Molecular Mechanisms of Osmotic Stress Recovery in Extremophile Plants: What Can We Learn from Proteomics?

  • Nèjia Farhat
  • Ahmed Debez


During their life cycle, plants are often exposed to phases of high salinity and dehydration stress. Extremophile plants have evolved mechanisms of stress tolerance allowing them to survive or recover from extremely adverse conditions such as water deficit stress and soil salinity. Plant adaptability environmental constraints are linked with deep modifications in proteomic profile, with relevance in abiotic tolerance. Research in extreme drought and high salinity tolerance in resurrection plants and halophytes, respectively, provided some insights into stress tolerance and stress recovery through dynamic changes in protein abundance. Identified proteins under drought and salinity conditions cover a wide range of biological functions: photosynthesis, energy metabolism, protein synthesis, protein folding and degradation and defence response. Proteins related to antioxidant metabolism and scavenging of oxygen radicals were found with higher abundance in halophytes and resurrection plants enabling them to cope with stressful conditions. Comprehensive data from recent proteomics studies confirming the relationship between stress tolerance and specific protein abundance are summarized in this paper.


Drought Salinity Halophytes Resurrection plants Recovery Proteomics 


  1. Abogadallah GM (2010) Insights into the significance of antioxidative defense under salt stress. Plant Signal Behav 5:369–374PubMedPubMedCentralCrossRefGoogle Scholar
  2. Abreu IA, Farinha AP, Negrão S, Gonçalves N, Fonseca C, Rodrigues M, Batista R, Nelson JM, Saibo M, Oliveira MM (2013) Coping with abiotic stress: proteome changes for crop improvement. J Proteome 93:145–168CrossRefGoogle Scholar
  3. Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. J Proteome Res 7:4858–4868PubMedCrossRefGoogle Scholar
  4. Alamillo JM, Bartels D (1996) Light and stage of development influence the expression of desiccation-induced genes in the resurrection plant Craterostigma plantagineum. Plant Cell Environ 19:300–310CrossRefGoogle Scholar
  5. Amzallag GN (1997) Influence of periodic fluctuation in root environment on adaptation to salinity in Sorghum bicolor. Funct Plant Biol 24:579–586CrossRefGoogle Scholar
  6. Ashraf MPJC, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  7. Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110CrossRefGoogle Scholar
  8. Askari H, Edqvist J, Hajheidari M, Kafi M, Salekdeh GH (2006) Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6:2542–2554PubMedCrossRefGoogle Scholar
  9. Athar HR, Ashraf M (2009) Strategies for crop improvement against salinity and drought stress: an overview. In: Ashraf M, Öztürk M, Athar HR (eds) Salinity and water stress: improving crop efficiency. Springer, New York, pp 1–16Google Scholar
  10. Atteya AM (2003) Alteration of water relations and yield of corn genotypes in response to drought stress. Bulg J Plant Physiol 29:63–76Google Scholar
  11. Azri W, Barhoumi Z, Chibani F, Borji M, Bessrour M, Mliki A (2016) Proteomic responses in shoots of the facultative halophyte Aeluropus littoralis (Poaceae) under NaCl salt stress. Funct Plant Biol 43:1028–1047CrossRefGoogle Scholar
  12. Baker J, Steele C, Dure L (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11:277–291PubMedCrossRefGoogle Scholar
  13. Barnabas B, Jagner K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38PubMedGoogle Scholar
  14. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta Biomembr 1465(1–2):140–151CrossRefGoogle Scholar
  15. Bogeat-Triboulot MB, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman J-F, Polle A, Kangasjärvi J, Dreyer E (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 143:876–892PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cao Y, Luo Q, Tian Y, Meng F (2017) Physiological and proteomic analyses of the drought stress response in Amygdalus Mira (Koehne) Yü et Lu roots. BMC Plant Biol 17(1)Google Scholar
  17. Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc Natl Acad Sci 104:18073–18078PubMedCrossRefGoogle Scholar
