Plant Molecular Biology Reporter

, Volume 30, Issue 1, pp 10–16 | Cite as

Characterization of the LhcSR Gene Under Light and Temperature Stress in the Green Alga Ulva linza

  • Meitao Dong
  • Xiaowen Zhang
  • Zhimeng Zhuang
  • Jian Zou
  • Naihao YeEmail author
  • Dong Xu
  • Shanli Mou
  • Chengwei Liang
  • Wenqi WangEmail author


As a green-tide-forming macroalga, Ulva linza is distributed worldwide and therefore subject to various environmental stresses. The LHCSR (also known as LI818 in green alga and LHCX in diatoms) protein is a stress-related member of the LHC family that plays an important role in photo-protective mechanism, which has been only found in algae. In this study, we cloned full-length cDNA sequence encoding the LhcSR gene from U. linza and analyzed its expression in response to different temperature and illumination gradients. The results showed that high light (HL) could enhance expression of LhcSR and that the expression level peaked at 3 h under HL. Similarly, the expression of LhcSR could also be induced by low temperature (LT). However, the expression patterns of LhcSR were quite different in response to LT and HL treatment. Specifically, the maximum gene expression under LT was much higher (11.8-fold) than under HL (5.4-fold) when compared to the expression under normal conditions. The upregulated expression of LhcSR lasted for 12 h under LT, but 3 h under HL. These data suggest that the LhcSR gene is involved in photoprotection in U. linza, and the results suggest a stronger link to LT. In addition, the discrepancy in expression under HL and LT was consistent with the ecological features of this alga, which only thrives during the cold season (featured as LT and low light).


Ulva linza LhcSR Full-length Expression analysis Green tide 



This work was supported by National special fund for transgenic project (2009ZX08009-019B), the Hi-Tech Research and Development Program (863) of China (2009AA10Z106), Natural Science Foundation of Shandong Province (2009ZRA02075), Qingdao Municipal Science and Technology plan project (09-2-5-8-hy, 10-4-1-13-hy) and the National Science & Technology Pillar Program (2008BAD95B11).


