Proteomic responses in shoots of the facultative halophyte Aeluropus littoralis (Poaceae) under NaCl salt stress
Wassim Azri A D , Zouhaier Barhoumi B C , Farhat Chibani A , Manel Borji A , Mouna Bessrour B and Ahmed Mliki AA Laboratory of Plant Molecular Physiology, Biotechnology Centre of Borj Cedria, PO Box 901, 2050 Hammam-Lif, Tunisia.
B Laboratory of Extremophyle Plants, Biotechnology Centre of Borj Cedria, PO Box 901, 2050 Hammam-Lif, Tunisia.
C King Khalid University, Biology Department, PO Box- 9004, Abha- 61413 Kingdom of Saudi Arabia.
D Corresponding author. Email: azwassim@yahoo.fr
Functional Plant Biology 43(11) 1028-1047 https://doi.org/10.1071/FP16114
Submitted: 24 March 2016 Accepted: 13 July 2016 Published: 9 August 2016
Abstract
Salinity is an environmental constraint that limits agricultural productivity worldwide. Studies on the halophytes provide valuable information to describe the physiological and molecular mechanisms of salinity tolerance. Therefore, because of genetic relationships of Aeluropus littoralis (Willd) Parl. with rice, wheat and barley, the present study was conducted to investigate changes in shoot proteome patterns in response to different salt treatments using proteomic methods. To examine the effect of salinity on A. littoralis proteome pattern, salt treatments (0, 200 and 400 mM NaCl) were applied for 24 h and 7 and 30 days. After 24 h and 7 days exposure to salt treatments, seedlings were fresh and green, but after 30 days, severe chlorosis was established in old leaves of 400 mM NaCl-salt treated plants. Comparative proteomic analysis of the leaves revealed that the relative abundance of 95 and 120 proteins was significantly altered in 200 and 400 mM NaCl treated plants respectively. Mass spectrometry-based identification was successful for 66 out of 98 selected protein spots. These proteins were mainly involved in carbohydrate, energy, amino acids and protein metabolisms, photosynthesis, detoxification, oxidative stress, translation, transcription and signal transduction. These results suggest that the reduction of proteins related to photosynthesis and induction of proteins involved in glycolysis, tricarboxylic acid (TCA) cycle, and energy metabolism could be the main mechanisms for salt tolerance in A. littoralis. This study provides important information about salt tolerance, and a framework for further functional studies on the identified proteins in A. littoralis.
Additional keywords: proteomics, salt-tolerance.
References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=99fa8bbb1f5b69ffca6fc56116a2dc3fCAS | 15377225PubMed |
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.
| Effects of salinity levels on proteome of Suaeda aegyptiaca leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslCgsbs%3D&md5=596cfe17689ddae04975de383c186c95CAS | 16612795PubMed |
Azri W, Chambon C, Herbette S, Brunel N, Coutand C, Leplé J-C, Ben Rejeb I, Ammar S, Julien JL, Roeckel-Drevet P (2009) Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation. Physiologia Plantarum 136, 193–208.
| Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlehsb8%3D&md5=f6e742880af6a467feb046935197f8e7CAS | 19453506PubMed |
Barhoumi Z, Djebali W, Smaoui A, Chaïbi W, Abdelly C (2007a) Contribution of NaCl excretion to salt resistance of Aeluropus littoralis (Willd) Parl. Journal of Plant Physiology 164, 842–850.
| Contribution of NaCl excretion to salt resistance of Aeluropus littoralis (Willd) Parl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslSisbc%3D&md5=acc919c1df416626a44845df2a23ca66CAS | 16876911PubMed |
Barhoumi Z, Djebali W, Chaibi W, Abdelly C, Smaoui A (2007b) Salt impact on photosynthesis and leaf ultrastructure in Aeluropus littoralis (Willd) Part. Journal of Plant Research 120, 529–537.
| Salt impact on photosynthesis and leaf ultrastructure in Aeluropus littoralis (Willd) Part.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntFOgurc%3D&md5=9c60a379c10f0594972a3ad7e7686499CAS | 17534691PubMed |
Ben Saad RB, Zouari N, Ramdhan WB, Azaza J, Meynard D, Guiderdoni E, Hassairi A (2010) Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger ‘AlSAP’ gene isolated from the halophyte grass Aeluropus littoralis. Plant Molecular Biology 72, 171–190.
| Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger ‘AlSAP’ gene isolated from the halophyte grass Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2mtb%2FO&md5=eff3a4d6f484e24fb6f448250109e91eCAS |
Bertoni G (2011) CBS domain proteins regulate redox homeostasis. The Plant Cell 23, 3562
| CBS domain proteins regulate redox homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1eku73P&md5=1ad1bfaaed7eb134bf429e9133d67f42CAS | 22021415PubMed |
Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot MB, Altman A, Polle A, Dreyer E, Rudd S, Paulin L, Auvinen P, Kangasjärvi J (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biology 6, R101
| Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert.Crossref | GoogleScholarGoogle Scholar | 16356264PubMed |
Carpentier SC, Panis B, Vertommen A, Swennen R, Sergeant K, Renaut J, Laukens K, Witters E, Samyn B, Devreese B (2008) Proteome analysis of non-model plants: a challenging but powerful approach. Mass Spectrometry Reviews 27, 354–377.
| Proteome analysis of non-model plants: a challenging but powerful approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVGiu70%3D&md5=4614b96869cc825895c86400a00b21efCAS | 18381744PubMed |
Centritto M, Loreto F, Chartzoulakis K (2003) The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant, Cell & Environment 26, 585–594.
| The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings.Crossref | GoogleScholarGoogle Scholar |
Chen JG, Wang SC, Lazarus CM, Napier RM, Jones AM (2006) Altered expression of auxin-binding protein 1 affects cell expansion and auxin pool size in tobacco cells. Journal of Plant Growth Regulation 25, 69–78.
| Altered expression of auxin-binding protein 1 affects cell expansion and auxin pool size in tobacco cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitlKgsbw%3D&md5=3004b530213c1a7885854cd80bd96007CAS |
Cheng T, Chen J, Zhang J, Shi S, Zhou Y, Lu L, Wang P, Jiang Z, Yang J, Zhang S, Shi J (2015) Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse response pathways critical for high salinity tolerance. Frontiers in Plant Science 6, 30
| Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse response pathways critical for high salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 25713577PubMed |
Debez A, Braun H, Pich A, Taamalli W, Koyro H, Abdelly C (2012) Huchzermeyer, B. Proteomic and physiological responses of the halophyte Cakile maritima to moderate salinity at the germinative and vegetative stages. Journal of Proteomics 75, 5667–5694.
| Huchzermeyer, B. Proteomic and physiological responses of the halophyte Cakile maritima to moderate salinity at the germinative and vegetative stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOgsLnI&md5=5e7c9c90f5c64f47aa81d022032a84ccCAS | 22940175PubMed |
Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6, 6498–6507.
| Proteomic responses of rice young panicles to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1Kisg%3D%3D&md5=daf39ca966eaa4bdaa7a59376fdfac35CAS | 17163441PubMed |
Fan P, Feng J, Jiang P, Chen X, Bao H, Nie L, Jiang D, Lv S, Kuang T, Li Y (2011) Coordination of carbon fixation and nitrogen metabolism in Salicornia europaea under salinity: comparative proteomic analysis on chloroplast proteins. Proteomics 11, 4346–4367.
| Coordination of carbon fixation and nitrogen metabolism in Salicornia europaea under salinity: comparative proteomic analysis on chloroplast proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSiu7bN&md5=2e0350ad8aa99582861859a94d3140f7CAS | 21905221PubMed |
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Annals of Botany 115, 327–331.
| Plant salt tolerance: adaptations in halophytes.Crossref | GoogleScholarGoogle Scholar | 25844430PubMed |
Gagneul D, Aïnouche A, Duhazé C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiology 144, 1598–1611.
| A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1Olsbg%3D&md5=de92a4071d309f0539685b8586caf3fbCAS | 17468212PubMed |
Gao F, Gao Q, Duan X, Yue G, Yang A, Zhang J (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. Journal of Experimental Botany 57, 3259–3270.
| Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1ygt7k%3D&md5=372ca9cc12420f6289e5657707a13b4cCAS | 16940040PubMed |
Gao F, Zhou Y, Zhu W, Li X, Fan L, Zhang G (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230, 1033–1046.
| Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOiurjF&md5=c431ba3046b00474c0188fba9361859cCAS | 19705148PubMed |
Gilbert L, Alhagdow M, Nunes-Nesi A, Quemener B, Guillon F, Bouchet B, Faurobert M, Gouble B, Page D, Garcia V, Petit J, Stevens R, Causse M, Fernie AR, Lahaye M, Rothan C, Baldet P (2009) GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. The Plant Journal 60, 499–508.
| GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVKisL3M&md5=8c2dbb1ad120fd551fd43e0c652bacb6CAS | 19619161PubMed |
Guan B, Hu Y, Zeng Y, Wang Y, Zhang F (2011) Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica. Molecular Biology Reports 38, 1889–1899.
| Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlensLg%3D&md5=55c851d1e11db2ccf48c35a544b63eedCAS | 20886297PubMed |
Guo S, Yin H, Zhang X, Zhao F, Li P, Chen S, Zhao Y, Zhang H (2006) Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Molecular Biology 60, 41–50.
| Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFynsbc%3D&md5=b63a29448e2e3935a2bb1eeb71fe5a11CAS | 16463098PubMed |
Habermann B, Oegema J, Sunyaev S, Shevchenko A (2004) The power and the limitations of cross-species protein identification by mass spectrometrydriven sequence similarity searches. Molecular & Cellular Proteomics 3, 238–249.
| The power and the limitations of cross-species protein identification by mass spectrometrydriven sequence similarity searches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisFWhsbo%3D&md5=026a019302218546021d6d56a758637aCAS |
Hafsi C, Romero-Puertas MC, Gupta DK, del Río LA, Sandalio LM, Abdelly C (2010) Moderate salinity enhances the antioxidative response in the halophyte Hordeum maritimum L. under potassium deficiency. Environmental and Experimental Botany 69, 129–136.
| Moderate salinity enhances the antioxidative response in the halophyte Hordeum maritimum L. under potassium deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFant7Y%3D&md5=5ccb2946fed2039efd5e621e604ba35bCAS |
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
| Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=6d8ab79bcb839ec84ba41d6870cfc25eCAS | 15012199PubMed |
Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Bureau of Horticulture Technical Communication 22.
Hossain Z, Nouri M, Komatsu S (2012) Plant cell organelle proteomics in response to abiotic stress. Journal of Proteome Research 11, 37–48.
| Plant cell organelle proteomics in response to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOgu7jM&md5=6ab286ca062b033a621a5cb9564af0ddCAS | 22029473PubMed |
Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiology 135, 1718–1737.
| Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqsbg%3D&md5=bf475e06505a5567e681f741a4037bcdCAS | 15247369PubMed |
Jiménez S, Li ZG, Reighard GL, Bielenberg DG (2010) Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. BMC Plant Biology 10, 25
| Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant.Crossref | GoogleScholarGoogle Scholar | 20144228PubMed |
Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Frontiers in Plant Science 6, 114
| Chromatin changes in response to drought, salinity, heat, and cold stresses in plants.Crossref | GoogleScholarGoogle Scholar | 25784920PubMed |
Kogan GL, Gvozdev VA (2014) Multifunctional nascent polypeptide-associated complex (NAC). Molecular Biology 48, 189–196.
| Multifunctional nascent polypeptide-associated complex (NAC).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntFGgsbs%3D&md5=776712dd686138a037e3e9dc64ee444cCAS |
Kosová K, Vítámvás P, Urban MO, Prášil IT (2013a) Plant proteome responses to salinity stress – comparison of glycophytes and halophytes. Functional Plant Biology 40, 775–786.
| Plant proteome responses to salinity stress – comparison of glycophytes and halophytes.Crossref | GoogleScholarGoogle Scholar |
Kosová K, Prášil IT, Vítámvás P (2013b) Protein contribution to plant salinity response and tolerance acquisition. International Journal of Molecular Sciences 14, 6757–6789.
| Protein contribution to plant salinity response and tolerance acquisition.Crossref | GoogleScholarGoogle Scholar | 23531537PubMed |
Kovach WL (1999) ‘MVSP—A multivariate statistical package for Windows. Ver. 3.1.’ (Kovach Computing Services: Pentraeth, Wales, UK)
Krapp AR, Tognetti VB, Carrillo N, Acevedo A (1997) The role of ferredoxin-NADP+ reductase in the concerted cell defense against oxidative damage. European Journal of Biochemistry 249, 556–563.
| The role of ferredoxin-NADP+ reductase in the concerted cell defense against oxidative damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFeltr4%3D&md5=7494b5ee1f832904ec7826e7dc0037daCAS | 9370367PubMed |
Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectivs of salinity tolerance in halophytes. Frontiers in Plant Science 6, 537
| Proteomics, metabolomics, and ionomics perspectivs of salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 26284080PubMed |
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=f771fc7db2ab91c72fd2b429b6d4095aCAS | 5432063PubMed |
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.
