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Large-scale de novo transcriptome analysis reveals specific gene expression and novel simple sequence repeats markers in salinized roots of the euhalophyte Salicornia europaea

  • Jinbiao Ma
  • Xinlong Xiao
  • Li Li
  • Albino Maggio
  • Dayong Zhang
  • Osama Abdalla Abdelshafy Mohamad
  • Michael Van Oosten
  • Gang Huang
  • Yufang Sun
  • Changyan Tian
  • Yinan Yao
Original Article
  • 105 Downloads

Abstract

Glycophytic plants suffer from severe stress and injury when roots are exposed to high salinity in the rhizosphere. In contrast, the euhalophyte Salicornia europaea grows well at 200 mM NaCl and can withstand up to 1000 mM NaCl in the root zone. Analysis of gene expression profiles and the underlying molecular mechanisms responsible for this tolerance have been largely overlooked. Using the Illumina sequencing platform and the short-reads assembly programme Trinity, we generated a total of 40 and 39 million clean reads and further 140,086 and 122,728 unigenes from the 200 mM NaCl and 0 mM NaCl treated tissues of S. europaea roots, respectively. All unigenes in this study were functionally annotated within context of the COG, GO and KEGG pathways. Unigene functional annotation analysis allowed us to identify hundreds of ion transporters related to homeostasis and osmotic adaptation as well as a variety of proteins related to cation, amino acid, lipid and sugar transport. We found significant enrichment in response to stress including the functional categories of “antioxidant activity”, “catalytic activity” and “response to stimuli”. These findings represent for a useful resource for the scientific community working on salt tolerance mechanisms. Conversely, a total of 8639 EST-SSRs from 131,594 unigenes were identified and 4539 non-redundant SSRs primers pairs were developed. These data provide a good foundation for future studies on molecular adaptation mechanisms of euhalophytes roots under saline environments and will likely facilitate the identification of critical salt tolerance traits to be transferred in economically important crops.

Keywords

Abiotic stress Illumina/Solexa sequencing Salicornia europaea root Transcriptome qRT-PCR 

Notes

Acknowledgements

This work was supported by Natural Science Foundation in China (Grant no. U1703106), Youth Innovation Promotion Association, CAS (2016381), and the Open Fund of the Shanghai Key Laboratory of Bio-Energy Crops.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11738_2018_2702_MOESM1_ESM.fa (77.1 mb)
Supplementary file S1: All-Unigene sequences of S. europaea roots (Description: Sequences with no gap and with a length longer than 200 bp were selected from the assembly results) (FA 78994 KB)
11738_2018_2702_MOESM2_ESM.xls (31.8 mb)
Supplementary file S2: Functional annotation of All-Unigenes, including GO, COG, and KEGG analyses (Description: All-Unigene sequences were searched against protein databases (Nr, Swiss-prot database, KEGG, COG, and GO) using BLASTX (E-value Nr, -5)) (XLS 32526 KB)
11738_2018_2702_MOESM3_ESM.xls (7.3 mb)
Supplementary file S3: Summary of functional annotation of identified DEGs (Description: Unigenes with an absolute value of |log2Ratio| ≥ 1 and FDR ≤ 0.001 were identified as DEGs. GO and KEGG analyses of DEGs were based on a cutoff E-value of less than or equal to 10-5) (XLS 7464 KB)
11738_2018_2702_MOESM4_ESM.xls (428 kb)
Supplementary file S4: GO categories of DEGs between salt-free and salt-treated roots of S. europaea (Description: DEGs were divided into three major categories: molecular functions, cellular components and biological processes. Gene numbers and gene ID are listed in this file) (XLS 428 KB)
11738_2018_2702_MOESM5_ESM.xlsx (62 kb)
Supplementary file S5: Summary of DEGs enriched in KEGG pathways (Description: Pathways and backbone gene numbers are given in the table. The q-values for all pathways are less than or equal to 0.05) (XLSX 61 KB)
11738_2018_2702_MOESM6_ESM.xls (21.5 mb)
Supplementary file S6: The transcriptome data comparison between shoot and root (Description: The gene length, rowreads number, RPKM value, gene annotation were given in form) (XLS 22034 KB)
11738_2018_2702_MOESM7_ESM.xlsx (202 kb)
Supplementary file S7: Summary of SSR primers (Description: The gene ID and primer pairs were given in form) (XLSX 202 KB)