  18. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot-Lond 103:551–560CrossRefGoogle Scholar
  19. Chen D, Wang S, Cao B, Cao D, Leng G, Li H, Yin L, Shan L, Deng X (2016) Genotypic variation in growth and physiological response to drought stress and re-watering reveals the critical role of recovery in drought adaptation in maize seedlings. Front Plant Sci 6:1241PubMedPubMedCentralGoogle Scholar
  20. 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 9:3100–3114PubMedCrossRefGoogle Scholar
  21. Cheng T, Chen J, Zhang J, Shi S, Zhou Y, Lu L, Wang P, Jiang Z, Yang J, 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. Front Plant Sci 6:30PubMedPubMedCentralGoogle Scholar
  22. Chitteti BR, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6:1718–1727PubMedCrossRefGoogle Scholar
  23. Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture–not by affecting ATP synthesis. Trends Plant Sci 5:187–188CrossRefGoogle Scholar
  24. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedCrossRefGoogle Scholar
  25. de Lacerda CF, Cambraia J, Oliva MA, Ruiz HA (2005) Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery. Environ Exp Bot 54:69–76CrossRefGoogle Scholar
  26. Debez A, Braun HP, Pich A, Taamalli W, Koyro HW, Abdelly C, Huchzermeyer B (2012) Proteomic and physiological responses of the halophyte Cakile maritima to moderate salinity at the germinative and vegetative stages. J Proteome 75:5667–5694CrossRefGoogle Scholar
  27. Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603PubMedCrossRefGoogle Scholar
  28. Denison FC, Paul AL, Zupanska AK, Ferl RJ (2011) 14-3-3 proteins in plant physiology. Semin Cell Dev Biol 22:720–727PubMedCrossRefGoogle Scholar
  29. Dinakar C, Bartels D (2013) Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome, and metabolome analysis. Front Plant Sci 4:482PubMedPubMedCentralCrossRefGoogle Scholar
  30. Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71:1450–1459PubMedCrossRefGoogle Scholar
  31. Epstein E, Rains DW (1987) Advances in salt tolerance. In: Genetic aspects of plant mineral nutrition. Springer, Dordrecht, pp 113–125CrossRefGoogle Scholar
  32. 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 11:4346–4367PubMedCrossRefGoogle Scholar
  33. Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689PubMedCrossRefGoogle Scholar
  34. Fernandez-Garcia N, Hernandez M, Casado-Vela J, Bru R, Elortza F, Hedden P, Olmos E (2011) Changes to the proteome and targeted metabolites of xylem sap in Brassica oleracea in response to salt stress. Plant Cell Environ 34:821–836PubMedCrossRefGoogle Scholar
  35. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319CrossRefGoogle Scholar
  36. Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol 174:799–810PubMedCrossRefGoogle Scholar
  37. Ghosh D, Xu J (2014) Abiotic stress responses in plant roots: a proteomics perspective. Front Plant Sci 5:6PubMedPubMedCentralCrossRefGoogle Scholar
  38. Goday A, Sánchez-Martínez D, Gómez J, Puigdomènech P, Pagès M (1988) Gene expression in developing Zea mays embryos: regulation by abscisic acid of a highly phosphorylated 23-to 25-kD group of proteins. Plant Physiol 88:564–569PubMedPubMedCentralCrossRefGoogle Scholar
  39. Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5:36PubMedPubMedCentralCrossRefGoogle Scholar
  40. Grzesiak MT, Grzesiak S, Skoczowski A (2006) Changes of leaf water potential and gas exchange during and after drought in triticale and maize genotypes differing in drought tolerance. Photosynthetica 44:561–568CrossRefGoogle Scholar
  41. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014. Article ID 701596Google Scholar
  42. Himabindu Y, Chakradhar T, Reddy MC, Kanygin A, Redding KE, Chandrasekhar T (2016) Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes. Environ Exp Bot 124:39–63CrossRefGoogle Scholar
  43. Höfler K, Migsch H, Rottenburg W (1941) Über die Austrocknungresistenz landwirtschaftlicher Kulturpflanzen. Forschungsdienst 12:50–61Google Scholar
  44. Ingle R, Schmidt U, Farrant J, Thomson J, Mundree S (2007) Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa. Plant Cell Environ 30:435–446PubMedCrossRefGoogle Scholar
