The effects of methanesulfonic acid on seed germination and morphophysiological changes in the seedlings of two Colobanthus species

Justyna Koc, Janusz Wasilewski, Piotr Androsiuk, Wioleta Kellmann-Sopyła, Katarzyna Joanna Chwedorzewska, Irena Giełwanowska


The effect of methanesulfonic acid (MSA) on the morphophysiology and biochemistry of the subantarctic species Colobanthus apetalus and the Antarctic species Colobanthus quitensis was examined. We evaluated the effects of various concentrations of MSA on the germination capacity and germination rate of seeds, seedling growth, chlorophyll fluorescence in cotyledons, and the proline content of seedlings under laboratory conditions at temperatures of 20°C (day) and 10°C (night) with a 12/12 h photoperiod. The examined C. apetalus seeds were grown in a greenhouse, and C. quitensis seeds were harvested in Antarctica and grown in a greenhouse (Olsztyn, Poland). The seeds of C. apetalus were characterized by the highest germination capacity and the highest germination rate, whereas C. quitensis seedlings were characterized by the most favorable growth and development. Only the highest concentrations of MSA decreased the intensity of chlorophyll fluorescence in the cotyledons of both Colobanthus species. The proline content of C. apetalus and C. quitensis seedlings increased significantly after MSA treatments. The results of this study clearly indicated that Colobanthus quitensis is more resistant to chemical stress induced by MSA. This is a first study to investigate the influence of MSA on the morphophysiology and biochemistry of higher plants.


Colobanthus apetalus; Colobanthus quitensis; sub-Antarctic; Antarctica; methanesulfonic acid; environmental stress

Full Text:



Chwedorzewska KJ. Terrestrial Antarctic ecosystems at the changing world – an overview. Pol Polar Res. 2009;30(3):263–276.

Alberdi M, Bravo LA, Gutiérrez A, Gidekel M, Corcuera LJ. Ecophysiology of Antarctic vascular plants. Physiol Plant. 2002;115(4):479–486.

Znój A, Chwedorzewska KJ, Androsiuk P, Cuba-Diaz M, Giełwanowska I, Koc J, et al. Rapid environmental changes in the Western Antarctic peninsula region due to climate change and human activity. Appl Ecol Environ Res. 2018;15(4):525–539.

Bravo LA, Griffith M. Characterization of antifreeze activity in Antarctic plants. J Exp Bot. 2005;56(414):1189–1196.

Wódkiewicz M, Chwedorzewska KJ, Bednarek PT, Znój A, Galera H. How much of the invader’s genetic variability can slip between our fingers? A case study of secondary dispersal of Poa annua on King George Island (Antarctica). Ecol Evol. 2018;8(1):592–600.

Chwedorzewska KJ, Giełwanowska I, Olech M, Molina-Montenegro MA, Wódkiewicz M, Galera H. Poa annua L. in the maritime-Antarctic – an overview. Polar Rec. 2015;51:637–643.

Androsiuk P, Jastrzębski PJ, Paukszto Ł, Okorski A, Pszczółkowska A, Chwedorzewska KJ, et al. Characterization of the complete chloroplast genome of Colobanthus apetalus (Labill.) Druce and comparisons with related species. PeerJ. 2018; 6:e4723.

West JG, Cowley KJ. Colobanthus. In: Wals NG, Entwisle TJ, editors. Flora of Victoria. Dicotyledons Winteraceae to Myrtaceae. Melbourne: Inkata Press; 1996.

Lichtenthaler HK. Vegetation stress: an introduction to the stress concept in plants. J Plant Physiol. 1996;148(1–2):4–14.

Kellmann-Sopyła W, Lahuta LB, Giełwanowska I, Górecki RJ. Soluble carbohydrates in developing and mature diaspores of polar Caryophyllaceae and Poaceae. Acta Physiol Plant. 2015;37(6):118.

Tapia-Valdebenito D, Ramirez LAB, Arce-Johnson P, Gutiérrez-Moraga A. Salt tolerance traits in Deschampsia antarctica Desv. Antarct Sci. 2016;28(6):462–472.

Xiong FS, Ruhland CT, Day TA. Photosynthetic temperature response of the Antarctic vascular plants Colobanthus quitensis and Deschampsia antarctica. Physiol Plant. 1999;106(3):276–286.

Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AG, et al. Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot. 2007;58(13):3581–3590.

Bascuñán-Godoy L, García-Plazaola JI, Bravo LA, Corcuera LJ. Leaf functional and micro-morphological photoprotective attributes in two ecotypes of Colobanthus quitensis from the Andes and maritime Antarctic. Polar Biol. 2010;33(7):885–896.

