CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Functional Plant Biology   
Functional Plant Biology
Journal Banner
  Plant Function & Evolutionary Biology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Research Fronts
Reviews
Evolutionary Reviews
Sample Issue
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow PrometheusWiki
blank image
PrometheusWiki
Protocols in ecological and environmental plant physiology

 

Article << Previous     |     Next >>   Contents Vol 40(9)

Plant proteome responses to salinity stress – comparison of glycophytes and halophytes

Klára Kosová A B , Pavel Vítámvás A , Milan Oldřich Urban A and Ilja Tom Prášil A

A Division of Plant Genetics, Breeding and Product Quality, Department of Genetics and Plant Breeding Methods, Crop Research Institute, Drnovska Street 507, 161 06 Prague 6 – Ruzyně, The Czech Republic.
B Corresponding author. Email: kosova@vurv.cz
This paper originates from a presentation at the COST WG2 MeetingPutting halophytes to workgenetics, biochemistry and physiologyHannover, Germany, 2831 August 2012.

Functional Plant Biology 40(9) 775-786 http://dx.doi.org/10.1071/FP12375
Submitted: 12 December 2012  Accepted: 25 March 2013   Published: 22 April 2013


 
PDF (363 KB) $25
 Export Citation
 Print
  
Abstract

The review discusses impacts of salinity on proteome composition in both salinity-sensitive (glycophytic) and salinity-tolerant (halophytic) plants. Salinity response with respect to proteome changes is compared in glycophytes and halophytes with a special focus on specific strategies employed by halophytes to cope with high (above 200 mM NaCl) salt concentrations. The results of comparative proteomic studies aimed at determination of the differences in salinity response between related plant species with contrasting salinity tolerance (Arabidopsis thaliana vs Thellungiella salsuginea, common wheat vs its hybrid, rice vs Porteresia coarctata) are analysed. The comparative studies have revealed that salt-tolerant plants display an enhanced constitutive expression of several salt-responsive genes and fewer salinity-related disturbances in energy metabolism with respect to the salt-sensitive plants. In conclusion, recent results of comparative proteomic studies are summarised and possible ways of utilisation of the obtained results for an improvement of plant (crop) salt tolerance are discussed.

Additional keywords: comparative proteomics, glycophyte, halophyte, proteome, salinity response, salt.


References

Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4, 2072–2081.
CrossRef | CAS | PubMed |

Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. Journal of Proteome Research 7, 4858–4868.
CrossRef | CAS | PubMed |

Aghaei K, Ehsanpour AA, Shah AH, Komatsu S (2009) Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 36, 91–98.
CrossRef | CAS | PubMed |

Askari H, Edqvist J, Hajheidari M, Kafi M, Salekdeh GH (2006) Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6, 2542–2554.
CrossRef | CAS | PubMed |

Bandehagh A, Salekdeh GH, Toorchi M, Mohammadi A, Komatsu S (2011) Comparative proteomic analysis of canola leaves under salinity stress. Proteomics 11, 1965–1975.
CrossRef | CAS | PubMed |

Barkla BJ, Vera-Estrella R, Hernandez-Coronado M, Pantoja O (2009) Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. The Plant Cell 21, 4044–4058.
CrossRef | CAS | PubMed |

Brini F, Hanin M, Lumbreras V, Irar S, Pages M, Masmoudi K (2007) Functional characterization of DHN-5, a dehydrin showing a differential phosphorylation pattern in two Tunisian durum wheat (Triticum durum Desf.) varieties with marked differences in salt and drought tolerance. Plant Science 172, 20–28.
CrossRef | CAS |

Caruso A, Morabito D, Delmotte F, Kahlem G, Carpin S (2002) Dehydrin induction during drought and osmotic stress in Populus. Plant Physiology and Biochemistry 40, 1033–1042.
CrossRef | CAS |

Caruso G, Cavaliere C, Guarino C, Gubbiotti R, Foglia P, Lagana A (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Analytical and Bioanalytical Chemistry 391, 381–390.
CrossRef | CAS | PubMed |

Chattopadhyay A, Subba P, Pandey A, Bhushan D, Kumar R, Datta A, Chakraborty S, Chakraborty N (2011) Analysis of the grasspea proteome and identification of stress-responsive proteins upon exposure to high salinity, low temperature, and abscisic acid treatment. Phytochemistry 72, 1293–1307.
CrossRef | CAS | PubMed |

Chen S, Gollop N, Heuer B (2009) Proteomic analysis of salt-stressed tomato (Solanum lycopersicum) seedlings: effect of genotype and exogenous application of glycinebetaine. Journal of Experimental Botany 60, 2005–2019.
CrossRef | CAS | PubMed |

Chen F, Zhang S, Jiang H, Ma W, Korpelainen H, Li C (2011) Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. Journal of Proteome Research 10, 3944–3958.
CrossRef | CAS | PubMed |

Cheng Y, Qi Y, Zhu Q, Chen X, Wang N, Zhao X, Chen H, Cui X, Xu L, Zhang W (2009) New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics 9, 3100–3114.
CrossRef | CAS | PubMed |

