Abstract
Plant growth and productivity are affected by both biotic and abiotic stress factors. Among the abiotic stresses, salt stress is the most prevalent and deleterious environmental factor which limits crop yield globally. Combined with the increasing population and food demands, this poses a great challenge to humanity. Currently, salinity affects more than 20% of the irrigated land. This is estimated to increase drastically in the near future due to the excessive irrigation practices. These factors have necessitated the researchers to understand the salt tolerance mechanisms in plants in order to use various approaches to generate salt-tolerant crops. Due to their sessile nature, plants cannot evade the stressful environment, and therefore, some species have evolved various adaptive strategies to grow and reproduce under unfavorable environments. Salt stress imparts both osmotic and ionic stress to the plants, affecting their metabolism and ion homeostasis, thereby leading to reduced growth and productivity and death in some cases. Salt tolerance is a complex phenomenon involving changes in the biochemical, molecular, and physiological processes of the plant. These changes consisting of a readjustment in the genomic and proteomic complement of the plants are imperative in unraveling the tolerance mechanisms. Recent advances in the omics research have shed more light on a range of promising candidate genes and proteins that render salt tolerance to plants. In this chapter, we describe the general effects of salt stress, the tolerance mechanisms of plants, and how recent advances in the field of proteomics can be utilized to enhance salt tolerance of crop plants.
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Abbreviations
- 1DE:
-
One-dimensional gel electrophoresis
- 2DE:
-
Two-dimensional gel electrophoresis
- ABA:
-
Abscisic acid
- APX:
-
Ascorbate peroxidase
- bHLH:
-
Basic helix-loop-helix
- CAT:
-
Catalase
- CCOMT:
-
CoA O-methyltransferase
- CNGCs:
-
Cyclic nucleotide-gated channels
- DHAR:
-
Dehydroascorbate reductase
- DIGE:
-
Difference gel electrophoresis
- EC:
-
Electric conductivity
- GPX:
-
Glutathione peroxidase
- HKT1:
-
High-affinity potassium transporter
- ICAT:
-
Isotope-coded affinity tags
- iTRAQ:
-
Isobaric tags for relative and absolute quantitation
- JA:
-
Jasmonic acid
- LRR:
-
Leucine-rich repeat
- MAPK:
-
Mitogen-activated protein kinase
- MDAR:
-
Monodehydroascorbate reductase
- MRM:
-
Multiple reaction monitoring
- MS:
-
Mass spectrometry
- MudPIT:
-
Multidimensional protein identification technology
- NaCl:
-
Sodium chloride
- NHX:
-
Sodium/hydrogen exchanger
- NSCC:
-
Nonselective cation channels
- PIP:
-
Plasma membrane intrinsic proteins
- POD:
-
Peroxidases
- PTMs:
-
Posttranslational modifications
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
- SAM:
-
S-adenosyl methionine
- SILAC:
-
Stable isotope labeling by amino acids in cell culture
- SOD:
-
Superoxide dismutase
- SOS1:
-
Salt overly sensitive1
- SRM:
-
Selective reaction monitoring
- SUMO:
-
Small ubiquitin-like modifiers
- SWATH MS:
-
Sequential window acquisition of all theoretical mass spectra
- TIP:
-
Tonoplast intrinsic proteins
- VDAC:
-
Voltage-dependent anion channel
- VPPase:
-
Vacuolar pyrophosphatase
References
Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4(7):2072–2081. https://doi.org/10.1002/pmic.200300741
Acosta-Motos JR, Ortuno MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7(18):1–38. https://doi.org/10.3390/agronomy7010018
Aghaei K, Komatsu S (2013) Crop and medicinal plants proteomics in response to salt stress. Front Plant Sci 4:8. https://doi.org/10.3389/fpls.2013.00008
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431):1256–1258
