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RESEARCH ARTICLE
Contents Vol 36(12)

Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemaneiformis (Rhodophyta) under phosphorus-limited and replete conditions

Zhiguang Xu A and Kunshan Gao B C
+ Author Affiliations
- Author Affiliations

A Marine Biology Institute, Shantou University, Shantou, Guangdong 515063, China.

B State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian 361005, China.

C Corresponding author. Email: ksgao@xmu.edu.cn

Functional Plant Biology 36(12) 1057-1064 https://doi.org/10.1071/FP09092
Submitted: 27 April 2009  Accepted: 24 July 2009   Published: 3 December 2009

Abstract

Solar ultraviolet radiation (UVR, 280–400 nm) is known to negatively affect macroalgal growth and photosynthesis, while phosphorus availability may affect their sensitivity to UVR. Here, we show that UV-A enhanced the growth rate of the red macroalga, Gracilaria lemaneiformis Bory de Saint-Vincent under inorganic phosphorus (Pi)-replete but reduced it under Pi-limited conditions. Maximal net photosynthetic rates were significantly reduced by both UV-A and UV-B, but the apparent photosynthetic efficiency was enhanced in the presence of UV-A. The UV-induced inhibition was exacerbated under Pi-limited conditions. The activity of total carbonic anhydrase was enhanced and the photosynthetic affinity for exogenous inorganic carbon (Ci) was raised for thalli grown in the presence of UVR under both Pi-replete and Pi-limited conditions. The relative growth rate was closely related to Ci acquisition capability (Vmax/KDIC), which was enhanced by UVR exposure under Pi-replete but not significantly affected under Pi-limited conditions.

Additional keywords: photosynthesis, pigment, the ratio of Vmax to KDIC, UV-absorbing compounds.


Acknowledgements

This research was supported by National Basic Research Program of China (2009CB421207), National Natural Science Foundation of China (90411018, 40876058) and ‘863’ project (2006AA10A413) and Ministry of Education (308015). Professor John Hodgkiss is thanked for his assistance with the English in this paper.


References


Aguilera J, Jiménez C, Figueroa F, Lebert M, Häder D (1999) Effects of ultraviolet radiation on thallus absorption and photosynthetic pigments in the red alga Porphyra umbilicalis. Journal of Photochemistry and Photobiology. B, Biology 48, 75–82.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Atienzar FA, Cordi B, Donkin ME, Evenden AJ, Jha AN, Depledge MH (2000) Comparison of ultraviolet-induced genotoxicity detected by random amplified polymorphic DNA with chlorophyll fluorescence and growth in a marine macroalgae, Palmaria palmata. Aquatic Toxicology (Amsterdam, Netherlands) 50, 1–12.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Functional Plant Biology 29, 335–347.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Beardall J, Heraud P, Roberts S, Shelly K, Stojkovic S (2002) Effects of UV-B radiation on inorganic carbon acquisition by the marine microalga Dunaliella tertiolecta (Chlorophyceae). Phycologia 41, 268–272. open url image1

Beardall J, Roberts R, Raven JA (2005) Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Canadian Journal of Botany 83, 859–864.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Reviews in Environmental Science and Biotechnology 5, 141–166.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Davison JR, Jordan TL, Fegley JC, Grobe CW (2007) Response of Laminaria saccharina (Phaeophyta) growth and photosynthesis to simultaneous ultraviolet radiation and nitrogen limitation. Journal of Phycology 43, 636–646.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dunlap WC, Rae GA, Helbling EW, Villafañe VE, Holm-Hansen O (1995) Ultraviolet-absorbing compounds in natural assemblages of Antarctic phytoplankton. Antarctic Journal of the United States 30, 323–326. open url image1

Fei X (2004) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512, 145–151.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Flores-Moya A, Hanelt D, Lopez-Figueroa F, Altamirano M, Vinegla B, Salles S (1999) Solar UV-B radiation shows beneficial effects on recovery of inhibited photosynthesis in the brown alga Dictyota dichotoma. Journal of Photochemistry and Photobiology. B, Biology 49, 129–135.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gao K, Xu J (2008) Effects of solar UV radiation on diurnal photosynthetic performance and growth of Gracilaria lemaneiformis (Rhodophyta). European Journal of Phycology 43, 297–307.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gao K, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiology 144, 54–59.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

García-Sánchez MJ, Fernández JA, Niell FX (1996) Photosynthetic responses of P-deficient Gracilaria tenuistipitata under two different phosphate treatments. Physiologia Plantarum 96, 601–606.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Häder DP, Lebert M, Marangoni P, Colombetti G (1999) ELDONET-European light dosimeter network hardware and software. Journal of Photochemistry and Photobiology. B, Biology 52, 51–58.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Häder DP, Lebert M, Sinha RP, Barbieri ES, Helbling EW (2002) Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochemical & Photobiological Sciences 1, 809–814.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Häder DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Sciences 6, 267–285.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hanelt D, Roleda MR (2009) UVB radiation may ameliorate photoinhibition in specific shallow-water tropical marine macrophytes. Aquatic Botany 91, 6–12.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Henley WJ (1993) Measurements and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and dial changes. Journal of Phycology 29, 729–739.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Henry BE, Van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. Journal of Phycology 40, 527–533.
|  CAS | Crossref |
open url image1