Pastorczyk M, Giełwanowska I, Lahuta LB. Changes in soluble carbohydrates in polar Caryophyllaceae and Poaceae plants in response to chilling. Acta Physiol Plant. 2014;36(7):1771–1780.

Fuentes-Lillo E, Cuba-Díaz M, Rifo S. Morpho-physiological response of Colobanthus quitensis and Juncus bufonius under different simulations of climate change. Polar Sci. 2017;11:11–18.

Cuba-Díaz M, Marín C, Castel K, Machuca Á, Rifo S. Effect of copper (II) ions on morpho-physiological and biochemical variables in Colobanthus quitensis. Journal of Soil Science and Plant Nutrition. 2017;17(2):429–440.

Androsiuk P, Chwedorzewska K, Szandar K, Giełwanowska I. Genetic variability of Colobanthus quitensis from King George Island (Antarctica). Pol Polar Res. 2015;36:281–295.

Kellmann-Sopyła W, Koc J, Górecki RJ, Domaciuk M, Giełwanowska I. Development of generative structures of polar Caryophyllaceae plants: the Arctic Cerastium alpinum and Silene involucrata, and the Antarctic Colobanthus quitensis. Pol Polar Res. 2017;3(1):83–104.

Rankin AM, Wolff EW. A year long record of size segregated aerosol composition at Halley, Antarctica. J Geophys Res Atmos. 2003;108(D24):4775.

Clegg SL, Brimblecombe P. The solubility of methanesulphonic acid and its implications for atmospheric chemistry. Environ Technol. 1985;6(1–11):269–278.

Brimblecombe P. The Global sulfur cycle. In: Schlesinger WH, editor. Biogeochemistry. Amsterdam: Elsevier; 2005. p. 645–682.

Murrell JC, Higgins T, Kelly DP. Bacterial metabolism of methanesulfonic acid. In: Murrell JC, Kelly DP, editors. Microbiology of atmospheric trace gases. Berlin: Springer; 1996. p. 243–253. (NATO ASI Series; vol 39).

Patai S. The chemistry of sulphonic acids. New York, NY: Wiley; 1991.

Dawson ML, Varner ME, Perraud V, Ezell MJ, Gerber RB, Finlayson-Pitts BJ. Simplified mechanism for new particle formation from methanesulfonic acid, amines, and water via experiments and ab initio calculations. Proc Natl Acad Sci USA. 2012;109(46):18719–18724.

Bork N, Elm J, Olenius T, Vehkamäki H. Methane sulfonic acid-enhanced formation of molecular clusters of sulfuric acid and dimethyl amine. Atmos Chem Phys. 2014;14(22):12023–12030.

Becagli S, Castellano E, Cerri O, Curran M, Frezzotti M, Marino F, et al. Methanesulphonic acid (MSA) stratigraphy from a Talos Dome ice core as a tool in depicting sea ice changes and southern atmospheric circulation over the previous 140 years. Atmos Environ. 2009;43(5):1051–1058.

Cook AM, Laue H, Junker F. Microbial desulfonation. FEMS Microbiol Rev. 1998;22(5):399–419.

Moosvi SA, McDonald IR, Pearce DA, Kelly DP, Wood AP. Molecular detection and isolation from Antarctica of methylotrophic bacteria able to grow with methylated sulfur compounds. Syst Appl Microbiol. 2005;28(6):541–554.

Baxter NJ, Scanlan J, de Marco P, Wood AP, Murrell JC. Duplicate copies of genes encoding methanesulfonate monooxygenase in Marinosulfonomonas methylotropha strain TR3 and detection of methanesulfonate utilizers in the environment. Appl Environ Microbiol. 2002;68(1):289–296.

de Marco P, Murrell JC, Bordalo AA, Moradas-Ferreira P. Isolation and characterization of two new methanesulfonic acid-degrading bacterial isolates from a Portuguese soil sample. Arch Microbiol. 2000;173(2):146–153.

Reichenbecher W, de Marco P, Scanlan J, Baxter N, Murrell JC. MSA monooxygenase. In: Fass R, Flashner Y, Reuveny S, editors. Novel approaches for bioremediation of organic pollution. Boston, MA: Springer; 1999. p. 29–37.

Biedlingmaier S, Schmidt A. Alkylsulfonic acids and some S-containing detergents as sulfur sources for growth of Chlorella fusca. Arch Microbiol. 1983;136(2):124–130.