Askari H, Edqvist J, Hajheidari M, Kafi M, Salekdeh GH (2006) Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6(8):2542–2554. https://doi.org/10.1002/pmic.200500328
Baisakh N, RamanaRao MV, Rajasekaran K, Subudhi P, Janda J, Galbraith D, Vanier C, Pereira A (2012) Enhanced salt stress tolerance of rice plants expressing a vacuolar H+ -ATPase subunit c1 (SaVHAc1) gene from the halophyte grass Spartina alterniflora Loisel. Plant Biotechnol J 10(4):453–464. https://doi.org/10.1111/j.1467-7652.2012.00678.x
Bandehagh A, Salekdeh GH, Toorchi M, Mohammadi A, Komatsu S (2011) Comparative proteomic analysis of canola leaves under salinity stress. Proteomics 11(10):1965–1975. https://doi.org/10.1002/pmic.201000564
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. Plant Cell 21(12):4044–4058. https://doi.org/10.1105/tpc.109.069211
Bayat F, Shiran B, Belyaev DV (2011) Overexpression of HvNHX2, a vacuolar Na+/H+ antiporter gene from barley, improves salt tolerance in Arabidopsis thaliana. Aust J Crop Sci 5:428–432
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099–1111. https://doi.org/10.1105/tpc.7.7.1099
Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139(2):790–805. https://doi.org/10.1104/pp.105.065029
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 Sci 172:20–28
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. Anal Bioanal Chem 391(1):381–390. https://doi.org/10.1007/s00216-008-2008-x
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(10):1293–1307. https://doi.org/10.1016/j.phytochem.2011.01.024
Cheeseman JM (1988) Mechanisms of salinity tolerance in plants. Plant Physiol 87(3):547–550
Chen S, Gollop N, Heuer B (2009) Proteomic analysis of salt-stressed tomato (Solanum lycopersicum) seedlings: effect of genotype and exogenous application of glycinebetaine. J Exp Bot 60(7):2005–2019. https://doi.org/10.1093/jxb/erp075
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. J Proteome Res 10(9):3944–3958. https://doi.org/10.1021/pr200535r
Chen T, Zhang L, Shang H, Liu S, Peng J, Gong W, Shi Y, Zhang S, Li J, Gong J, Ge Q, Liu A, Ma H, Zhao X, Yuan Y (2016) iTRAQ-based quantitative proteomic analysis of cotton roots and leaves reveals pathways associated with salt stress. PLoS One 11(2):e0148487. https://doi.org/10.1371/journal.pone.0148487
Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14(11):2723–2743
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(11):3100–3114. https://doi.org/10.1002/pmic.200800340
Cheng L, Li X, Huang X, Ma T, Liang Y, Ma X, Peng X, KJia J, Chen S, Chen Y, Deng B, Liu G (2013) Overexpression of sheep grass R1-MYB transcription factor LcMYB1 confers salt tolerance in transgenic Arabidopsis. Plant Physiol Biochem 70:252–260
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. Front Plant Sci 6:30. https://doi.org/10.3389/fpls.2015.00030
Chitteti BR, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6(5):1718–1727. https://doi.org/10.1021/pr060678z
Cosentino C, Di Silvestre D, Fischer-Schliebs E, Homann U, De Palma A, Comunian C, Mauri PL, Thiel G (2013) Proteomic analysis of Mesembryanthemum crystallinum leaf microsomal fractions finds an imbalance in V-ATPase stoichiometry during the salt-induced transition from C3 to CAM. Biochem J 450(2):407–415. https://doi.org/10.1042/BJ20121087
Dani V, Simon WJ, Duranti M, Croy RR (2005) Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 5(3):737–745. https://doi.org/10.1002/pmic.200401119
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6(24):6498–6507. https://doi.org/10.1002/pmic.200600367
Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71(13):1450–1459. https://doi.org/10.1016/j.phytochem.2010.05.020
Dunkley TP, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci 103(17):6518–6523. https://doi.org/10.1073/pnas.0506958103
