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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Comparative study on the effects of NaCl on selected moss and fern representatives

Milica Bogdanović A D , Milena Ilić A , Suzana Živković A , Aneta Sabovljević B , Dragoljub Grubišić A B C and Marko Sabovljević B
+ Author Affiliations
- Author Affiliations

A Institute for Biological Research Siniša Stanković, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia.

B Institute of Botany and Botanical Garden, Faculty of Biology, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia.

C Deceased.

D Corresponding author. Email: milica84bog@gmail.com

Australian Journal of Botany 59(8) 734-740 https://doi.org/10.1071/BT11059
Submitted: 18 February 2011  Accepted: 8 November 2011   Published: 23 January 2012

Abstract

Salt demonstrates various osmotic and ionic effects on vascular plant growth, development and function, but very few data can be found on how salt affects non-tracheophytes. To explore this, gametophytes of two moss – Bryum argenteum Hedw. and Atrichum undulatum (Hedw.) P. Beauv., and three fern species – Asplenium viride Britton, Ceterach officinarum DC, and Phyllitis scolopendrium (L.) Newman, were treated for 3 days with different NaCl concentrations in growth medium under in vitro controlled conditions. Subsequently, these plants recovered for 18 days on NaCl-free medium, after which the following parameters were measured for mosses: presence of secondary protonema and shoots, protonemal radius and index of multiplication. Survival, chlorophyll a, b, total and a/b ratio were determined as well as total phenolic content, both for ferns and mosses. All species tolerated 50 and 100 mM of NaCl-enriched media, quite well. On higher salt concentrations in the substrata, measured morphological parameters and chlorophyll content were reduced. In general, mosses exhibited higher NaCl tolerance than ferns. Change of phenolic content in ferns suggests these plants use antioxidative properties of phenolics as a mechanism of salt tolerance, in contrast with mosses whose phenolic content was stable.


References

Adam KP (1999) Phenolic constituents of the fern Phegopteris connectilis. Phytochemistry 52, 929–934.
Phenolic constituents of the fern Phegopteris connectilis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFCisQ%3D%3D&md5=00b37a657252b4fa9e441bfee8f45098CAS |

Asakawa Y (2008) Liverworts – potential source of medicinal compounds. Current Pharmaceutical Design 14, 3067–3088.
Liverworts – potential source of medicinal compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSjsw%3D%3D&md5=b139962fefdd040453a48e92d57985f1CAS |

Asakawa Y, Ludwiczuk A, Nagashima F, Toyota M, Hashimoto T, Tori M, Fukuyama Y, Harinantenaina L (2009) Bryophytes: biol.- and chemical diversity, bioactivity and chemosystematics. Heterocycles 77, 99–150.
Bryophytes: biol.- and chemical diversity, bioactivity and chemosystematics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVShtr8%3D&md5=187199dc6389d4e3335b55cc3e99a963CAS |

Benito B, Rodríguez-Navarro A (2003) Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. The Plant Journal 36, 382–389.
Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVyku74%3D&md5=d110163c3747825d9793eff494641168CAS |

Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7s%3D&md5=c54606252dc091273f23a1da3e7a48fbCAS |

Chobot V, Kubicová L, Nabbout S, Jahodář L, Vytlačilová J (2006) Antioxidant and free radical scavenging activities of five moss species. Fitoterapia 77, 598–600.
Antioxidant and free radical scavenging activities of five moss species.Crossref | GoogleScholarGoogle Scholar |

Choudhary MI, Naheed N, Abbaskhan A, Musharraf SG, Siddiqui H, Atta ur R (2008) Phenolic and other constituents of fresh water fern Salvinia molesta. Phytochemistry 69, 1018–1023.
Phenolic and other constituents of fresh water fern Salvinia molesta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhslGrsr4%3D&md5=d68bdd81bbacc4829f6062309e7eeaabCAS |

Delfine S, Alvino A, Villani MC, Loreto F (1999) Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiology 119, 1101–1106.
Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFymu7w%3D&md5=330898bbf895ccedca1e1be8b5a1a798CAS |