References

  1. Abogadallah GM (2010) Insights into the significance of antioxidative defense under salt stress. Plant Signal Behav 5:369–374.  https://doi.org/10.4161/psb.5.4.10873 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Al-Sadi AM, Al-Masoudi RS, Al-Habsi N et al (2010) Effect of salinity on pythium damping-off of cucumber and on the tolerance of Pythium aphanidermatum. Plant Pathol 59:112–120.  https://doi.org/10.1111/j.1365-3059.2009.02176.x CrossRefGoogle Scholar
  3. Barthakur S, Babu V, Bansa KC (2001) Over-expression of osmotin induces proline accumulation and confers tolerance to osmotic stress in transgenic tobacco. J Plant Biochem Biotechnol 10:31–37.  https://doi.org/10.1007/BF03263103 CrossRefGoogle Scholar
  4. Butt A, Mousley C, Morris K et al (1998) Differential expression of a senescence-enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringae. Plant J 16:209–221.  https://doi.org/10.1046/j.1365-313x.1998.00286.x CrossRefPubMedGoogle Scholar
  5. Carter CT, Ungar IA (2004) Relationships between seed germinability of Spergularia marina (Caryophyllaceae) and the Formation of zonal communities in an inland salt marsh. Ann Bot 93:119–125.  https://doi.org/10.1093/aob/mch018 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chaparzadeh N, D’Amico ML, Khavari-Nejad R-A et al (2004) Antioxidative responses of Calendula officinalis under salinity conditions. Plant Physiol Biochem 42:695–701.  https://doi.org/10.1016/j.plaphy.2004.07.001 CrossRefPubMedGoogle Scholar
  7. Chen X, Han H, Jiang P et al (2011) Transformation of beta-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant Cell Physiol 52:909–921.  https://doi.org/10.1093/pcp/pcr043 CrossRefPubMedGoogle Scholar
  8. Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676.  https://doi.org/10.1093/bioinformatics/bti610 CrossRefPubMedGoogle Scholar
  9. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223.  https://doi.org/10.1046/j.1365-313X.1993.04020215.x CrossRefGoogle Scholar
  10. Duarte B, Caetano M, Almeida PR et al (2010) Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environ Pollut 158:1661–1668.  https://doi.org/10.1016/j.envpol.2009.12.004 CrossRefPubMedGoogle Scholar
  11. Ellouzi H, Ben Hamed K, Cela J et al (2011) Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol Plant 142:128–143.  https://doi.org/10.1111/j.1399-3054.2011.01450.x CrossRefPubMedGoogle Scholar
  12. Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67:780–784CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fan P, Nie L, Jiang P et al (2013) Transcriptome analysis of Salicornia europaea under saline conditions revealed the adaptive primary metabolic pathways as early events to facilitate salt adaptation. PLoS One 8:e80595.  https://doi.org/10.1371/journal.pone.0080595 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319.  https://doi.org/10.1093/jxb/erh003 CrossRefPubMedGoogle Scholar
  15. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963.  https://doi.org/10.1111/j.1469-8137.2008.02531.x CrossRefPubMedGoogle Scholar
  16. Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–337.  https://doi.org/10.1086/415032 CrossRefGoogle Scholar
  17. Flowers TJ, Garcia A, Koyama M, Yeo AR (1997) Breeding for salt tolerance in crop plants—the role of molecular biology. Acta Physiol Plant 19:427–433.  https://doi.org/10.1007/s11738-997-0039-0 CrossRefGoogle Scholar
  18. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612.  https://doi.org/10.1071/FP09269 CrossRefGoogle Scholar
  19. Ghassemi F, Jakeman AJ, Nix HA (1995) Salinisation of land and water resources: human causes, extent, management and case studies. CAB International, WallingfordGoogle Scholar