El Rabey HA, Al-Malki AL, Abulnaja KO, Rohde W (2015) Proteome analysis for understanding abiotic stress (salinity and drought) tolerance in date palm (Phoenix dactylifera L.). Int J Genomics 2015:407165. https://doi.org/10.1155/2015/407165
Eldakak M, Milad SI, Nawar AI, Rohila JS (2013) Proteomics: a biotechnology tool for crop improvement. Front Plant Sci 4:35. https://doi.org/10.3389/fpls.2013.00035
Enstone JE, Perterson CA, Ma FS (2003) Root endodermis and exodermis: structure, function and response to the environment. J Plant Growth Regul 21:335–351
Evers D, Legay S, Lamoureux D, Hausman JF, Hoffmann L, Renaut J (2012) Towards a synthetic view of potato cold and salt stress response by transcriptomic and proteomic analyses. Plant Mol Biol 78(4–5):503–514. https://doi.org/10.1007/s11103-012-9879-0
Faiyue B, Al-Azzawi MJ, Flowers TJ (2010) The role of lateral roots in bypass flow in rice (Oryza sativa L.). Plant Cell Environ 33(5):702–716. https://doi.org/10.1111/j.1365-3040.2009.02078.x
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. Mol Biol Rep 39(5):6387–6397. https://doi.org/10.1007/s11033-012-1460-z
Flowers TJ (2004) Improving crop salt tolerance. J Exp Biol 55(396):307–319. https://doi.org/10.1093/jxb/erh003
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115(3):327–331
Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian. J Plant Physiol 22:875–884
Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 6(2):821–827. https://doi.org/10.1021/pr060474i
Gao L, Yan X, Li X, Guo G, Hu Y, Ma W, Yan Y (2011) Proteome analysis of wheat leaf under salt stress by two-dimensional difference gel electrophoresis (2D-DIGE). Phytochemistry 72(10):1180–1191. https://doi.org/10.1016/j.phytochem.2010.12.008
Gharat SA, Parmar S, Tambat S, Vasudevan M, Shaw BP (2016) Transcriptome analysis of the response to NaCl in Suaeda maritima provides an insight into salt tolerance mechanisms in halophytes. PLoS One 11(9):e0163485. https://doi.org/10.1371/journal.pone.0163485
Gorg A, Drews O, Luck C, Weiland F, Weiss W (2009) 2-DE with IPGs. Electrophoresis 30(Suppl 1):S122–S132. https://doi.org/10.1002/elps.200900051
Guerra D, Crosatti C, Khoshro HH, Mastrangelo AM, Mica E, Mazzucotelli E (2015) Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms. Front Plant Sci 6:57. https://doi.org/10.3389/fpls.2015.00057
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596. https://doi.org/10.1155/2014/701596
Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19(3):1720–1730
Hakeem KR, Chandan R, Rehman RU, Tahir I, Sabir M, Iqbal M (eds) (2013) Salt stress in plants: signalling, omics and adaptations enhancing plant productivity under salt stress: relevance of poly-omics. Springer, New York. https://doi.org/10.1007/978-1-4614-6108-1_3
Hasanuzzaman M, Nahar K, Fujita M, Ahmad P, Chandna R, Prasad MNV, Ozturk M (eds) (2013) Salt stress in plants: signalling, omics and adaptations Enhancing plant productivity under salt stress: relevance of poly-omics. Springer, New York. https://doi.org/10.1007/978-1-4614-6108-1_6
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499. https://doi.org/10.1146/annurev.arplant.51.1.463
Hashiguchi A, Komatsu S (2016) Impact of post-translational modifications of crop proteins under abiotic stress. Proteomes 4(4):42. https://doi.org/10.3390/proteomes4040042
He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44(6):903–916. https://doi.org/10.1111/j.1365-313X.2005.02575.x
Hu J, Rampitsch C, Bykova NV (2015) Advances in plant proteomics toward improvement of crop productivity and stress resistancex. Front Plant Sci 6:209. https://doi.org/10.3389/fpls.2015.00209
