Skip to main content
Springer Nature Link
Log in

Proteomic analysis of salinity-stressed Chlamydomonas reinhardtii revealed differential suppression and induction of a large number of important housekeeping proteins

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Salinity stress is one of the most common abiotic stresses that hamper plant productivity worldwide. Successful plant adaptations to salt stress require substantial changes in cellular protein expression. In this work, we present a 2-DE-based proteomic analysis of a model unicellular green alga, Chlamydomonas reinhardtii, subjected to 300 mM NaCl for 2 h. Results showed that, in addition to the protein spots that showed partial up- or down-regulation patterns, a number of proteins were exclusively present in the proteome of the control cells, but were absent from the salinity-stressed samples. Conversely, a large number of proteins exclusively appeared in the proteome of the salinity-stressed samples. Of those exclusive proteins, we could successfully identify, via LC–MS/MS, 18 spots uniquely present in the control cells and 99 spots specific to NaCl-treated cells. Interestingly, among the salt-exclusive protein spots, we identified several important housekeeping proteins like molecular chaperones and proteins of the translation machinery, suggesting that they may originate from post-translational modifications rather than from de novo biosynthesis. The possible role and the salt-specific modification of these proteins by salinity stress are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

2-DE:

Two-dimensional gel electrophoresis

LC–MS/MS:

Liquid chromatography couple with tandem mass spectrometry

PTM:

Post-translational modification

ROS:

Reactive oxygen species

References

  • Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice sheath. Proteomics 4:2072–2081

    Article  PubMed  CAS  Google Scholar 

  • Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    Article  PubMed  CAS  Google Scholar 

  • Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. J Proteome Res 7:4858–4868

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443–1453

    Article  PubMed  CAS  Google Scholar 

  • Arisz SA, Munnik T (2011) The salt stress-induced LPA response in Chlamydomonas is produced via PLA2 hydrolysis of DGK-generated phosphatidic acid. J Lipid Res 52:2012–2020

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Su H, Shen B (1999) Molecular mechanisms of salinity tolerance. In: Shinozaki K, Yamaguchi-Shinozaki K (eds) Molecular responses to cold, drought, heat and salt stress in higher plants. RG Landes Company, Austin, pp 29–60

    Google Scholar 

  • Boyer JS (1982) Plant productivity and environments. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  PubMed  CAS  Google Scholar 

  • Chitteti BR, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6:1718–1727

    Article  PubMed  CAS  Google Scholar 

  • Cruz JA, Salbilla BA, Kanazawa A, Kramer DM (2007) Inhibition of plastocyanin to P700+ electron transfer in Chlamydomonas reinhardtii by hyperosmotic stress. Plant Physiol 127:1167–1179

    Article  Google Scholar 

  • Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6:6498–6507

    Article  PubMed  CAS  Google Scholar 

  • Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6:2733–2745

    Article  PubMed  CAS  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook—a comprehensive guide to biology and laboratory use. Academic Press, San Diego

    Google Scholar 

  • Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910–920

    Article  PubMed  CAS  Google Scholar 

  • Kosová K, Vítámvás P, Prásil T, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322

    Article  PubMed  Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294

    Article  PubMed  CAS  Google Scholar 

  • Liska AJ, Shevchenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136:2806–2817

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Mahong B, Roytrakul S, Phaonaklop N, Wongratana J, Yokthongwattana K (2012) Proteomic analysis of a model unicellular green alga, Chlamydomonas reinhardtii, during short-term exposure to irradiance stress reveals significant down regulation of several heat-shock proteins. Planta. doi 10.1007/s00425-011-1521-x (in press)

  • Marín-Navarro J, Moreno J (2006) Cysteins 449 and 459 modulate the reduction-oxidation conformational changes of ribulose 1,5-bisphosphate carboxylase/oxygenase and the translocation of the enzyme to membranes during stress. Plant Cell Environ 29:898–908

    Article  PubMed  Google Scholar 

  • Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  PubMed  CAS  Google Scholar 

  • Ndimba BK, Chivasa S, Simon WJ, Slabas AR (2005) Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 5:4185–4196

    Article  PubMed  CAS  Google Scholar 

  • Neale PJ, Melis A (1989) Salinity-stress enhances photoinhibition of photosystem II in Chlamydomonas reinhardtii. J Plant Physiol 134:619–622

    Article  CAS  Google Scholar 

  • Pandhal J, Wright PC, Biggs CA (2008) Proteomics with a pinch of salt: a cyanobacterial perspective. Saline Systems 4:1. doi:10.1186/1746-1448-4-1