Chitteti B, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. Journal of Proteome Research 6, 1718–1727.
CrossRef | CAS | PubMed |

Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. Journal of Experimental Botany 57, 1059–1078.
CrossRef | CAS | PubMed |

Dani V, Simon WJ, Duranti M, Croy RRD (2005) Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 5, 737–745.
CrossRef | CAS | PubMed |

Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nature Genetics 43, 913–918.
CrossRef | CAS | PubMed |

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

Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71, 1450–1459.
CrossRef | CAS | PubMed |

Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T, Struik PC (2012) The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Molecular Biology Reports 39, 6387–6397.
CrossRef | CAS | PubMed |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. Tansley Review. New Phytologist 179, 945–963.
CrossRef | CAS | PubMed |

Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Quarterly Review of Biology 61, 313–337.
CrossRef |

Geissler N, Hussin S, Koyro HW (2010) Elevated atmospheric CO2 concentration enhances salinity tolerance in Aster tripolium L. Planta 231, 583–594.
CrossRef | CAS | PubMed |

Godoy JA, Lunar S, Torres-Schumann J, Moreno J, Rodrigo RM, Pintor-Toro JA (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Molecular Biology 26, 1921–1934.
CrossRef | CAS | PubMed |

Gong Q, Li P, Ma S, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44, 826–839.
CrossRef | CAS | PubMed |

Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC6803. Proteomics 6, 910–920.
CrossRef | CAS | PubMed |

Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. Journal of Proteome Research 9, 6595–6604.
CrossRef | CAS | PubMed |

Jaffrey SR, Snyder SH (2001) The biotin switch method for the detection of S-nitrosylated proteins. Science’s STKE 86, 1
CrossRef |

Jain S, Srivastava S, Sarin NB, Kav NNV (2006) Proteomics reveals elevated levels of PR10 proteins in saline-tolerant peanut (Arachis hypogaea) calli. Plant Physiology and Biochemistry 44, 253–259.
CrossRef | CAS | PubMed |

Jellouli N, Ben Jouira H, Skouri H, Ghorbel A, Gourgouri A, Mliki A (2008) Proteomic analysis of Tunisian grapevine cultivar Razegui under salt stress. Journal of Plant Physiology 165, 471–481.
CrossRef | CAS | PubMed |

Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. Journal of Experimental Botany 58, 3591–3607.
CrossRef | CAS | PubMed |

Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant, Cell & Environment 29, 1220–1234.
CrossRef | CAS |

Katz A, Waridel P, Shevchenko A, Pick U (2007) Salt-induced changes in the plasma membrane proteome of the halotolerant alga Dunaliella salina as revealed by blue native gel electrophoresis and nano-LC-MS/MS analysis. Molecular & Cellular Proteomics 6, 1459–1472.
CrossRef | CAS |

Kav NNV, Srivastava S, Goonewardene L, Blade SF (2004) Proteome-level changes in the roots of Pisum sativum in response to salinity. Annals of Applied Biology 145, 217–230.
CrossRef | CAS |

Kim DW, Rakwal R, Agrawal GK, Jung YH, Shibato J, Jwa NS, Iwahashi Y, Iwahashi H, Kim DH, Shim IS, Usui K (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26, 4521–4539.
CrossRef | CAS | PubMed |

Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress – contribution of proteomics studies to understanding plant stress response. Journal of Proteomics 74, 1301–1322.
CrossRef | PubMed |

Kumar Swami A, Alam SI, Sengupta N, Sarin R (2011) Differential proteomic analysis of salt response in Sorghum bicolor leaves. Environmental and Experimental Botany 71, 321–328.
CrossRef |

Kumari S, Panjabi SV, Kushwaha HR, Sopory SK, Singla-Pareek SL, Pareek A (2009) Transcriptome map for seedling stage specific salinity stress response indicates a specific set of genes as candidate for saline tolerance in Oryza sativa L. Functional & Integrative Genomics 9, 109–123.
CrossRef | CAS |

Li W, Zhang C, Lu Q, Wen X, Lu C (2011) The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. Journal of Plant Physiology 168, 1743–1752.
CrossRef | CAS | PubMed |

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 Physiology 136, 2806–2817.
CrossRef | CAS | PubMed |

Manaa A, Ahmed HB, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobet M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. Journal of Experimental Botany 62, 2797–2813.
CrossRef | CAS | PubMed |

Mehta PA, Rebala KC, Venkataraman G, Parida A (2009) A diurnally regulated dehydrin from Avicennia marina that shows nucleo-cytoplasmic localization and is phosphorylated by Casein kinase II in vitro. Plant Physiology and Biochemistry 47, 701–709.
CrossRef | CAS | PubMed |

Moons A, Bauw G, Prinsen E, Van Montagu M, Van Der Straeten D (1995) Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant Indica rice varietites. Plant Physiology 107, 177–186.
CrossRef | CAS | PubMed |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
CrossRef | CAS |

Munns R (2005) Genes and salt tolerance: bringing them together. Tansley Review. New Phytologist 167, 645–663.
CrossRef | CAS | PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS | PubMed |