Huang Q, Wang Y, Li B, Chang J, Chen M, Li K, Yang G, He G (2015a) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol 15:268. https://doi.org/10.1186/s12870-015-0644-9
Huang Q, Yang L, Luo J, Guo L, Wang Z, Yang X, Jin W, Fang Y, Ye J, Shan B, Zhang Y (2015b) SWATH enables precise label-free quantification on proteome scale. Proteomics 15(7):1215–1223. https://doi.org/10.1002/pmic.201400270
Jain S, Srivastava S, Sarin NB, Kav NN (2006) Proteomics reveals elevated levels of PR 10 proteins in saline-tolerant peanut (Arachis hypogaea) calli. Plant Physiol Biochem 44(4):253–259. https://doi.org/10.1016/j.plaphy.2006.04.006
Ji W, Cong R, Li S, Li R, Qin Z, Li Y, Zhou X, Chen S, Li J (2016) Comparative proteomic analysis of soybean leaves and roots by iTRAQ provides insights into response mechanisms to short-term salt stress. Front Plant Sci 7:573. https://doi.org/10.3389/fpls.2016.00573
Jia H, Shao M, He Y, Guan R, Chu P, Jiang H (2015) Proteome dynamics and physiological responses to short-term salt stress in Brassica napus leaves. PLoS One 10(12):e0144808. https://doi.org/10.1371/journal.pone.0144808
Jia YL, Chen H, Zhang C, Gao LJ, Wang XC, Qiu LL, Wu JF (2016) Proteomic analysis of halotolerant proteins under high and low salt stress in Dunaliella salina using two-dimensional differential in-gel electrophoresis. Genet Mol Biol 39(2):239–247. https://doi.org/10.1590/1678-4685-GMB-2015-0108
Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25. https://doi.org/10.1186/1471-2229-6-25
Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58(13):3591–3607. https://doi.org/10.1093/jxb/erm207
Jiang Q, Li X, Niu F, Sun X, Hu Z, Zhang H (2017) iTRAQ-based quantitative proteomic analysis of wheat roots in response to salt stress. Proteomics 17:1–13. https://doi.org/10.1002/pmic.201600265
Jorrin-Novo JV, Maldonado AM, Echevarria-Zomeno S, Valledor L, Castillejo MA, Curto M, Valero J, Sghaier B, Donoso G, Redondo I (2009) Plant proteomics update (2007–2008): second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge. J Proteome 72(3):285–314
Jyothi-Prakash PA, Mohanty B, Wijaya E, Lim TM, Lin Q, Loh CS, Kumar PP (2014) Identification of salt gland-associated genes and characterization of a dehydrin from the salt secretor mangrove Avicennia officinalis. BMC Plant Biol 14:291. https://doi.org/10.1186/s12870-014-0291-6
Kim DW, Rakwal R, Agrawal GK, Jung YH, Shibato J, Jwa NS, Iwahashi Y, Iwahashi H, Kim DH, Shim Ie S, Usui K (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26(23):4521–4539. https://doi.org/10.1002/elps.200500334
Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50(2):207–218. https://doi.org/10.1111/j.1365-313X.2007.03044.x
Kim DY, Jin JY, Alejandro S, Martinoia E, Lee Y (2010) Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol Plant 139(2):170–180. https://doi.org/10.1111/j.1399-3054.2010.01353.x
Kim K, Seo E, Chang SK, Park TJ, Lee SJ (2016) Novel water filtration of saline water in the outermost layer of mangrove roots. Sci Rep 6:20426. https://doi.org/10.1038/srep20426
Kosava K, Vitamvas P, Prasil IT, TRenaut J (2011) Plant proteome changes under abiotic stress- condition of proteomics studies to understanding plant stress response. J Proteome 74:1301–1322
Kosava K, Vitamvas P, Urban MO, Prail IT (2013) Plant proteome responses to salinity stress-comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786
Kosova K, Prail IT, Vitamvas P (2013) Protein contribution to plant salinity response and tolerance acquisition. Int J Mol Sci 14(4):6757–6789. https://doi.org/10.3390/ijms14046757
Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62(12):4215–4228. https://doi.org/10.1093/jxb/err135