  20. Gierth M, Mäser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137:1105–1114.  https://doi.org/10.1104/pp.104.057216 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Glenn EP, Brown JJ, Blumwald E (1999) Salt Tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255.  https://doi.org/10.1080/07352689991309207 CrossRefGoogle Scholar
  22. Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652.  https://doi.org/10.1038/nbt.1883 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Guo Y-Q, Tian Z-Y, Qin G-Y et al (2009) Gene expression of halophyte Kosteletzkya virginica seedlings under salt stress at early stage. Genetica 137:189–199.  https://doi.org/10.1007/s10709-009-9384-9 CrossRefPubMedGoogle Scholar
  24. Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767.  https://doi.org/10.1093/jxb/ert040 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Han H, Li Y, Zhou S (2008) Overexpression of phytoene synthase gene from Salicornia europaea alters response to reactive oxygen species under salt stress in transgenic Arabidopsis. Biotechnol Lett 30:1501–1507.  https://doi.org/10.1007/s10529-008-9705-6 CrossRefPubMedGoogle Scholar
  26. Han B, Wang C, Tang Z et al (2015) Genome-wide analysis of microsatellite markers based on sequenced database in Chinese spring wheat (Triticum aestivum L.). PLoS One 10:e0141540.  https://doi.org/10.1371/journal.pone.0141540 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hester MW, Mendelssohn IA, McKee KL (2001) Species and population variation to salinity stress in Panicum hemitomon, Spartina patens, and Spartina alterniflora: morphological and physiological constraints. Environ Exp Bot 46:277–297.  https://doi.org/10.1016/S0098-8472(01)00100-9 CrossRefGoogle Scholar
  28. Howitt SM, Udvardi MK (2000) Structure, function and regulation of ammonium transporters in plants. Biochim Biophys Acta (BBA) Biomembr 1465:152–170.  https://doi.org/10.1016/S0005-2736(00)00136-X CrossRefGoogle Scholar
  29. Hsu SY, Hsu YT, Kao CH (2003) The effect of polyethylene glycol on proline accumulation in rice leaves. Biol Plant 46:73–78.  https://doi.org/10.1023/A:1022362117395 CrossRefGoogle Scholar
  30. Husaini AM, Abdin MZ (2008) Development of transgenic strawberry (Fragaria × ananassa Duch.) plants tolerant to salt stress. Plant Sci 174:446–455.  https://doi.org/10.1016/j.plantsci.2008.01.007 CrossRefGoogle Scholar
  31. Iseli C, Cv J, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. In: Proceedings of the international conference on intelligent systems for molecular biology; ISMB international conference on intelligent systems for molecular biology, pp 138–148Google Scholar
  32. Ji H, Pardo JM, Batelli G et al (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286.  https://doi.org/10.1093/mp/sst017 CrossRefPubMedGoogle Scholar
  33. Kader J-C (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627–654.  https://doi.org/10.1146/annurev.arplant.47.1.627 CrossRefPubMedGoogle Scholar
  34. Kishor PBK, Sangam S, Amrutha RN et al (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438Google Scholar
  35. Li H, Wang Y, Jiang J et al (2009) Identification of genes responsive to salt stress on Tamarix hispida roots. Gene 433:65–71.  https://doi.org/10.1016/j.gene.2008.12.007 CrossRefPubMedGoogle Scholar
  36. Li J, Pu L, Han M et al (2014a) Soil salinization research in China: advances and prospects. J Geogr Sci 24:943–960.  https://doi.org/10.1007/s11442-014-1130-2 CrossRefGoogle Scholar
  37. Li J, Sun X, Yu G et al (2014b) Generation and analysis of expressed sequence tags (ESTs) from halophyte Atriplex canescens to explore salt-responsive related genes. Int J Mol Sci 15:11172–11189.  https://doi.org/10.3390/ijms150611172 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lv S, Jiang P, Chen X et al (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol Biochem 51:47–52.  https://doi.org/10.1016/j.plaphy.2011.10.015 CrossRefPubMedGoogle Scholar