| The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFGiu78%3D&md5=b50a5a8757e0864c5a74b78d27e8cc45CAS | 21663998PubMed |
Liu X, Yang C, Zhang L, Li L, Liu S, Yu J, You L, Zhou D, Xia C, Zhao J, Wu H (2011) Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics. Ecotoxicology (London, England) 20, 1422–1431.
| Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslahsbY%3D&md5=b86bdad1a00336dbb13dec3959c23e62CAS |
Liu C-W, Chang T-S, Hsu Y-K, Wang AZ, Yen H-C, Wu Y-P, Wang CS, Lai CC (2014) Comparative proteomic analysis of early salt stress responsive proteins in roots and leaves of rice. Proteomics 14, 1759–1775.
| Comparative proteomic analysis of early salt stress responsive proteins in roots and leaves of rice.Crossref | GoogleScholarGoogle Scholar | 24841874PubMed |
Liu H, Sultan MARF, Liu XL, Zhang J, Yu F, Zhao HX (2015) Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS One 10, e0121852
| Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum).Crossref | GoogleScholarGoogle Scholar | 25859656PubMed |
Modarresi M, Nematzadeh G, Moradian F, Alavi S (2012) Identification and cloning of the Cu/Zn superoxide dismutase gene from halophyte plant Aeluropus littoralis. Russian Journal of Genetics 48, 118–122.
| Identification and cloning of the Cu/Zn superoxide dismutase gene from halophyte plant Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjsl2ktA%3D%3D&md5=1092b87fc28a7340588598dcd6a03359CAS |
Modarresi M, Nematzadeh GA, Zarein M (2013) Glyceraldehyde-3-phosphate dehydrogenase gene from halophyte Aeluropus lagopoides: identification and characterization. Journal of Crop Improvement 27, 281–290.
| Glyceraldehyde-3-phosphate dehydrogenase gene from halophyte Aeluropus lagopoides: identification and characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXks1Oksbc%3D&md5=d6fde7c6a4684f645b69bcf56c1cec38CAS |
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
| Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=ec575b5a94258a1c6a8d564f45b9464eCAS |
Munns R (2005) Genes and salt tolerance: bringing them together. Tansley review. New Phytologist 167, 645–663.
| Genes and salt tolerance: bringing them together. Tansley review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGisbfP&md5=8fe6bc89fa7bf2db6d4f7f44c2294ae5CAS | 16101905PubMed |
Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9, 255–262.
| Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXksFWisro%3D&md5=0baa20599fdc5763140bdaefdfa4f27bCAS | 2466658PubMed |
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.
| Identification and profiling of salinity stress-responsive proteins in Sorghum bicolor seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFCisLg%3D&md5=bf8645eeeebde2c6d1976af13b6c6d9fCAS | 22652490PubMed |
Ohmiya A, Tanaka Y, Kadowaki K, Hayashi T (1998) Cloning of genes encoding auxin-binding proteins (ABP19/20) from peach: significant peptide sequence similarity with germin-like proteins. Plant & Cell Physiology 39, 492–499.
| Cloning of genes encoding auxin-binding proteins (ABP19/20) from peach: significant peptide sequence similarity with germin-like proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsFSmt74%3D&md5=aa54e46182389c7740f18da8ce480a5cCAS |
Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Letters 532, 279–282.
| Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptlCqt7g%3D&md5=6f702a2e4490f9f7d790cf84848afca5CAS | 12482579PubMed |
Palma JM, Sandalio LM, Javier Corpas F, Romero-Puertas MC, McCarthy I, del Rıo LA (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiology and Biochemistry 40, 521–530.
| Plant proteases, protein degradation, and oxidative stress: role of peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVajtbs%3D&md5=a33ad9bbe0c7efc284c04212020331f0CAS |
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.
| Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvVKrur8%3D&md5=1f10d4c02c7db9cf541ff69541c6c33aCAS | 20377188PubMed |
Parker R, Flowers TJ, Moore AL, Harpham NV (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.
| An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls7k%3D&md5=a588e5fdca402e7ee39d00d10cb228aaCAS | 16513811PubMed |
Ramagli LS, Rodriguez LV (1985) Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 6, 559–563.
| Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xhslentg%3D%3D&md5=12b38eae4f71523703571131a9cc45dfCAS |
Redondo-Gómez S, Mateos-Naranjo E, Davy AJ, Fernández-Muñoz F, Castellanos EM, Luque T, Figueroa ME (2007) Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Annals of Botany 100, 555–563.
| Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides.Crossref | GoogleScholarGoogle Scholar | 17684026PubMed |
Renard BY, Xu B, Kirchner M, Zickmann F, Winter D, Korten S, Brattig NW, Tzur A, Hamprecht FA, Steen H (2012) Overcoming species boundaries in peptide identification with Bayesian information criterion-driven error-tolerant peptide search (BICEPS). Molecular & Cellular Proteomics 11, M111.014167
| Overcoming species boundaries in peptide identification with Bayesian information criterion-driven error-tolerant peptide search (BICEPS).Crossref | GoogleScholarGoogle Scholar |
Rospert S, Dubaquie Y, Gautschi M (2002) Nascent-polypeptide-associated complex. Cellular and Molecular Life Sciences 59, 1632–1639.
| Nascent-polypeptide-associated complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOntbg%3D&md5=f27a7e630cf96dd059f978fe6e55aa9dCAS | 12475173PubMed |
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiologia Plantarum 132, 209–219.
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.
| Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agsb0%3D&md5=18b3f5cb2f600963b3e2fd6d445f2638CAS | 19130079PubMed |
Singh BN, Mishra RN, Agarwal PK, Goswami M, Nair S, Sopory SK, Reddy MK (2004) A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochemical and Biophysical Research Communications 320, 523–530.
| A pea chloroplast translation elongation factor that is regulated by abiotic factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1egtLw%3D&md5=9255f3ed0c9616449b29b470cd39c62fCAS | 15219860PubMed |
Sinha R, Chattopadhyay S (2011) Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternata infection. Journal of Proteomics 74, 327–336.
| Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternata infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWqsrg%3D&md5=4cc12f1dce0d9ff1422512dec1e69ce6CAS | 21111074PubMed |
Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115, 433–447.
| Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 25564467PubMed |
Sobhanian H, Motamed N, Jazii FR, Nakamura T, Komatsu S (2010a) 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.
| Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1OntrY%3D&md5=b0dcf4e68626be18e7ae093ead7610b9CAS | 20397718PubMed |
Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii R, Motamed N, Komatsu S (2010b) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Science 8, 19
| Proteome analysis of soybean leaves, hypocotyls and roots under salt stress.Crossref | GoogleScholarGoogle Scholar | 20350314PubMed |
Sousa MF, Campos FAP, Prisco JT, Enéas-Filho J, Gomes-Filho E (2003) Growth and protein pattern in cowpea seedlings subjected to salinity. Biologia Plantarum 47, 341–346.
| Growth and protein pattern in cowpea seedlings subjected to salinity.Crossref | GoogleScholarGoogle Scholar |
Tada Y, Kashimura T (2009) Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant & Cell Physiology 50, 439–446.
| Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFSjtrk%3D&md5=2d463ff08aa32bc47791966c22c9d67dCAS |
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.
| Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqsb4%3D&md5=afe368a0cc4c91c323765f1d70e76c6cCAS | 15247402PubMed |
Tasleem-Tahir A, Nadaud I, Chambon C, Branlard G (2012) Expression profiling of starchy endosperm metabolic proteins at 21 stages of wheat grain development. Journal of Proteome Research 11, 2754–2773.
| Expression profiling of starchy endosperm metabolic proteins at 21 stages of wheat grain development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlGltb4%3D&md5=633023e04ce079ad5db2afb16a42d66dCAS | 22394196PubMed |
Vítámvás P, Prášil IT, Kosová K, Planchon S, Renaut J (2012) Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics 12, 68–85.
| Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation.Crossref | GoogleScholarGoogle Scholar | 22065556PubMed |
Wan XY, Liu JY (2008) Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Molecular & Cellular Proteomics 7, 1469–1488.
| Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrs7vN&md5=ac69f72cb2a04a2f1e7d2e6fca9a5382CAS |
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.
| Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVOmsb4%3D&md5=93651dfaf8568c9ae2c9de9a57252b6dCAS | 18383010PubMed |
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.
| Proteomic analysis of the response to high-salinity stress in Physcomitrella patens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtVamtrs%3D&md5=f60f6b35229471848fb53b279747d54fCAS | 18351383PubMed |
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.