Krishnamurthy P, Jyothi-Prakash PA, Qin L, He J, Lin Q, Loh CS, Kumar PP (2014a) Role of root hydrophobic barriers in salt exclusion of a mangrove plant Avicennia officinalis. Plant Cell Environ 37(7):1656–1671. https://doi.org/10.1111/pce.12272
Krishnamurthy P, Tan XF, Lim TK, Lim TM, Kumar PP, Loh CS, Lin Q (2014b) Proteomic analysis of plasma membrane and tonoplast from the leaves of mangrove plant Avicennia officinalis. Proteomics 14(21–22):2545–2557. https://doi.org/10.1002/pmic.201300527
Krishnamurthy P, Mohanty B, Wijaya E, Lee DY, Lim TM, Lin Q, Xu J, Loh CS, Kumar P (2017) Transcriptomics analysis of salt stress tolerance in the roots of the mangrove Avicennia officinalis, Scientific Reports 7:10031
Lal S, Gulyani V, Khurana P (2008) Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res 17(4):651–663. https://doi.org/10.1007/s11248-007-9145-4
Lee S, Lee EJ, Yang EJ, Lee JE, Park AR, Song WH, Park OK (2004) Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell 16(6):1378–1391. https://doi.org/10.1105/tpc.021683
Li F, Guo S, Zhao Y, Chen D, Chong K, Xu Y (2010a) Overexpression of a homopeptide repeat-containing bHLH protein gene (OrbHLH001) from Dongxiang Wild Rice confers freezing and salt tolerance in transgenic Arabidopsis. Plant Cell Rep 29(9):977–986. https://doi.org/10.1007/s00299-010-0883-z
Li XJ, Yang MF, Chen H, Qu LQ, Chen F, Shen SH (2010b) Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. Biochim Biophys Acta 1804(4):929–940. https://doi.org/10.1016/j.bbapap.2010.01.004
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. J Plant Physiol 168(15):1743–1752. https://doi.org/10.1016/j.jplph.2011.03.018
Li W, Zhao F, Fang W, Xie D, Hou J, Yang X, Zhao Y, Tang Z, Nie L, Lv S (2015) Identification of early salt stress responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing iTRAQ-based proteomic technique. Front Plant Sci 6:732. https://doi.org/10.3389/fpls.2015.00732
Liu CW, Chang TS, Hsu YK, Wang AZ, Yen HC, Wu YP, Wang CS, Lai CC (2014) Comparative proteomic analysis of early salt stress responsive proteins in roots and leaves of rice. Proteomics 14(15):1759–1775. https://doi.org/10.1002/pmic.201300276
Luo J, Tang S, Peng X, Yan X, Zeng X, Li J, Li X, Wu G (2015) Elucidation of cross-talk and specificity of early response mechanisms to salt and PEG-simulated drought stresses in Brassica napus using comparative proteomic analysis. PLoS One 10(10):e0138974. https://doi.org/10.1371/journal.pone.0138974
Ma FS, Peterson CA (2003) Current insights into the development, structure and chemistry of the endodermis and exodermis of roots. Can J Bot 81:405–421
Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471(2):146–158. https://doi.org/10.1016/j.abb.2008.01.010
Manaa A, Ahmed HB, Smiti S, Faurobert M (2011) Salt-stress induced physiological and proteomic changes in tomato (Solanum lycopersicum) seedlings. OMICS 15(11):801–809. https://doi.org/10.1089/omi.2011.0045
Mastrobuoni G, Irgang S, Pietzke M, Assmus HE, Wenzel M, Schulze WX, Kempa S (2012) Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii. BMC Genomics 13:215. https://doi.org/10.1186/1471-2164-13-215
Maurel C, Chrispeels MJ (2001) Aquaporins. A molecular entry into plant water relations. Plant Physiol 125(1):135–138
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624. https://doi.org/10.1146/annurev.arplant.59.032607.092734
Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ, Very AA (2011) Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68(3):468–479. https://doi.org/10.1111/j.1365-313X.2011.04701.x
Mishra A, Tanna B (2017) Halophytes: potential resources for salt stress tolerance genes and promoters. Front Plant Sci 8:829. https://doi.org/10.3389/fpls.2017.00829
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nat NVK, Sanjeeva S, Laksiri G, Stanford FB (2004) Proteome-level changes in the roots of Pisum sativum in response to salinity. Ann Appl Biol 145:217–230