  1. Carzoli FG, Michelotti V, Fambrini M, Salvini M, Pugliesi C (2009) Molecular cloning and organ-specific expression of two gibberellin 20-oxidase genes of Helianthus annuus. Plant Mol Biol Rep 27:144–152CrossRefGoogle Scholar
  2. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequences alignment with the clustal series of programs. Nucleic Acids Res 31:3497–3500PubMedCrossRefGoogle Scholar
  3. Demeter S, Janda T, Kovacs L, Mende D, Wiessner W (1995) Effects of in vivo CO2-depletion on electron transport and photoinhibition in the green algae, Chlamydobotrys stellata and Chlamydomonas reinhardtii. Biochim Biophys Acta 1229:1–9CrossRefGoogle Scholar
  4. Figueroa FL, Jiménez C, Lubián LM, Montero O, Lebert M, Häder D-P (1997) Effects of high irradiance and temperature on photosynthesis and photoinhibition in Nannochloropsis gaditana Lubián (Eustigmatophyceae). J Plant Phys 151:6–15CrossRefGoogle Scholar
  5. Fletcher RL (1996) The British Isles. In: Schramm W, Nienhuis PH (eds) Marine benthic vegetation: recent changes and the effects of eutrophication. Springer, Berlin, pp 150–223Google Scholar
  6. Fu G, Yao J, Liu F, Liu J, Wang X, Fu W, Li D, Zhou M, Sun S, Duan D (2008) Effect of temperature and irradiance on the growth and reproduction of Enteromorpha prolifera J. Ag. (Chlorophycophyta, Chlorophyceae). Chin J Ocean Limnol 4:357–362CrossRefGoogle Scholar
  7. Fu W, Shuai L, Yao J, Yu S, Liu F, Duan D (2010) Molecular cloning and analysis of a cytosolic Hsp70 gene from Enteromorpha prolifera (Ulvophyceae, Chlorophyta). Plant Mol Biol Rep 28:430–437CrossRefGoogle Scholar
  8. Gao S, Chen X, Yi Q, Wang G, Pan G, Lin A, Peng G (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of Sporangia by fragmentation. PloS ONE 5(1):e8571. doi: 10.1371/journal.pone.0008571 PubMedCrossRefGoogle Scholar
  9. Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:685–714PubMedCrossRefGoogle Scholar
  10. Guiry MD, Guiry GM (2007) Algae Base version 4.2. Worldwide electronic publication: National University of Ireland, Galway. Available at: (Accessed 2 May 2007).
  11. Häder D-P, Lebert M, Helbling EW (2001) Effects of solar radiation on the Patagonian macroalga Enteromorpha linza (L.) J. Agardh—Chlorophyceae. J Photoch Photobio B 62:43–54CrossRefGoogle Scholar
  12. Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294CrossRefGoogle Scholar
  13. Im CS, Zhang ZD, Shrager J, Chang CW, Grossman AR (2003) Analysis of light and CO2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth Res 75:111–125PubMedCrossRefGoogle Scholar
  14. Kong FN, Jiang SM, Meng XB, Song CL, Shi JF, Jin DM, Jiang SL, Wang B (2009) Cloning and characterization of the DHDPS gene encoding the lysine biosynthetic enzyme dihydrodipocolinate synthase from Zizania latifolia (Griiseb). Plant Mol Biol Report 27:199–208CrossRefGoogle Scholar
  15. Ledford HK, Baroli I, Shin JW, Fischer BB, Eggen RIL, Niyogi KK (2004) Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii. Mol Genet Genomics 272:470–479PubMedCrossRefGoogle Scholar
  16. Li T, Gong C, Wang T (2010) The rice light-regulated gene RA68 encodes a novel protein interacting with oxygen-evolving complex PsbO mature protein. Plant Mol Biol Rep 28:136–143CrossRefGoogle Scholar
  17. Lin A, Shen S, Wang J, Yan B (2008) Reproduction diversity of Enteromorpha prolifera. J Integr Plant Biol 50:622–629PubMedCrossRefGoogle Scholar
  18. Liu XM, Anderson JM, Pijut PM (2010) Cloning and characterization of Prunus serotina AGAMOUS, a putative flower homeotic gene. Plant Mol Biol Rep 28:193–203CrossRefGoogle Scholar
  19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408Google Scholar
  20. Luo T, Deng WY, Zeng J, Zhang FL (2009) Cloning and characterization of a stearoyl–acyl carrier protein desaturase gene from Cinnamomum longepaniculatum. Plant Mol Biol Rep 27:13–19CrossRefGoogle Scholar
  21. Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, Ohyama K, Fukuzawa H (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135:1595–1607PubMedCrossRefGoogle Scholar
  22. Mu XW, Lu QQ, Hu CM, Chen SY, Zhang T, Zhang XF, Xu P (2010) Preliminary report on the green algae investigation in mariculture ponds along the coastline of Jiangsu Province. In: Wang QY (ed) Marine aquaculture industry based on ecologic system. China Ocean Press, Beijing, pp 28–37Google Scholar
  23. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7:3964–3979PubMedCrossRefGoogle Scholar
  24. Neilson JA, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71PubMedCrossRefGoogle Scholar
  25. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50:333–359PubMedCrossRefGoogle Scholar
  26. Niyogi KK (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3:455–460PubMedCrossRefGoogle Scholar
  27. Nymark M, Valle KC, Brembu T, Hancke K, Winge P, Andresen K, Johnsen G, Bones AM (2009) An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PloS ONE 4:e7743Google Scholar
  28. Park S, Jung G, Hwan Y-S, Jin E (2010) Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to high irradiance. Planta 231:349–360Google Scholar
  29. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521PubMedCrossRefGoogle Scholar
  30. Richard C, Ouellet H, Guertin M (2000) Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol Biol 42:303–316PubMedCrossRefGoogle Scholar
  31. Sambrook J, Fritsch EF, Maniatis T (2001) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New YorkGoogle Scholar
  32. Savard F, Richard C, Guertin M (1996) The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol Biol 32:461–473PubMedCrossRefGoogle Scholar
  33. Soria-Guerra RE, Rosales-Mendoza S, Gasic K, Wisniewski ME, Band M, Korban SS (2011) Gene expression is highly regulated in early developing fruit of apple. Plant Mol Bio Rep. doi: 10.1007/s11105-011-0300-y Google Scholar
  34. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  35. Taylor R, Fletcher RL, Raven JA (2001) Preliminary studies on the growth of selected “green tide” algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Bot Mar 44:327–336CrossRefGoogle Scholar
  36. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  37. Wang L, Li X, Zhao Q, Jing S, Chen S, Yuan H (2009) Identification of genes induced in response to low-temperature treatment in tea leaves. Plant Mol Biol Rep 27:257–265CrossRefGoogle Scholar
  38. Ye NH, Zhang XW, Mao YZ, Liang CW, Xu D, Zou J, Zhuang ZM, Wang QY (2011) ‘Green tides’ are overwhelming the coastline of our blue planet: taking the world’s largest example. Ecol Res. doi: 10.1007/s11284-011-0821-8
  39. Ye NH, Zhuang ZM, Jin XS, Wang QY, Zhang XW, Li DM, Wang HX, Mao YZ, Jiang ZJ, Li B, Xue ZX (2008) China is on the tracking Enteromorpha spp Forming green tide. Nature Proceedings hdl:10101/npre 2008; 2352.1.Google Scholar
  40. Zhang ZD, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348PubMedCrossRefGoogle Scholar
  41. Zhang X, Wang H, Mao Y, Liang C, Zhuang Z, Wang Q, Ye N (2010) Somatic cells serve as a potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. J Appl Phycol 22:173–180CrossRefGoogle Scholar
  42. Zhang XW, Xu D, Mao YZ, Li YX, Xue SY, Zou J, Lian W, Liang CW, Zhuang ZM, Wang QY, Ye NH (2011) Vegetative fragments of Ulva prolifera in settlement confirmed as an important seed source for succession of a large-scale green tide bloom. Limnol Oceanogr 56:233–242CrossRefGoogle Scholar
  43. Zhu SH, Beverley RG (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797:1449–1457PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Meitao Dong
    • 1
    • 2
  • Xiaowen Zhang
    • 1
  • Zhimeng Zhuang
    • 1
  • Jian Zou
    • 1
  • Naihao Ye
    • 1
    Email author
  • Dong Xu
    • 1
  • Shanli Mou
    • 3
  • Chengwei Liang
    • 4
  • Wenqi Wang
    • 2
    Email author
  1. 1.Yellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdaoChina
  2. 2.Qingdao Agricultural UniversityQingdaoChina
  3. 3.Key Laboratory of Marine Bioactive substance, The First Institute of OceanographyState Oceanic Administration (SOA)QingdaoChina
  4. 4.Qingdao University of Science & TechnologyQingdaoChina

Personalised recommendations