J., Xie, Y., Amombo, E., Liu, A., Gitau, M.M., Khaldun, A., Chen, L., Fu, J.: Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. - Plant Physiol. Biochem. 100: 94-104, 2016.
Go to original source... - Iwasato, M., Nagamatsu, D.: Plant species diversity and habitat conditions in a protected large coastal dune area of western Japan. - Lands Ecol. Eng. 14: 99-113, 2018.
Go to original source... - Jenkins, S., Barrett-Lennard, E.G., Rengel, Z.: Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on salt land with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves. - Plant Soil 329: 91-104, 2010.
Go to original source... - Kalaji, H.M., Bosa, K., Koĥcielniak, J., Żuk-Go³aszewska, K.: Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. - Environ. exp. Bot. 73: 64-72, 2011.
Go to original source... - Kumari, A., Das, P., Parida, A.K., Agarwal, P.K.: Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. - Front. Plant Sci. 6: 537-537, 2015.
Go to original source... - Lee, D.H., Kim, Y.S., Lee, C.B.: The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). - J. Plant Physiol. 158: 737-745, 2001.
Go to original source... - Li, Z., Cheng, B., Zeng, W., Zhang, X., Peng, Y.: Proteomic and metabolomic profilings reveal crucial function of γ-aminobutyric acid (GABA) on regulating ionic, water, and metabolic homeostasis in creeping bentgrass under salt stress. - J. Proteome Res. 19: 769-780, 2020.
Go to original source... - Liu, A., Hu, Z., Bi, A., Fan, J., Gitau, M.M., Amombo, E., Chen, L., Fu, J.: Photosynthesis, antioxidant system and gene expression of bermudagrass in response to low temperature and salt stress. - Ecotoxicology 25: 1445-1457, 2016.
Go to original source... - Lu, C., Vonshak, A.: Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. - Physiol. Plant. 114: 405-413, 2002.
Go to original source... - Mansour, M.: Nitrogen containing compounds and adaptation of plants to salinity stress. - Biol. Plant. 43: 491-500, 2000.
Go to original source... - Meng, R., Saade, S., Kurtek, S., Berger, B., Brien, C., Pillen, K., Tester, M., Sun, Y.: Growth curve registration for evaluating salinity tolerance in barley. - Plant Methods 13: 18-18, 2017.
Go to original source... - Morton, M.J., Awlia, M., Al-Tamimi, N., Saade, S., Pailles, Y., Negrão, S., Tester, M. Salt stress under the scalpel-dissecting the genetics of salt tolerance. - Plant J. 97: 148-163, 2019.
Go to original source... - Muchate, N.S., Nikalje, G.C., Rajurkar, N.S., Suprasanna, P., Nikam, T.D.: Physiological responses of the halophyte Sesuvium portulacastrum to salt stress and their relevance for saline soil bio-reclamation. - Flora 224: 96-105, 2016.
Go to original source... - Nazar, R., Iqbal, N., Syeed, S., Khan, N.A.: Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. - J. Plant Physiol. 168: 807-815, 2011.
Go to original source... - Noreen, Z., Ashraf, M., Akram, N. Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). - J. Agron. Crop Sci. 196: 273-285, 2010.
Go to original source... - Parida, A.K., Das, A.B., Mohanty, P.: Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. - J. Plant Physiol. 161: 531-542, 2004.
Go to original source... - Perales-Vela, H.V., González-Moreno, S., Montes-Horcasitas, C., Cañizares-Villanueva, R.O.: Growth, photosynthetic and respiratory responses to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). - Chemosphere 67: 2274-2281, 2007.
Go to original source... - Rangani, J., Parida, A.K., Panda, A., Kumari, A.: Coordinated changes in antioxidative enzymes protect the photosynthetic machinery from salinity induced oxidative damage and confer salt tolerance in an extreme halophyte Salvadora persica L. - Front. Plant Sci. 7: 50-50, 2016.
Go to original source... - Rodgers III, J.C., Murrah, A.W., Cooke, W.H.: The Impact of hurricane Katrina on the coastal vegetation of the Weeks Bay Reserve, Alabama from NDVI data. - Estuaries Coasts 32: 496-507, 2009.
Go to original source... - Rozema, J., Van Manen, Y., Vugts, H., Leusink, A.: Airborne and soilborne salinity and the distribution of coastal and inland species of the genus Elytrigia. - Acta bot. neerl. 32: 447-456, 1983.