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(16):4185–4196. https://doi.org/10.1002/pmic.200401282
Palmblad M, Mills DJ, Bindschedler LV (2008) Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. J Proteome Res 7(2):780–785. https://doi.org/10.1021/pr0705340
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(5):2584–2599. https://doi.org/10.1021/pr100034f
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Parida AK, Jha B (2010) Salt tolerance mechanisms in mangroves: a review. Trees 24:199–217
Parida AK, Das AB, Mittra B, Mohanty P (2004a) Salt-stress induced alterations in protein profile and protease activity in the mangrove Bruguiera parviflora. Z Naturforsch C 59(5–6):408–414
Parida AK, Das AB, Mohanty P (2004b) Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161(5):531–542. https://doi.org/10.1078/0176-1617-01084
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. J Exp Bot 57(5):1109–1118. https://doi.org/10.1093/jxb/erj134
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(12):2676–2686. https://doi.org/10.1074/mcp.M900052-MCP200
Peterson CA (1988) Exodermal Casparian bands: their significance for ion uptake by roots. Physiol Plant 72:204–208
Popp M (1995) Salt resistance in herbaceous halophytes and mangroves. Prog Bot 56:415–429
Qiao WH, Zhao XY, Li W, Luo Y, Zhang XS (2007) Overexpression of AeNHX1, a root-specific vacuolar Na+/H+ antiporter from Agropyron elongatum, confers salt tolerance to Arabidopsis and Festuca plants. Plant Cell Rep 26(9):1663–1672. https://doi.org/10.1007/s00299-007-0354-3
Qing DJ, Lu HF, Li N, Dong HT, Dong DF, Li YZ (2009) Comparative profiles of gene expression in leaves and roots of maize seedlings under conditions of salt stress and the removal of salt stress. Plant Cell Physiol 50(4):889–903. https://doi.org/10.1093/pcp/pcp038
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4):1755–1767. https://doi.org/10.1104/pp.103.025742
Ranathunge K, Steudle E, Lafitte R (2003) Control of water uptake by rice (Oryza sativa L.): role of the outer part of the root. Planta 217(2):193–205. https://doi.org/10.1007/s00425-003-0984-9
Ranjithakumari BD, Radhakrishnan (2008) Plant proteomics. In: Nangia SB (ed) Plant with biotic and abiotic factors interaction proteomics. A. P. H. Publishing Corporation, New Delhi
Rasoulnia A, Bihamta MR, Peyghambari SA, Alizadeh H, Rahnama A (2011) Proteomic response of barley leaves to salinity. Mol Biol Rep 38(8):5055–5063. https://doi.org/10.1007/s11033-010-0651-8
Razavizadeh R, Ehsanpour AA, Ahsan N, Komatsu S (2009) Proteome analysis of tobacco leaves under salt stress. Peptides 30(9):1651–1659. https://doi.org/10.1016/j.peptides.2009.06.023
Reinhardt DH, Rost TL (1995) Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environ Exp Bot 35:563–574
Rossignol M, Peltier JB, Mock HP, Matros A, Maldonado AM, Jorrin JV (2006) Plant proteome analysis: a 2004–2006 update. Proteomics 6(20):5529–5548. https://doi.org/10.1002/pmic.200600260
Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol 11:34. https://doi.org/10.1186/1471-2229-11-34
Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2(9):1131–1145. https://doi.org/10.1002/1615-9861(200209)2:9<1131::AID-PROT1131>3.0.CO;2-1
Sanyal A, Lajoie BR, Jain G, Dekker J (2012) The long-range interaction landscape of gene promoters. Nature 489(7414):109–113. https://doi.org/10.1038/nature11279
Scholander PF (1968) How mangroves desalinate water. Physiol Plant 21:251–261
Schreiber L, Franke BR (2011) Endodermis and exodermis in roots. Wiley, Chichester
Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292