Heraud P, Roberts S, Shelly K, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. II. Effects on rates of damage and repair. Journal of Phycology 41, 1212–1218.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hernández I, Niell FX, Whitton BA (2002) Phosphatase activity of benthic marine algae. An overview. Journal of Applied Phycology 14, 475–487.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hessen DO, Van Donk E, Andersen T (1995) Growth responses, P-uptake and loss of flagella in Chlamydomonas reinhardtii exposed to UV-B. Journal of Plankton Research 17, 17–27.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Holzinger A, Lütz C (2006) Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron (Oxford, England) 37, 190–207.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493, 187–200.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hwang R, Tsai C, Lee T (2004) Assessment of temperature and nutrient limitation on seasonal dynamics among species of Sargassum from a coral reef in southern Taiwan. Journal of Phycology 40, 463–473.
| Crossref |
open url image1

Irihimovitch V, Yehudai-Resheff S (2008) Phosphate and sulfur limitation responses in the chloroplast of Chlamydomonas reinhardtii. FEMS Microbiology Letters 283, 1–8.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jiang H, Gao K, Helbling EW (2007) Effects of solar UV radiation on germination of conchospores and morphogenesis of sporelings in Porphyra haitanensis (Rhodophyta). Marine Biology 151, 1751–1759.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia 92, 317–326.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Karsten U, Wiencke C (1999) Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). Journal of Plant Physiology 155, 407–415.
|  CAS |
open url image1

Kozlowska-Szerenos B, Zieliński P, Maleszewski S (2000) Involvement of glycolate metabolism in acclimation of Chlorella vulgaris cultures to low phosphate supply. Plant Physiology and Biochemistry 38, 727–734.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kramer GF, Norman HA, Krizek DT, Mirecki RM (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30, 2101–2108.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lapointe BE (1987) Phosphorus- and nitrogen-limited photosynthesis and growth of Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: an experimental field study. Marine Biology 93, 561–568.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Larned ST (1998) Nitrogen- versus phosphorus-limited growth and sources of nutrient for coral reef macroalgae. Marine Biology 132, 409–421.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Makarov M (1999) Influence of ultraviolet radiation on the growth of the dominant macroalgae of the Barents Sea. Chemosphere. Global Change Science 1, 461–467.
| Crossref | GoogleScholarGoogle Scholar | open url image1

McKenzie RL, Aucamp PJ, Bais AF, Björn LO, Ilyas M (2007) Changes in biologically-active ultraviolet radiation reaching the Earth’s surface. Photochemical & Photobiological Sciences 6, 218–231.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem Π under environmental stress. Biochimica et Biophysica Acta 1767, 414–421.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Murphy TM (1983) Membranes as targets of ultraviolet radiation. Physiologia Plantarum 58, 381–388.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Neale PJ (2000) Spectral weighting functions for quantifying the effects of ultraviolet radiation in marine ecosystems. In ‘Effects of UV radiation on the marine environment’. (Eds SJ DeMora, M Vernet) pp. 73–100. (Cambridge University Press: Cambridge)

Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiology Letters 269, 1–10.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pakker H, Beekman CAC, Breeman AM (2000) Efficient photoreactivation of UVBR-induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). European Journal of Phycology 35, 109–114.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Raven JA, Beardall J (1981) Respiration and photorespiration. Canadian Bulletin of Fisheries and Aquatic Sciences 210, 55–82. open url image1

Roleda MY, Wiencke C, Lüder UH (2006) Impact of ultraviolet radiation on cell structure, UV-absorbing compounds, photosynthesis, DNA damage, and germination in zoospores of Arctic Saccorhiza dermatodea. Journal of Experimental Botany 57, 3847–3856.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shelly K, Roberts S, Heraud P, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. I. Effects on growth, phosphate uptake, and chlorophyll fluorescence. Journal of Phycology 41, 1204–1211.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Siegelman HW , Kycia JH (1978) Algal biliproteins. In ‘Handbook of phycological methods: physiological and biochemical methods’. (Eds JA Hellebust, JS Craigie) pp. 71–79. (Cambridge University Press: Cambridge)

Sigee DC (2005) ‘Freshwater microbiology.’ 516 pp. (Wiley: Chichester)

Sobrino C, Montero O, Lubián LM (2004) UV-B radiation increases cell permeability and damages nitrogen incorporation mechanisms in Nannochloropsis gaditana. Aquatic Sciences 66, 421–429.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Song Y, Qiu B (2007) The CO2-concentrating mechanism in the bloom-forming cyanobacterium Microcystis aeruginosa (Cyanophyceae) and effects of UVB radiation on its operation. Journal of Phycology 43, 957–964.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tyrrell T (1999) The relative influence of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Vincent WF , Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In ‘The effects of UV radiation in the marine environment’. (Eds ST de Mora, S Demers, M Vernet) pp. 149–176. (Cambridge University Press: Cambridge)

Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Weatherhead EC, Andersen SB (2006) The search for signs of recovery of the ozone layer. Nature 441, 39–45.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
|  CAS |
open url image1

Wu H, Gao K (2009) Ultraviolet radiation stimulated activity of extracellular carbonic anhydrase in the marine diatom Skeletonema costatum. Functional Plant Biology 36, 137–143.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Xu Z (2007) The physiological responses of two economic marine macroalgal species to nutrients supplies in seawater. MSc Thesis, Shantou University, Shantou, China.

Zheng Y, Gao K (2009) Impacts of solar UV radiation on the photosynthesis, growth and UV-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations. Journal of Phycology 45, 314–323.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zou D, Xia J, Yang Y (2004) Photosynthetic use of exogenous inorganic carbon in the agarophyte Gracilaria lemaneiformis (Rhodophyta). Aquaculture 237, 421–431.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1