    Article  PubMed  Google Scholar 

  • Pandhal J, Ow SY, Wright PC, Biggs CA (2009) Comparative proteomics study of salt tolerance between a nonsequenced extremely halotolerant cyanobacterium and its mildly halotolerant relative using in vivo metabolic labeling and in vitro isobaric labeling. J Proteome Res 8:818–828

    Article  PubMed  CAS  Google Scholar 

  • Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative Proteomics of Salt Tolerance in Arabidopsis thaliana and Thellungiella halophile. J Proteome Res 9:2584–2599

    Article  PubMed  CAS  Google Scholar 

  • Shama PK, Hall DO (1991) Interaction of salt stress and photoinhibition on photosynthesis in barley and sorghum. J Plant Physiol 138:614–619

    Article  Google Scholar 

  • Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7 (http://www.biomedcentral.com/1472-6750/11/7)

    Google Scholar 

  • Sobhanian H, Aghaei K, Komatsu S (2011) Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops? J Proteomics 74:1323–1337

    Article  PubMed  CAS  Google Scholar 

  • Subramanyam R, Jolley C, Thangaraj B, Nellaepalli S, Webber AN, Fromme P (2010) Structural and functional changes of PSI–LHCI supercomplexes of Chlamydomonas reinhardtii cells grown under high salt conditions. Planta 231:913–922

    Article  PubMed  CAS  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu Y-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  PubMed  CAS  Google Scholar 

  • Vega JM, Garbayo I, Domínguez MJ, Vigara J (2006) Effects of abiotic stress on photosynthesis and respiration in Chlamydomonas reinhardtii: induction of oxidative stress. Enzyme Microb Tech 40:163–167

    Article  CAS  Google Scholar 

  • Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8:1470–1489

    Article  PubMed  CAS  Google Scholar 

  • Zörb C, Herbst R, Forreiter C, Schubert S (2009) Short-term effects of salt exposure on the maize chloroplast protein pattern. Proteomics 9:4209–4220

    Article  PubMed  Google Scholar 

  • Zuo Z-J, Zhu Y-R, Bai Y-L, Wang Y (2012) Volatile communication between Chlamydomonas reinhardtii cells under salt stress. Biochem Syst Ecol 40:19–24

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was conducted with funding in part from KURDI, Faculty of Science, Kasetsart University, Office of the Higher Education Commission and Thailand Research Fund grant # MRG5280035 to CY. KY thanks Thailand Research Fund, Office of the Higher Education Commission and Mahidol University for financial support.

Author information

Author notes

  1. Bancha Mahong

    Present address: Department of Plant Molecular Systems Biotechnology, Crop Biotech Institute, Kyung Hee University, Yongin, 446–701, Korea

Authors and Affiliations

  1. Department of Biochemistry, Faculty of Science, Kasetsart University, 50 Phahonyothin Rd., Bangkok, 10900, Thailand

    Chotika Yokthongwattana

  2. Department of Biochemistry, Center for Excellence in Protein Structure and Function, Faculty of Science, Mahidol University, 272 Rama 6 Rd., Bangkok, 10400, Thailand

    Bancha Mahong & Kittisak Yokthongwattana

  3. Genome Institute, National Center for Genetic Engineering and Biotechnology, 113 Thailand Science Park, Phahonyothin Rd., Pathumthani, 12120, Thailand

    Sittiruk Roytrakul & Narumon Phaonaklop

  4. Department of Biotechnology, Faculty of Science, Mahidol University, 272 Rama 6 Rd., Bangkok, 10400, Thailand

    Jarunya Narangajavana

Authors
  1. Chotika Yokthongwattana
    View author publications

    Search author on:PubMed Google Scholar

  2. Bancha Mahong
    View author publications

    Search author on:PubMed Google Scholar

  3. Sittiruk Roytrakul
    View author publications

    Search author on:PubMed Google Scholar

  4. Narumon Phaonaklop
    View author publications

    Search author on:PubMed Google Scholar

  5. Jarunya Narangajavana
    View author publications

    Search author on:PubMed Google Scholar

  6. Kittisak Yokthongwattana
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Kittisak Yokthongwattana.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yokthongwattana, C., Mahong, B., Roytrakul, S. et al. Proteomic analysis of salinity-stressed Chlamydomonas reinhardtii revealed differential suppression and induction of a large number of important housekeeping proteins. Planta 235, 649–659 (2012). https://doi.org/10.1007/s00425-012-1594-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1594-1

Keywords

Profiles

  1. Kittisak Yokthongwattana View author profile