Shiio Y, Aebersold R (2006) Quantitative proteome analysis using isotope-coded affinity tags and mass spectrometry. Nat Protoc 1(1):139–145. https://doi.org/10.1038/nprot.2006.22
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 C(4) plant. J Proteome Res 9(6):2882–2897. https://doi.org/10.1021/pr900974k
Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR, Motamed N, Komatsu S (2010b) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Sci 8:19. https://doi.org/10.1186/1477-5956-8-19
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(8):1323–1337. https://doi.org/10.1016/j.jprot.2011.03.018
Swami AK, Alam SI, Sengupta N, Sarin R (2011) Differential proteomic analysis of salt stress response in Sorghum bicolor leaves. Environ Exp Bot 71:321–328
Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MP, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9:593. https://doi.org/10.1186/1471-2164-9-593
Tada Y, Kashimura T (2009) Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant Cell Physiol 50(3):439–446. https://doi.org/10.1093/pcp/pcp002
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 Physiol 135(3):1697–1709. https://doi.org/10.1104/pp.104.039909
Tan WK, Lim TK, Loh CS, Kumar P, Lin Q (2015) Proteomic characterisation of the salt gland-enriched tissues of the mangrove tree species Avicennia officinalis. PLoS One 10(7):e0133386. https://doi.org/10.1371/journal.pone.0133386
Tang X, Mu X, Shao H, Wang H, Brestic M (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Crit Rev Biotechnol 35(4):425–437. https://doi.org/10.3109/07388551.2014.889080
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. Plant J 60(5):795–804. https://doi.org/10.1111/j.1365-313X.2009.04000.x
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527
Tsuzuki M, Moskvin OV, Kuribayashi M, Sato K, Retamal S, Abo M, Zeilstra-Ryalls J, Gomelsky M (2011) Salt stress-induced changes in the transcriptome, compatible solutes, and membrane lipids in the facultatively phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 77(21):7551–7559. https://doi.org/10.1128/AEM.05463-11
Veeranagamallaiah G, Jyothsnakumari G, Thippeswamy M, Reddy PCO, 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 Sci 175:631–641
Verma D, Singla-Pareek SL, Rajagopal D, Reddy MK, Sopory SK (2007) Functional validation of a novel isoform of Na+/H+ antiporter from Pennisetum glaucum for enhancing salinity tolerance in rice. J Biosci 32(3):621–628
Vincent D, Ergul A, Bohlman MC, Tattersall EA, 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. J Exp Bot 58(7):1873–1892. https://doi.org/10.1093/jxb/erm012
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. J Plant Physiol 168(6):519–526. https://doi.org/10.1016/j.jplph.2010.08.016
Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63(5):609–623. https://doi.org/10.1007/s11103-006-9112-0
Wang H, Miyazaki S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52(4):873–891
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(7):1470–1489. https://doi.org/10.1002/pmic.200700569
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(1):167–177. https://doi.org/10.1007/s00425-008-0727-z
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(7):3331–3345. https://doi.org/10.1021/pr801083a
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(1):e83141. https://doi.org/10.1371/journal.pone.0083141
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(4):655–669. https://doi.org/10.1111/pce.12428
Wei P, Wang L, Liu A, Yu B, Lam HM (2016) GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front Plant Sci 7:1082. https://doi.org/10.3389/fpls.2016.01082
Wen G, Cai L, Liu Z, Li DK, Lou Q, Li XF, Wan J, Yang Y (2011) Arabidopsis thaliana VDAC2 involvement in salt stress response pathway. Afr J Biotechnol 10:11588–11593
