Abstract
A simulation experiment was conducted to explore the influence of enhanced ultraviolet-B (UV-B) radiation, water deficit, and their combination on UV-absorbing compounds and osmotic adjustment substances of mosses Bryum argenteum and Didymodon vinealis isolated from biological soil crusts (BSCs) growing in a revegetated area of the Tengger Desert, China. Four levels of UV-B radiation and two gradients of water regime were employed. Compared with their controls, amounts of total flavonoids, chlorophyll, carotenoids, soluble sugars, and soluble proteins significantly decreased (p < 0.05), but proline content significantly increased (p < 0.05), when exposed to either enhanced UV-B or water deficit. The negative effects of enhanced UV-B were alleviated when water deficit was applied. There were increases in UV-absorbing compounds and osmotic adjustment substances when exposed to a combination of enhanced UV-B and water deficit compared with single stresses, except for the proline content in D. vinealis. In addition, our results also indicated interspecific differences in response to enhanced UV-B, water deficit, and their combination. Compared with B. argenteum, D. vinealis was more resistant to enhanced UV-B and water deficit singly and in combination. These results suggest that the damage of enhanced UV-B on both species might be alleviated by water deficit. This alleviation is important for understanding the response of BSCs to UV-B radiation in future global climate change. This also provides novel insights into assessment damages of UV-B to BSC stability in arid and semiarid regions.
Similar content being viewed by others
Abbreviations
- BSCs:
-
Biological soil crusts
- N:
-
Nitrogen
- UV-B:
-
Ultraviolet-B
- Car:
-
Carotenoid
- Chl:
-
Chlorophyll
- ANOVA:
-
Analysis of variance
References
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344
Alexieva V, Ivanov S, Sergiev I, Karanov E (2003) Interaction between stresses. Bulg J Plant Physiol 29(3-4):1–17
Atanassova M, Georgieva S, Ivancheva K (2011) Total phenolic and total flavonoid contents, antioxidant capacity and biological contaminants in medicinal herbs. J Univ Chem Technol Metall 46:81–88
Bais AF, McKenzie RL, Bernhard G, Aucamp PJ, Ilyas M, Madronich S, Tourpali K (2015) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 14:19–52
Balouchi HR, Sanavy SAMM, Emam Y, Dolatabadian A (2009) UV radiation, elevated CO2 and water stress effect on growth and photosynthetic characteristics in durum wheat. Plant Soil Environ 55:443–453
Bandurska H, Pietrowska–Borek M, Cieślak M (2012) Response of barley seedlings to water deficit and enhanced UV–B irradiation acting along and in combination. Acta Physiol Plant 34:161–171
Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV–B radiation. Plant Sci 213:98–105
Bates LS, Waldren RP, Teare LD (1973) Rapid determination of the free proline for water stress studies. Plant Soil 39:205–207
Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer–Verlag, Berlin
Bornman JF, Barnes PW, Robinson SA, Ballare CL, Flint SD, Caldwell MM (2015) Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems. Photochem Photobiol Sci 14:88–107
Bowker MA, Reed SC, Belnap J, Phillips SL (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microb Ecol 43:13–25
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Chen LZ, Deng SQ, De Philippis R, Tian WQ, Wu H, Wang J (2013) UV–B resistance as a criterion for the selection of desert microalgae to be ultilized for inoculating desert soils. J Appl Phycol 25:1009–1015
Couee I, Sulmon C, Gouesbet G, EI Amrani A (2006) Involvement of soluble sugar in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
Dubois M, Gilles KA, Hamilton JK, Hofman G, Smith F (1956) Colorimetric method for the determination of sugars. Anal Chem 28:350–355
Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212
Feng HY, Li SW, Xue LG, An LZ, Wang XF (2007) The interactive effects of enhanced UV–B radiation and soil drought on spring wheat. S Afr J Bot 73:429–434
Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257
Guidi L, DeglInnocenti E, Remorini D, Biricolti S, Fini A, Ferrini F, Nicese FP, Tattini M (2011) The impact of UV-radiation on the physiology and biochemistry of Ligustrum vulgare exposed to different visible-light irradiance. Environ Exp Bot 70:88–95
Hassan IA, Basahi JM, Halba NS, Kadi MW (2013) Investigation of climate changes on metabolic response of plants; interactive effects of drought stress and excess UV–B. J Earth Sci Clim Chang 4:129
He LH, Jia XY, Gao ZQ, Li RZ (2011) Genotype–dependent responses of wheat (Triticum aestivum L.) seedlings to drought, UV–B radiation and their combined stresses. Afri. J Biotechnol 10:4046–4056