  45. Jiang G, Wang Z, Shang H, Yang W, Hu Z, Phillips J, Deng X (2007a) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225:1405PubMedCrossRefGoogle Scholar
  46. Jiang Y, Yang B, Harris NS, Deyholos MK (2007b) Comparative proteomic analysis of NaCl stress responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607PubMedCrossRefGoogle Scholar
  47. Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress–contribution of proteomics studies to understanding plant stress response. J Proteome 74:1301–1322CrossRefGoogle Scholar
  48. Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lafitte HR, Yongsheng G, Yan S, Li ZK (2007) Whole plant responses, key processes, and adaptation to drought stress: the case of rice. J Exp Bot 58:169–175PubMedCrossRefGoogle Scholar
  50. Li XJ, Yang MF, Chen H, Qu LQ, Chen F, Shen SH (2010) Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. Biochim Biophysi Acta (BBA)-Proteins Proteomics 1804:929–940CrossRefGoogle Scholar
  51. Malakshah SN, Rezaei MH, Heidari M, Salekdeh GH (2007) Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci Biotechnol Biochem 71:2144–2154CrossRefGoogle Scholar
  52. Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62:2797–2813PubMedCrossRefGoogle Scholar
  53. Michel D, Furini A, Salamini F, Bartels D (1994) Structure and regulation of an ABA- and desiccation-responsive gene from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 24(4):549–560PubMedCrossRefGoogle Scholar
  54. Mohammadi PP, Moieni A, Hiraga S, Komatsu S (2012) Organ-specific proteomic analysis of drought-stressed soybean seedlings. J Proteome 75:1906–1923CrossRefGoogle Scholar
  55. Moradi P, Ford-Lloyd B, Pritchard J (2018) Metabolic responses of Thymus vulgaris to water deficit stress. Curr Metabolomics 6:64–74CrossRefGoogle Scholar
  56. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  57. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  58. Ndima T, Farrant J, Thomson J, Mundree S (2001) Molecular characterization of XVT8, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baker. Plant Growth Regul 35:137–145CrossRefGoogle Scholar
  59. Oliver MJ, Jain R, Balbuena TS, Agrawal G, Gasulla F, Thelen JJ (2011) Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry 72:1273–1284PubMedCrossRefGoogle Scholar
  60. Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 9:2584–2599PubMedCrossRefGoogle Scholar
  61. Pardossi A, Malorgio F, Oriolo D, Gucci R, Serra G, Tognoni F (1998) Water relations and osmotic adjustment in Apium graveolens during long-term NaCl stress and subsequent relief. Physiol Plant 102:369–376CrossRefGoogle Scholar
  62. 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. Mol Cell Proteomics 8:2676–2686PubMedPubMedCentralCrossRefGoogle Scholar
  63. Perrone I, Pagliarani C, Lovisolo C, Chitarra W, Roman F, Schubert A (2012) Recovery from water stress affects grape leaf petiole transcriptome. Planta 235:1383–1396PubMedCrossRefGoogle Scholar
  64. Pitman MG, Lauchli A (2002) Global impact of salinity and agricultural ecosystems. In: Lauchli A, Luttge U (eds) Salinity: environmental, plants, molecules. Springer, Dordrecht, pp 3–20Google Scholar
  65. Polle A (2001) Dissecting the superoxide dismutase–ascorbate peroxidase–glutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462PubMedPubMedCentralCrossRefGoogle Scholar
  66. Qiu Y, Xi J, Du L, Poovaiah BW (2012) The function of calreticulin in plant immunity: new discoveries for an old protein. Plant Signal Behav 7:907–910PubMedPubMedCentralCrossRefGoogle Scholar
  67. Rehman S, Harris PJC, Ashraf M (2005) Stress environments and their impact on crop production. In: Ashraf M, Harris PJC (eds) Abiotic stresses: plant resistance through breeding and molecular approaches. Haworth Press, New York, pp 3–18Google Scholar
  68. Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223PubMedCrossRefGoogle Scholar
  69. Rodziewicz P, Swarcewicz B, Chmielewska K, Wojakowska A, Stobiecki M (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol Plant 36:1–19CrossRefGoogle Scholar