Ngara R, Ndimba R, Borch-Jensen J, Jensen ON, Ndimba B (2012) Identification and profiling of salinity stress-responsive proteins in Sorghum bicolor seedlings. Journal of Proteomics 75, 4139–4150.
CrossRef | CAS | PubMed |

Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. Journal of Proteome Research 9, 2584–2599.
CrossRef | CAS | PubMed |

Parker R, Flowers TJ, Moore AL, Harpham NVJ (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. Journal of Experimental Botany 57, 1109–1118.
CrossRef | CAS | PubMed |

Peng Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Molecular & Cellular Proteomics 8, 2676–2686.
CrossRef | CAS |

Rasoulnia A, Bihamta MR, Peyghambari SA, Alizadeh H, Rahnama A (2011) Proteomic response of barley leaves to salinity. Molecular Biology Reports 38, 5055–5063.
CrossRef | CAS | PubMed |

Razavizadeh R, Ehsanpour AA, Ahsan N, Komatsu S (2009) Proteome analysis of tobacco leaves under salt stress. Peptides 30, 1651–1659.
CrossRef | CAS | PubMed |

Salekdeh GH, Komatsu S (2007) Crop proteomics: aim at sustainable agriculture of tomorrow. Proteomics 7, 2976–2996.
CrossRef | CAS | PubMed |

Sengupta S, Majumder AL (2009) Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229, 911–929.
CrossRef | CAS | PubMed |

Sengupta S, Majumder AL (2010) Porteresia coarctata (Roxb.) Tateoka, a wild rice: a potential model for studying salt-stress biology in rice Plant, Cell and Environment 33, 526–542.

Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences of the United States of America 97, 6896–6901.

Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465–477.
CrossRef | CAS | PubMed |

Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR, Motamed N, Komatsu S (2010a) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Science 8, 19
CrossRef | PubMed |

Sobhanian H, Motamed N, Jazii FR, Nakamura T, Komatsu S (2010b) Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant. Journal of Proteome Research 9, 2882–2897.
CrossRef | CAS | PubMed |

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

Sugimoto M, Takeda K (2009) Proteomic analysis of specific proteins in the root of salt-tolerant barley. Bioscience, Biotechnology, and Biochemistry 73, 2762–2765.
CrossRef | CAS | PubMed |

Tada Y, Kashimura T (2009) Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant & Cell Physiology 50, 439–446.
CrossRef | CAS |

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

Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal 60, 795–804.
CrossRef | CAS | PubMed |

Thompson JE, Hopkins MT, Taylor C, Wang TW (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends in Plant Science 9, 174–179.
CrossRef | CAS | PubMed |

Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. The Plant Cell 11, 1743–1754.
CrossRef | CAS | PubMed |

Veeranagamallaiah G, Jyothsnakumari G, Thippeswamy M, Reddy COP, Surabhi GK, Sriranganayakulu G, Mahesh Y, Rajasekhar B, Madhurarekha C, Sudhakar C (2008) Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv. Prasad) seedlings. Plant Science 175, 631–641.
CrossRef | CAS |

Vincent D, Ergül A, Bohlman MC, Tattersall EAR, Tillett RL, Wheatley MD, Woolsey R, Quilici DR, Joets J, Schlauch K, Schooley DA, Cushman JC, Cramer GR (2007) Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. Journal of Experimental Botany 58, 1873–1892.
CrossRef | CAS | PubMed |

Wakeel A, Asif AR, Pitann B, Schubert S (2011) Proteome analysis of sugar beet (Beta vulgaris L.) elucidates constitutive adaptation during the first phase of salt stress. Journal of Plant Physiology 168, 519–526.
CrossRef | CAS | PubMed |

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

Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, He Y (2008b) Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 228, 167–177.
CrossRef | CAS | PubMed |

Wang X, Fan P, Song H, Chen X, Li X, Li Y (2009) Comparative proteomic analysis of differentially expressed proteins in shoots of Salicornia europaea under different salinity. Journal of Proteome Research 8, 3331–3345.
CrossRef | CAS | PubMed |

Witzel K, Weidner A, Surabhi GK, Börner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. Journal of Experimental Botany 60, 3545–3557.
CrossRef | CAS | PubMed |

Witzel K, Weidner A, Surabhi GK, Varshney RK, Kunze G, Buck-Sorlin GH, Börner A, Mock HP (2010) Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant, Cell & Environment 33, 211–222.
CrossRef | CAS |

Xu C, Sibicky T, Huang B (2010) Protein profile analysis of salt-responsive proteins in leaves and roots in two cultivars of creeping bentgrass differing in salinity tolerance. Plant Cell Reports 29, 595–615.
CrossRef | CAS | PubMed |

Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781–803.
CrossRef | CAS | PubMed |

Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5, 235–244.
CrossRef | CAS | PubMed |

Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. Journal of Proteome Research 10, 3852–3870.
CrossRef | CAS | PubMed |

Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. Journal of Proteome Research 11, 49–67.
CrossRef | PubMed |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
CrossRef | CAS | PubMed |

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

Zörb C, Schmitt S, Mühling KH (2010) Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10, 4441–4449.
CrossRef | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014