Hofmann RW, Campbell BD, Bloor SJ, Swinny EE, Markham KR, Ryan KG, Fountain DW (2003) Responses to UV–B radiation in Trifolium repens L.—physiological links to plant productivity and water availability. Plant Cell Environ 26:603–612
Hui R, Li XR, Chen CY, Zhao X, Jia RL, Liu LC, Wei YP (2013) Responses of photosynthetic properties and chloroplast ultrastructure of Bryum argenteum from a desert biological soil crust to elevated ultraviolet–B radiation. Physiol Plant 147:489–501
Hui R, Li XR, Jia RL, Liu LC, Zhao RM, Zhao X, Wei YP (2014) Photosynthesis of two moss crusts from the Tengger Desert with contrasting sensitivity to supplementary UV-B radiation. Photosynthetica 52:36–49
Hui R, Zhao RM, Liu LC, Li G, Yang HT, Gao YH, Wang XQ (2016) Modelling the influence of snowfall on cyanobacterial crusts in the Gurbantunggut Desert, northern China. Aust J Bot 64:476–483
Javadmanesh S, Rahmani F, Pourakbar L (2012) UV–B radiation, soil salinity, drought stress and their concurrent effects on some physiological parameters in maize plant. Am Eurasian J Toxicol Sci 4:154–164
Jia RL, Li XR, Liu LC, Gao YH, Li XJ (2008) Responses of biological soil crusts to sand burial in a revegetated area of the Tengger Desert, Northern China. Soil Biol Biochem 40:2827–2834
Jia RL, Li XR, Liu LC, Gao YH, Zhang XT (2012) Differential wind tolerance of soil crust mosses explains their micro–distribution in nature. Soil Biol Biochem 45:31–39
Jiang H, Qiu B (2005) Photosynthetic adaptation of a bloomforming cyanobacterium Microcystis aeruginosa to prolonged UV–B exposure. J Phycol 41:983–992
Kalu BA, Fick GW (1981) Quantifying morphological development of alfalfa for studies of herbage quality. Crop Sci 21:267–271
Karioti A, Kitsaki CK, Zygouraki S, Ziobora M, Djeddi S, Skaltsa H, Liakopoulos G (2008) Occurrence of flavonoids in Ophrys (Orchidaceae) flower parts. Flora 203:602–609
Kurkdjian A, Guern J (1989) Intracellular pH: measurement and importance in cell activity. Annu Rev Plant Physiol Plant Mol Biol 40:271–303
Lan SB, Wu L, Zhang DL, Hu CX, Liu YD (2011) Ethanol outperforms multiple solvents in the extraction of chlorophyll–a from biological soil crusts. Soil Biol Biochem 43:857–861
Li XR (2012) Study on eco–hydrology of desert biological soil crusts. High education press, Beijing
Li XR, Tian F, Jia RL, Zhang ZS, Liu LC (2010) Do biological soil crusts determine vegetation changes in sandy deserts? Implications for managing artificial vegetation. Hydrol Process 24:3621–3630
Li XR, Zhang P, Su YG, Jia RL (2012) Carbon fixation by biological soil crusts following stabilization of sand dune in arid desert regions of China: a four–year field study. Catena 97:119–126
Li JH, Li XR, Zhang P (2014) Micro–morphology, ultrastructure and chemical composition changes of Bryum argenteum from a desert biological soil crust following one–year desiccation. Bryologist 117:232–240
Liu LX, Xu SM, Woo KC (2005) Solar UV–B radiation on growth, photosynthesis and the xanthophyll cycle in tropical acacias and eucalyptus. Environ Exp Bot 54:121–130
Liu YM, Li XR, Xing ZS, Zhao X, Pan YX (2013) Responses of soil microbial biomass and community composition to biological soil crusts in revegetated areas of the Tengger Desert. Appl Soil Ecol 65:52–59
Ma CH, Chu JZ, Shi XF, Liu CQ, Yao XQ (2016) Effects of enhanced UV–B radiation on the nutritional and active ingredient contents during the floral development of medicinal chrysanthemum. J Photochem Photobiol B 158:228–234
Martínez–Lüscher J, Morales F, Delrot S, Sánchez–Díaz M, Gomès E, Aguirreolea J, Pascual I (2015) Characterization of the adaptive response of grapevine (cv. Tempranillo) to UV–B radiation under water deficit conditions. Plant Sci 232:13–22
McKenzie RL, Björn LO, Bais A, Ilyasd M (2003) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem Photobiol Sci 2:5–15
Mishler BD, Oliver MJ (2009) Putting Physcomitrella patens on the tree of life: the evolution and ecology of mosses. Annu Plant Rev 36:1–15
Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Le Thiec D, Bréchet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoids × Populus nigra. New Phytol 169:765–777
Niemi R, Martikainen PJ, Silvola J, Sonninen E, Wulff A, Holopainen T (2002) Responses of two Sphagnum moss species and Eriophorum vaginatum to enhanced UV-B in a summer of low UV intensity. New Phytol 156:509–515
Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260:1623–1639
Nikolopoulos D, Petropoulou Y, Kyparissis A, Manetas Y (1995) Effects of enhanced UV–B radiation on the drought semideciduous Mediterranean shrub Phlomis fruticose under field conditions are season–specific. Aust J Plant Physiol 22:737–745
Ochoa–Hueso R, Manrique E (2011) Effects of nitrogen deposition and soil fertility on cover and physiology of Cladonia foliacea (Huds.) Willd., a lichen of biological soil crusts from Mediterranean Spain. Environ Pollut 159:449–457