Witzel K, Weidner A, Surabhi GK, Borner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 60(12):3545–3557. https://doi.org/10.1093/jxb/erp198
Wu X, Gong F, Cao D, Hu X, Wang W (2016) Advances in crop proteomics: PTMs of proteins under abiotic stress. Proteomics 16(5):847–865. https://doi.org/10.1002/pmic.201500301
Xianjun P, Xingyong M, Weihong F, Man S, Liqin C, Alam I, Lee BH, Dongmei Q, Shihua S, Gongshe L (2011) Improved drought and salt tolerance of Arabidopsis thaliana by transgenic expression of a novel DREB gene from Leymus chinensis. Plant Cell Rep 30(8):1493–1502. https://doi.org/10.1007/s00299-011-1058-2
Xiong Y, Peng X, Cheng Z, Liu W, Wang GL (2016) A comprehensive catalog of the lysine-acetylation targets in rice (Oryza sativa) based on proteomic analyses. J Proteome 138:20–29. https://doi.org/10.1016/j.jprot.2016.01.019
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(6):595–615. https://doi.org/10.1007/s00299-010-0847-3
Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5(1):235–244. https://doi.org/10.1002/pmic.200400853
Yan H, Li Q, Park SC, Wang X, Liu YJ, Zhang YG, Tang W, Kou M, Ma DF (2016) Overexpression of CuZnSOD and APX enhance salt stress tolerance in sweet potato. Plant Physiol Biochem 109:20–27. https://doi.org/10.1016/j.plaphy.2016.09.003
Yang Y, Tang RJ, Jiang CM, Li B, Kang T, Liu H, Zhao N, Ma XJ, Yang L, Chen SL, Zhang HX (2015) Overexpression of the PtSOS2 gene improves tolerance to salt stress in transgenic poplar plants. Plant Biotechnol J 13(7):962–973. https://doi.org/10.1111/pbi.12335
Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580(4):1183–1191. https://doi.org/10.1016/j.febslet.2005.12.009
Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. J Exp Bot 38:1141–1153
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(9):3852–3870. https://doi.org/10.1021/pr101102p
Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012a) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11(1):49–67. https://doi.org/10.1021/pr200861w
Zhang YM, Liu ZH, Wen ZY, Zgang HM, Yang F, Guo XL (2012b) The vacuolar Na+–H+ antiport gene TaNHX2 confers salt tolerance on transgenic alfalfa (Medicago sativa). Funct Plant Biol 39:708–716
Zhou J, Li F, Wang JL, Ma Y, Chong K, Xu YY (2009) Basic helix-loop-helix transcription factor from wild rice (OrbHLH2) improves tolerance to salt- and osmotic stress in Arabidopsis. J Plant Physiol 166(12):1296–1306. https://doi.org/10.1016/j.jplph.2009.02.007
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6(5):441–445
Zhuang J, Zhang J, Hou XL, Wang F, Xiong AS (2014) Transcriptomic, proteomic, metabolomic and functional genomic approaches for the study of abiotiuc stress in vegetable crops. Crit Rev Plant Sci 33:225–237
Zorb C, Herbst R, Forreiter C, Schubert S (2009) Short-term effects of salt exposure on the maize chloroplast protein pattern. Proteomics 9(17):4209–4220. https://doi.org/10.1002/pmic.200800791
Zorb C, Schmitt S, Muhling KH (2010) Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10(24):4441–4449. https://doi.org/10.1002/pmic.201000231
Acknowledgments
The research work in our laboratory is supported by the Singapore National Research Foundation under its Environment and Water Research Programme and administered by PUB, Singapore’s National Water Agency, Singapore, NRF-EWI-IRIS (R-706-000-010-272 and R-706-000-040-279).
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Krishnamurthy, P., Qingsong, L., Kumar, P.P. (2018). Proteomics Perspectives in Post-Genomic Era for Producing Salinity Stress-Tolerant Crops. In: Kumar, V., Wani, S., Suprasanna, P., Tran, LS. (eds) Salinity Responses and Tolerance in Plants, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-90318-7_10
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