| Comparative proteomic analysis of differentially expressed proteins in shoots of Salicornia europaea under different salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFOitLY%3D&md5=bd2c1c90d3555fb7438af2b2bb7f6804CAS | 19445527PubMed |
Wang X, Chang L, Wang B, Wang D, Li P, Wang L, Yi X, Huang Q, Peng M, Guo A (2013) Comparative proteomics of Thellungiella halophila leaves under different salinity revealed chloroplast starch and soluble sugar accumulation played important roles in halophyte salt tolerance. Molecular & Cellular Proteomics 12, 2174–2195.
| Comparative proteomics of Thellungiella halophila leaves under different salinity revealed chloroplast starch and soluble sugar accumulation played important roles in halophyte salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Sht73J&md5=a5218aef70342dc1a7e1e4d237ff10e5CAS |
Wang L, Liu X, Liang M, Tan F, Liang W, Chen Y, Lin Y, Huang L, Xing J, Chen W (2014) Proteomic analysis of salt-responsive proteins in the leaves of mangrove Kandelia candel during short-term stress. PLoS One 9, e83141
| Proteomic analysis of salt-responsive proteins in the leaves of mangrove Kandelia candel during short-term stress.Crossref | GoogleScholarGoogle Scholar | 24416157PubMed |
Wang J, Meng Y, Li B, Ma X, Lai Y, Si E, Yang K, Xu X, Shang X, Wang H, Wang D (2015) Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant, Cell & Environment 38, 655–669.
| Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvVKjtrc%3D&md5=ba5fa3378f3f5bd65cef35900564abcbCAS |
Wei Y, Guangmin X, Daying Z, Huimin C (2001) Transfer of salt tolerance from Aeluropus littorulis sinensis to wheat (Triticum aestivum L.) via asymmetric somatic hybridization. Plant Science 161, 259–266.
| Transfer of salt tolerance from Aeluropus littorulis sinensis to wheat (Triticum aestivum L.) via asymmetric somatic hybridization.Crossref | GoogleScholarGoogle Scholar | 11448756PubMed |
Wu C, Gao X, Kong X, Zhao Y, Zhang H (2009) Molecular cloning and functional analysis of a Na+/H+ antiporter gene ThNHX1 from a halophytic plant Thellungiella halophila. Plant Molecular Biology Reporter 27, 1–12.
| Molecular cloning and functional analysis of a Na+/H+ antiporter gene ThNHX1 from a halophytic plant Thellungiella halophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVOntLjJ&md5=ede77ef067555ee3f0fa4d024eb4b396CAS |
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.
| Protein profile analysis of salt-responsive proteins in leaves and roots in two cultivars of creeping bentgrass differing in salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtV2jtbk%3D&md5=eb077c13781ba35e28c09d5f0172b292CAS | 20361191PubMed |
Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biology 12, 188
| The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVSqs78%3D&md5=cc146ce61c163b2934e53b852dcc11e1CAS | 23057782PubMed |
Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5, 235–244.
| Proteomic analysis of salt stress-responsive proteins in rice root.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtleisL8%3D&md5=eb3a2b440c9ab7c84d70f860f746afdbCAS | 15672456PubMed |
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.
| Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVyhsbc%3D&md5=55cd290f37c5410f388823a5ad7b9589CAS | 21732589PubMed |
Zhang Y, Lai J, Sun S, Li Y, Liu Y, Liang L, Chen M, Xie Q (2008) Comparison analysis of transcripts from the halophyte Thellungiella halophila. Journal of Integrative Plant Biology 50, 1327–1335.
| Comparison analysis of transcripts from the halophyte Thellungiella halophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaitbvE&md5=f97b98e443f34713459ec73f18a0fe1aCAS | 19017120PubMed |
Zhao Q, Zhang H, Wang T, Chen SX, Dai SJ (2013) Proteomics-based investigation of salt-responsive mechanisms in plant roots. Journal of Proteomics 82, 230–253.
| Proteomics-based investigation of salt-responsive mechanisms in plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslegsrk%3D&md5=fc002cb02fd582365647ae6fc1a7f085CAS | 23385356PubMed |
Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
| Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyjtLs%3D&md5=1e14ced429b923e751d9f157947218dbCAS | 11173290PubMed |
Zouari N, Ben Saad R, Legavre T, Azaza J, Sabau X, Jaoua M, Masmoudi K, Hassairi A (2007) Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene 404, 61–69.
| Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFyku7nE&md5=78a059101c56f8e339e1356bbd4d3394CAS | 17916418PubMed |