Randriamanana TR, Nissinen K, Moilanen J, Nybakken L, Julkunen-Tiitto R (2015) Long-term UV-B and temperature enhancements suggest that females of Salix myrsinifolia plants are more tolerant to UV-B than males. Environ Exp Bot 109:296–305
Ranjbarfordoei A, Samson R, Van Damme P (2011) Photosynthesis performance in sweet almond [Prunus dulcis (Mill) D. Webb] exposed to supplemental UV–B radiation. Photosynthetica 49:107–111
Robinson SA, Wasley J, Tobin AK (2003) Living on the edge–plants and global change in continental and maritime Antarctica. Glob Chang Biol 9:1681–1717
Rossi F, Potrafka RM, Garcia–Pichel F, De Philippis R (2012) The role of the exopolysaccarides in enhancing hydraulic conductivity of biological soil crusts. Soil Biol Biochem 46:33–40
Ryan KG, Hunt JE (2005) The effects of UV–B radiation on temperate southern hemisphere forests. Environ Pollut 137:415–427
Samanta A, Das G, Das SK (2011) Roles of flavonoids in plants. Carbon 100:6
Sangtarash MH, Qaderi MM, Chinnappa CC, Reid DM (2009a) Differential responses of two Stellaria longipes ecotypes to ultraviolet–B radiation and drought stress. Flora Morphol Distrib Funct Ecol Plants 204:593–603
Sangtarash MH, Qaderi MM, Chinnappa CC, Reid DM (2009b) Differential sensitivity of canola (Brassica napus) seedlings to ultraviolet–B radiation, water stress and abscisic acid. Environ Exp Bot 66:212–219
Sharmila P, Pardha Saradhi P (2002) Proline accumulation in heavy metal stressed plants: an adaptive strategy. In: Prasad MNV, Strazlka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, Dordrecht, pp 179–199
Singh R, Singh S, Tripathi R, Agrawal SB (2011) Supplemental UV–B radiation induced changes in growth, pigments and antioxidant pool of bean (Dolichos lablab) under field conditions. J Environ Biol 32:139–145
Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118
Turnbull JD, Leslie SJ, Robinson SA (2009) Desiccation protects Antarctic mosses from ultraviolet–B induced DNA damage. Funct Plant Biol 36:214–221
Wahid A (2007) Physiological implication of metabolite biosynthesis for net assimilation and heat–stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 120:219–228
Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plant 51:104–109
Xie ZM, Wang YX, Liu YD, Liu YM (2009) Ultraviolet–B exposure induces photo–oxidative damage and subsequent repair strategies in a desert cyanobacterium Microcoleus vaginatus Gom. Eur J Soil Biol 45:377–382
Yao X, Chu J, He X, Ba C (2011) Protective role of selenium in wheat seedlings subjected to enhanced UV–B radiation. Russ J Plant Physiol 58:283–289
Yu H, Liu R (2013) Effect of UV-B radiation on the synthesis of UV–absorbing compounds in a terrestrial cyanobacterium, Nostoc flagelliforme. J Appl Phycol 25:1441–1446
Yu J, Tang XX, Zhang PX, Tian JY, Cai HJ (2004) Effects of CO2 enrichment on photosynthesis, lipid peroxidation and activities of antioxidative enzymes of Platymonas subcordiformis subjected to UV–B radiation stress. Acta Bot Sin 46:682–690
Zancan S, Suglia I, La Rocca N, Ghisi R (2008) Effects of UV–B radiation on antioxidant parameters of iron–deficient barley plants. Environ Exp Bot 63:71–79
Zelikova TJ, Housman DC, Grote EE, Neher DA, Belnap J (2012) Warming and increased precipitation frequency on the Colorado Plateau: implications for biological soil crusts and soil processes. Plant Soil 355:265–282
Zhang X, Tang X, Wang M, Zhang W, Zhou B, Wang Y (2017a) ROS and calcium signaling mediated pathways involved in stress responses of the marine microalgae Dunaliella salina to enhanced UV–B radiation. J Photochem Photobiol B 173:360–367
Zhang JW, Chen GX, Zhao PS, Zhou Q, Zhao X (2017b) The abundance of certain metabolites responds to drought stress in the highly drought tolerant plant Caragana korshinskii. Acta Physiol Plant 39:116
Zheng XQ, Jin J, Chen H, Du YY, Ye JH, Lu JL, Lin C, Dong JJ, Sun QL, Wu LY, Liang YR (2008) Effect of ultraviolet B irradiation on accumulation of catechins in tea (Camellia sinensis (L.) O. Kuntze). Afr J Biotechnol 7:3283–3287
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Funding
This study was supported by the National Natural Science Foundation of China (Nos. 41621001, 41530746, and 41701104) and by the West Light Program for Talent Cultivation of the Chinese Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Hui, R., Zhao, R., Song, G. et al. Effects of enhanced ultraviolet-B radiation, water deficit, and their combination on UV-absorbing compounds and osmotic adjustment substances in two different moss species. Environ Sci Pollut Res 25, 14953–14963 (2018). https://doi.org/10.1007/s11356-018-1689-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1689-8