Go to original source... - Rybka, K., Nita, Z.: Physiological requirements for wheat ideotypes in response to drought threat. - Acta Physiol. Plant. 37: 97-97, 2015.
Go to original source... - Scandalios, J.G.: Oxygen stress and superoxide dismutases. - Plant Physiol. 101: 7-12, 1993.
Go to original source... - Sekmen, A.H., Turkan, I., Tanyolac, Z.O., Ozfidan, C., Dinc, A.: Different antioxidant defense responses to salt stress during germination and vegetative stages of endemic halophyte Gypsophila oblanceolata BARK. - Environ. exp. Bot. 77: 63-76, 2012.
Go to original source... - Shabala, S.: Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. - Ann. Bot. 112: 1209-1221, 2013.
Go to original source... - Shahverdi M. A., Omidi H, Tabatabaei S. J.: Stevia (Stevia rebaudiana Bertoni) responses to NaCl stress: growth, photosynthetic pigments, diterpene glycosides and ion content in root and shoot. - J. Saudi Soc. agr. Sci. 18: 355-360, 2019.
Go to original source... - Sivritepe, N., Erturk, U., Yerlikaya, C., Turkan, I., Bor, M., Ozdemir, F.: Response of the cherry rootstock to water stress induced in vitro. - Biol. Plant. 52: 573-576, 2008.
Go to original source... - Slama, I., Abdelly, C., Bouchereau, A., Flowers, T., Savoure, A.: Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. - Ann. Bot. 115: 433-447, 2015.
Go to original source... - Stitt, M., Hurry, V.: A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. - Curr. Opin. Plant Biol. 5: 199-206, 2002.
Go to original source... - Sykes, M., Wilson, J.: The effect of salinity on the growth of some New Zealand sand dune species. - Acta Bot. Neerlandica 38: 173-182, 1989.
Go to original source... - Valluru, R., Van den Ende, W.: Myo-inositol and beyond-emerging networks under stress. - Plant Sci. 181: 387-400, 2011.
Go to original source... - Wang, G., Chen, L., Hao, Z., Li, X., Liu, Y.: Effects of salinity stress on the photosynthesis of Wolffia arrhiza as probed by the OJIP test. - Fresenius environ. Bull. 20: 432-438, 2011.
- Wang, Y., Zeng, X., Xu, Q., Mei, X., Yuan, H., Jiabu, D., Sang, Z., Nyima, T.: Metabolite profiling in two contrasting Tibetan hulless barley cultivars revealed the core salt-responsive metabolome and key salt-tolerance biomarkers. - AoB Plants 11: plz021, 2019.
Go to original source... - Xia, J., Psychogios, N., Young, N., Wishart, D.S.: MetaboAnalyst: a web server for metabolomic data analysis and interpretation. - Nucl. Acids Res. 37: 652-660, 2009.
Go to original source... - Xie, Y., Hu, L., Du, Z., Sun, X., Amombo, E., Fan, J., Fu, J.: Effects of cadmium exposure on growth and metabolic profile of bermudagrass [Cynodon dactylon (L.) Pers.]. - PLoS ONE 9: e115279, 2014.
Go to original source... - Zhang, H., Li, X., Zhang, S., Yin, Z., Zhu, W., Li, J., Meng, L., Zhong, H., Xu, N., Wu, Y.: Rootstock alleviates salt stress in grafted mulberry seedlings: physiological and PS II function responses. - Front. Plant Sci. 9: 1806, 2018.
Go to original source... - Zhang, Y., Li, D., Zhou, R., Wang, X., Dossa, K., Wang, L., Zhang, Y., Yu, J., Gong, H., Zhang, X.: Transcriptome and metabolome analyses of two contrasting sesame genotypes reveal the crucial biological pathways involved in rapid adaptive response to salt stress. - BMC Plant Biol. 19: 66-66, 2019.
Go to original source... - Zheng, C., Jiang, D., Liu, F., Dai, T., Jing, Q., Cao, W.: Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. - Plant Sci. 176: 575-582, 2009.
Go to original source... - Zhu, D., Hou, L., Xiao, P., Guo, Y., Deyholos, M.K., Liu, X.: VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. - Plant Sci. 280: 132-142, 2019.
Go to original source...