Logan Miller A, AOSA, SCST. Tetrazolium testing handbook. Ithaca, NY: Association of Official Seed Analysts, Tetrazolium Subcommittee and Society of Commercial Seed Technologists; 2010.

Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39(1):205–207.

Nazarenko M, Lykholat Y, Grigoryuk I, Khromykh N. Consequences of mutagen depression caused by dimethilsulfate. Poljoprivreda i Sumarstvo. 2017;63(3):63–73.

Pipinis E, Milios E, Aslanidou M, Mavrokordopoulou O, Efthymiou E, Smiris P. Effects of sulphuric acid scarification, cold stratification and plant growth regulators on the germination of Rhus coriaria L. seeds. Journal of Environmental Protection and Ecology. 2017;18(2):544–552

Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA. Changes in ethylene evolution and polyamine profiles of seedlings of nine cultivars of Lactuca sativa L. in response to salt stress during germination. Plant Sci. 2003;164(4):557–563.

Almansouri M, Kinet JM, Lutts S. Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant Soil. 2001;231(2):243–254.

Constantinidou H, Kozlowski TT, Jensen K. Effects of sulfur dioxide on Pinus resinosa seedlings in the cotyledon stage 1. J Environ Qual. 1976;5(2):141–144.

Suwannapinunt W, Kozlowski TT. Effect of SO2 on transpiration, chlorophyll content, growth, and injury in young seedlings of woody angiosperms. Can J For Res. 1980;10(1):78–81.

Yi H, Liu J, Zheng K. Effect of sulfur dioxide hydrates on cell cycle, sister chromatid exchange, and micronuclei in barley. Ecotoxicol Environ Saf. 2005;62(3):421–426.

Ghosh A, Dey K, Bauri FK, Dey AN. Effects of different pre-germination treatment methods on the germination and seedling growth of yellow passion fruit (Passiflora edulis var. flavicarpa). Int J Curr Microbiol Appl Sci. 2017;6(4):630–636.

López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol. 2003;6(3):280–287.

Lichtenthaler HK, Miehé JA. Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci. 1997;2(8):316–320.

Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 2004;55(403):1607–1621.

Jiang Y, Ding X, Zhang D, Deng Q, Yu CL, Zhou S, et al. Soil salinity increases the tolerance of excessive sulfur fumigation stress in tomato plants. Environ Exp Bot. 2017;133:70–77.

Liu Y, Li Y, Li L, Zhu Y, Liu J, Li G, et al. Attenuation of sulfur dioxide damage to wheat seedlings by co-exposure to nitric oxide. Bull Environ Contam Toxicol. 2017;99(1):146–151.

Khan MIR, Nazir F, Asgher M, Per TS, Khan NA. Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol. 2015;173:9–18.

Karolewski P. The role of free proline in the sensitivity of poplar (Populus ‘Robusta’) plants to the action of SO1. For Pathol. 1985;15(4):199–206.

Anbazhagan M, Krishnamurthy R, Bhagwat KA. Proline: an enigmatic indicator of air pollution tolerance in rice cultivars. J Plant Physiol. 1988;133(1):122–123.

Tanveer A, Javaid MM, Abbas RN, Ali HH, Nazir MQ, Balal RM, et al. Germination ecology of catchfly (Silene conoidea) seeds of different colors. Planta Daninha. 2017;35:e017152429.

Baskin JM, Baskin CC. Germination dimorphism in Heterotheca subaxillaris var. subaxillaris. Bulletin of the Torrey Botanical Club. 1976;103(5):201–206.

Silvertown JW. Phenotypic variety in seed germination behavior: the ontogeny and evolution of somatic polymorphism in seeds. Am Nat. 1984;124(1):1–16.

de Figueiredo PS, Silva NML. Somatic polymorphism variation in Crotalaria retusa L. Seeds. Am J Plant Sci. 2018;9(01):46–59. 10.4236/ajps.2018.91005

Sorensen AE. Somatic polymorphism and seed dispersal. Nature. 1978;276(5684):174–176.

Sharma NK, Sharma MM, Sen DN. Seed perpetuation in Rhynchosia capitata DC. Biol Plant. 1978;20(3):225–228.

Harper JL, Obeid M. Influence of seed size and depth of sowing on the establishment and growth of varieties of fiber and oil seed flax. Crop Sci. 1967;7(5):527–532.

Harper JL. Establishment, aggression and cohabitation in weedy species. In: Baker IM, Stebbins GL, editors. The genetics of colonization species. New York, NY: Academic Press; 1965. p. 243–268.