Ding ZT, Fang YS, Tai ZG, Yang MH, Xu YQ, Li F, Cao QE (2008) Phenolic content and radical scavenging capacity of 31 species of ferns. Fitoterapia 79, 581–583.
Phenolic content and radical scavenging capacity of 31 species of ferns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGgsr%2FL&md5=1042bc98a38fb99ef0c4fa85d3c08b65CAS |

Frank W, Ratnadewi D, Reski R (2005) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220, 384–394.
Physcomitrella patens is highly tolerant against drought, salt and osmotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1WksrY%3D&md5=410c3b475edb107cfe0d46bdaa53b7a9CAS |

Glime JM (2006) Water relations: rehydration and repair. In ‘Bryophyte ecology. Vol. 1. Physiological ecology’. Ebook sponsored by Michigan Technological University and the International Association of Bryologists, Michigan, United States of America. Accessed on November 20. 2011. Available at http://www.bryoecol.mtu.edu/

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Biology 51, 463–499.
Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=f9742c0d10ab5d277adfbdb4cf3b4ec9CAS |

Jampeetong A, Brix H (2009) Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. Aquatic Botany 91, 181–186.
Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKntbfN&md5=4dee1bdbdfaa1177c87cdf6abfb01064CAS |

Jungklang J, Usui K, Matsumoto H (2003) Differences in physiological responses to NaCl between salt-tolerant Sesbania rostrata Brem. & Oberm. and non-tolerant Phaseolus vulgaris L. Weed Biology and Management 3, 21–27.
Differences in physiological responses to NaCl between salt-tolerant Sesbania rostrata Brem. & Oberm. and non-tolerant Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCrtbs%3D&md5=ff14fad6880a8af7c7c456bb53964905CAS |

Kenrick P (2000) The relationships of vascular plants. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 847–855.
The relationships of vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FjtFymtg%3D%3D&md5=0ac84c5df27e2dcdf542e7c06c46e4c7CAS |

Kim H-J, Fonseca JM, Choi J-H, Kubota C, Kwon DY (2008) Salt in irrigation water affects the nutritional and visual properties of Romaine lettuce (Lactuca sativa L.). Journal of Agricultural and Food Chemistry 56, 3772–3776.
Salt in irrigation water affects the nutritional and visual properties of Romaine lettuce (Lactuca sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFCgu7c%3D&md5=807ac2e9ba7fd5d5569cee5cbb19a987CAS |

Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007) Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiology and Biochemistry 45, 244–249.
Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslCiu70%3D&md5=419dc707ac3b5cd3aa1f15d94b000444CAS |

Lu C, Vonshak A (1999) Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytologist 141, 231–239.
Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFeku7Y%3D&md5=c114b9f0a21742dcae97451ec0f0aba6CAS |

Masood A, Abraham G (2006) Physiological response of Azolla pinnata plants to salinity stress. Roumanian Biotechnological Letters 11, 2841–2844.

M’Rah S, Ouerghi Z, Berthomieu C, Havaux M, Jungas C, Hajji M, Grignon C, Lachaâl M (2006) Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila. Journal of Plant Physiology 163, 1022–1031.
Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFajsr7I&md5=6b7ac566465ad88f58e4d3a4a2b9a42cCAS |

Mišić D, Šiler B, Filipović B, Popović Z, Živković S, Cvetić T, Mijović A (2009) Rapid in vitro selection of salt-tolerant genotypes of the potentially medicinal plant Centaurium maritimum (L.) Fritsch. Archives of Biological Sciences 61, 57–69.
Rapid in vitro selection of salt-tolerant genotypes of the potentially medicinal plant Centaurium maritimum (L.) Fritsch.Crossref | GoogleScholarGoogle Scholar |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=c50f8020f0a80c514f64c7765eb44ce9CAS |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bioassays with tobacco tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=3408220b7f2f5619c27497814efac5dbCAS |

Navarro JM, Flores P, Garrido C, Martinez V (2006) Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity. Food Chemistry 96, 66–73.
Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGht7zP&md5=37ad471ce6473d33319a4fcb3869c5e3CAS |

Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integrative and Comparative Biology 45, 788–799.
Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats?Crossref | GoogleScholarGoogle Scholar |

Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60, 324–349.
Salt tolerance and salinity effects on plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKlt7nN&md5=4c0b57aad0d22446af7fc6a1e7f92ca4CAS |

Qiu Y-L, Palmer JD (1999) Phylogeny of early land plants: insights from genes and genomes. Trends in Plant Science 4, 26–30.
Phylogeny of early land plants: insights from genes and genomes.Crossref | GoogleScholarGoogle Scholar |

Rajesh A, Arumugam R, Venkatesalu V (1998) Growth and photosynthetic characteristics of Ceriops roxburghiana under NaCl stress. Photosynthetica 35, 285–287.
Growth and photosynthetic characteristics of Ceriops roxburghiana under NaCl stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkt1Shs7c%3D&md5=9bc8c3cd97bf4f20a4490b44062753ecCAS |

Ranjbarfordoei A, Samson R, Van Damme P (2006) Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl. Photosynthetica 44, 513–522.
Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVKju77I&md5=ad805a3965ddcaf481b25a226dd82821CAS |

Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends in Plant Science 2, 152–159.
Antioxidant properties of phenolic compounds.Crossref | GoogleScholarGoogle Scholar |

Rowan KS (1989) ‘Photosynthetic pigments of algae.’ (Cambridge University Press: Cambridge)

Sabovljevic M, Sabovljevic A (2007) Contribution to the coastal bryophytes of the Northern Mediterranean: are there halophytes among bryophytes? Phytologia balcanica 13, 131–135.

Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164, 151–162.
Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlGjs7o%3D&md5=be7b8999cf35c3530582f43116e11144CAS |

Sgherri C, Cosi E, Navari-Izzo F (2003) Phenols and antioxidative status of Raphanus sativus grown in copper excess. Physiologia Plantarum 118, 21–28.
Phenols and antioxidative status of Raphanus sativus grown in copper excess.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1egsr0%3D&md5=04241ddf8b6244e1a31edd40ba87bdd5CAS |

Sgherri C, Stevanovic B, Navari-Izzo F (2004) Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiologia Plantarum 122, 478–485.
Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeksg%3D%3D&md5=3fa647486622a7714d1d3ec4cd61d641CAS |

Singh AK, Dubey RS (1995) Changes in chlorophyll a and b contents and activities of photosystems 1 and 2 in rice seedlings induced by NaCl. Photosynthetica 31, 489–499.

Singleton V, Rossi J (1965) Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid reagents. American Journal of Enology and Viticulture 16, 144–158.

Sroka Z, Cisowski W (2005) The anti-ROS activity of various plant extracts. Advances in Clinical and Experimental Medicine 14, 423–433.

Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiology 149, 1154–1165.
Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1ajs7c%3D&md5=126bebced7ab4df9a2ab81f36ad907f4CAS |

Tanaka N, Yuhara H, Wada H, Murakami T, Cambie RC, Braggins JE (1993) Phenolic constituents of Pteridium esculentum. Phytochemistry 32, 1037–1039.
Phenolic constituents of Pteridium esculentum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFegsbw%3D&md5=03f559d9bc9fa6f7d095f45376b0c4b5CAS |

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyisbk%3D&md5=a520338f53200edb707cffcc8ec65d1cCAS |

Tuba Z, Proctor MCF, Csintalan Z (1998) Ecophysiological responses of homoichlorophyllous and poikilochlorophyllous dessication tolerant plants: a comparison and a ecological perspective. Plant Growth Regulation 24, 211–217.
Ecophysiological responses of homoichlorophyllous and poikilochlorophyllous dessication tolerant plants: a comparison and a ecological perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOrsLc%3D&md5=c6c699e99d00b57a9d3f88ae82dbb973CAS |

Yuan G, Wang X, Guo R, Wang Q (2010) Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chemistry 121, 1014–1019.
Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsF2gs74%3D&md5=b05cf8f544ed1881446b0055dc6f6225CAS |

Zhu J-K (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiology 124, 941–948.
Genetic analysis of plant salt tolerance using Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlWrurw%3D&md5=4b152483837f004b0b7b5c9e01f64564CAS |