  70. Röhrig H, Schmidt J, Colby T, Bräutigam A, Hufnagel P, Bartels D (2006) Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation. Plant Cell Environ 29:1606–1617PubMedCrossRefGoogle Scholar
  71. Sengupta S, Majumder AL (2009) Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229:911–929PubMedCrossRefGoogle Scholar
  72. Shabala SN, Mackay AS (2011) Ion transport in halophytes. Adv Bot Res 57:151–187CrossRefGoogle Scholar
  73. Sobhanian H, Motamed N, Jazii FR, Nakamura T, Komatsu S (2010) Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant. J Proteome Res 9:2882–2897PubMedCrossRefGoogle Scholar
  74. Sobhanian H, Aghaei K, Komatsu S (2011) Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops? J Proteome 74:1323–1337CrossRefGoogle Scholar
  75. Spreitzer RJ, Salvucci ME (2002) RUBISCO: structure, regulatory interactions and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475PubMedCrossRefGoogle Scholar
  76. Tang M, Liu X, Deng H, Shen S (2011) Over-expression of JcDREB, a putative AP2/EREBP domain-containing transcription factor gene in woody biodiesel plant Jatropha curcas, enhances salt and freezing tolerance in transgenic Arabidopsis thaliana. Plant Sci 181:623–631PubMedCrossRefGoogle Scholar
  77. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132PubMedCrossRefGoogle Scholar
  78. Wang WX, Barak T, Vinocur B, Shoseyov O, Altman A (2003) Abiotic resistance and chaperones: possible physiological role of SP1, a stable and stabilizing protein from Populus. In: Plant biotechnology 2002 and beyond. Springer, Dordrecht, pp 439–443CrossRefGoogle Scholar
  79. 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. J Proteome Res 8:3331–3345PubMedCrossRefGoogle Scholar
  80. Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 9:6561–6577PubMedCrossRefGoogle Scholar
  81. 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 from plants subjected to salinity reveals the importance of chloroplastic starch and soluble sugars in halophyte salt tolerance. Mol Cell Proteomics 12:2174–2195PubMedPubMedCentralCrossRefGoogle Scholar
  82. 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 Environ 38:655–669PubMedCrossRefGoogle Scholar
  83. Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, He Y (2008a) Proteomic analysis of the response to high-salinity stress in Physcomitrella Patens. Planta 228:167–177PubMedCrossRefGoogle Scholar
  84. Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008b) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8:1470–1489PubMedCrossRefGoogle Scholar
  85. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139PubMedCrossRefGoogle Scholar
  86. 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 Rep 29:595–615PubMedCrossRefGoogle Scholar
  87. Xu GY, Rocha PSCF, Wang ML, Xu ML, Cui YC, Li LY, Zhu YX, Xia X (2011) A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta 234:47–59PubMedCrossRefGoogle Scholar
  88. Yang L, Ma C, Wang L, Chen S, Li H (2012) Salt stress induced proteome and transcriptome changes in sugar beet monosomic addition line M14. J Plant Physiol 169:839–850PubMedCrossRefGoogle Scholar
  89. Yoshimura K, Masuda A, Kuwano M, Yokota A, Akashi K (2008) Programmed proteome response for drought avoidance/tolerance in the root of a C3 xerophyte (wild watermelon) under water deficits. Plant Cell Physiol 49:226–241PubMedCrossRefGoogle Scholar
  90. 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. J Proteome Res 10:3852–3870PubMedCrossRefGoogle Scholar
  91. Zhang H, Han B, Wang T, Chen SX, Li HY (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67PubMedCrossRefGoogle Scholar
  92. Zhang Y, Fonslow BR, Shan B, Baek MC, Yates IIIJR (2013) Protein analysis by shotgun/bottom-up proteomics. Chem Rev 113:2343–2394PubMedPubMedCentralCrossRefGoogle Scholar
  93. Zhou S, Sauvé RJ, Liu Z, Reddy S, Bhatti S, Hucko SD, Fish T, Thannhauser TW (2011) Identification of salt-induced changes in leaf and root proteomes of the wild tomato, Solanum chilense. J Am Soc Hortic Sci 136:288–302CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Nèjia Farhat
    • 1
  • Ahmed Debez
    • 1
  1. 1.Laboratory of Extremophile PlantsCenter of Biotechnology of Borj Cedria, (CBBC)Hammam-LifTunisia

Personalised recommendations