  39. Ma J, Zhang M, Xiao X et al (2013) Global transcriptome profiling of Salicornia europaea L. shoots under NaCl treatment. PLoS One 8:e65877.  https://doi.org/10.1371/journal.pone.0065877 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Maathuis FJM, Sanders D (1996) Mechanisms of potassium absorption by higher plant roots. Physiol Plant 96:158–168.  https://doi.org/10.1111/j.1399-3054.1996.tb00197.x CrossRefGoogle Scholar
  41. Maathuis FJM, Sanders D (1997) Regulation of K+ absorption in plant root cells by external K+: interplay of different plasma membrane K+ transporters. J Exp Bot 48:451–458CrossRefPubMedGoogle Scholar
  42. Manousaki E, Kalogerakis N (2009) Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16:844–854.  https://doi.org/10.1007/s11356-009-0224-3 CrossRefGoogle Scholar
  43. Martínez-Atienza J, Jiang X, Garciadeblas B et al (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012.  https://doi.org/10.1104/pp.106.092635 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Momonoki YS, Oguri S, Kato S, Kamimura H (1996) Studies on the mechanism of salt tolerance in Salicornia europaea L.: III. Salt accumulation and ACh function. Jpn J Crop Sci 65:693–699.  https://doi.org/10.1626/jcs.65.693 CrossRefGoogle Scholar
  45. Mortazavi A, Williams BA, McCue K et al (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Meth 5:621–628.  https://doi.org/10.1038/nmeth.1226 CrossRefGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. Oh D-H, Leidi E, Zhang Q et al (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222.  https://doi.org/10.1104/pp.109.137802 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Olías R, Eljakaoui Z, Li J et al (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916.  https://doi.org/10.1111/j.1365-3040.2009.01971.x CrossRefPubMedGoogle Scholar
  49. Öztürk L, Demir Y (2002) In vivo and in vitro protective role of proline. Plant Growth Regul 38:259–264.  https://doi.org/10.1023/A:1021579713832 CrossRefGoogle Scholar
  50. Panta S, Flowers T, Lane P et al (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83.  https://doi.org/10.1016/j.envexpbot.2014.05.006 CrossRefGoogle Scholar
  51. Parida AK, Jha B (2010) Antioxidative defense potential to salinity in the euhalophyte Salicornia brachiata. J Plant Growth Regul 29:137–148.  https://doi.org/10.1007/s00344-009-9129-0 CrossRefGoogle Scholar
  52. Parkhi V, Kumar V, Sunilkumar G et al (2009) Expression of apoplastically secreted tobacco osmotin in cotton confers drought tolerance. Mol Breed 23:625–639.  https://doi.org/10.1007/s11032-009-9261-3 CrossRefGoogle Scholar
  53. Pasapula V, Shen G, Kuppu S et al (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9:88–99.  https://doi.org/10.1111/j.1467-7652.2010.00535.x CrossRefPubMedGoogle Scholar
  54. Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160.  https://doi.org/10.1093/jxb/erj068 CrossRefPubMedGoogle Scholar
  55. Rubio F, Santa-María GE, Rodríguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109:34–43.  https://doi.org/10.1034/j.1399-3054.2000.100106.x CrossRefGoogle Scholar
  56. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421Google Scholar
  57. Shabala S, Shabala L, Volkenburgh EV (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Funct Plant Biol 30:507–514.  https://doi.org/10.1071/fp03016 CrossRefGoogle Scholar
  58. Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. PNAS 97:6896–6901.  https://doi.org/10.1073/pnas.120170197 CrossRefPubMedGoogle Scholar
  59. Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477.  https://doi.org/10.1105/tpc.010371 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Singh NK, Handa AK, Hasegawa PM, Bressan RA (1985) Proteins associated with adaptation of cultured tobacco cells to NaCl. Plant Physiol 79:126–137.  https://doi.org/10.1104/pp.79.1.126 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Singh NK, Bracker CA, Hasegawa PM et al (1987) Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol 85:529–536.  https://doi.org/10.1104/pp.85.2.529 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Stewart GR, Lee JA (1974) The role of proline accumulation in halophytes. Planta 120:279–289.  https://doi.org/10.1007/BF00390296 CrossRefPubMedGoogle Scholar
  63. Subramanyam K, Arun M, Mariashibu TS et al (2012) Overexpression of tobacco osmotin (Tbosm) in soybean conferred resistance to salinity stress and fungal infections. Planta 236:1909–1925.  https://doi.org/10.1007/s00425-012-1733-8 CrossRefPubMedGoogle Scholar
  64. Szabolcs I (1994) Soil and salinization. In: Pessarakli M (ed) Handbook of plant and crop stress, vol 19. Marcell Decker Inc., New York, pp 768–770Google Scholar
  65. Tang R-J, Liu H, Bao Y et al (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74:367–380.  https://doi.org/10.1007/s11103-010-9680-x CrossRefPubMedGoogle Scholar
  66. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527.  https://doi.org/10.1093/aob/mcg058 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ungar IA (1996) Effect of salinity on seed germination, growth, and ion accumulation of Atriplex patula (Chenopodiaceae). Am J Bot 83:604–607.  https://doi.org/10.2307/2445919 CrossRefGoogle Scholar
  68. Van Oosten MJ, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146.  https://doi.org/10.1016/j.envexpbot.2014.11.010 CrossRefGoogle Scholar
  69. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655.  https://doi.org/10.1016/S0168-9452(03)00022-0 CrossRefGoogle Scholar
  70. Wang X, Fan P, Song H et al (2009) Comparative proteomic analysis of differentially expressed proteins in shoots of Salicornia europaea under different salinity. J Proteome Res 8:3331–3345.  https://doi.org/10.1021/pr801083a CrossRefPubMedGoogle Scholar
  71. Wang F, Zang X, Kabir MR et al (2014) A wheat lipid transfer protein 3 could enhance the basal thermotolerance and oxidative stress resistance of Arabidopsis. Gene 550:18–26.  https://doi.org/10.1016/j.gene.2014.08.007 CrossRefPubMedGoogle Scholar
  72. Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469.  https://doi.org/10.1023/A:1005934428906 CrossRefPubMedGoogle Scholar
  73. Wu S, Su Q, An LJ (2010) Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes. Indian J Biochem Biophys 47:298–305PubMedGoogle Scholar
  74. Yamanaka T, Miyama M, Tada Y. Bioscience (2009) Transcriptome profiling of the mangrove plant Bruguiera gymnorhiza and identification of salt tolerance genes by agrobacterium functional screening. Biotechnol Biochem 73:304–310.  https://doi.org/10.1271/bbb.80513 CrossRefGoogle Scholar
  75. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512.  https://doi.org/10.1016/j.tplants.2003.09.004 CrossRefPubMedGoogle Scholar
  76. Yang X, Ji J, Wang G et al (2011) Over-expressing Salicornia europaea (SeNHX1) gene in tobacco improves tolerance to salt. Afr J Biotechnol 10:16452–16460Google Scholar
  77. Yoshida S, Ito M, Nishida I, Watanabe A (2001) Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana. Plant Cell Physiol 42:170–178.  https://doi.org/10.1093/pcp/pce021 CrossRefPubMedGoogle Scholar
  78. Zhang Y, Lai J, Sun S et al (2008) Comparison analysis of transcripts from the halophyte Thellungiella halophila. J Integr Plant Biol 50:1327–1335.  https://doi.org/10.1111/j.1744-7909.2008.00740.x CrossRefPubMedGoogle Scholar
  79. Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71.  https://doi.org/10.1016/S1360-1385(00)01838-0 CrossRefPubMedGoogle Scholar
  80. Zou H-W, Tian X-H, Ma G-H, Li Z-X (2013) Isolation and functional analysis of ZmLTP3, a homologue to Arabidopsis LTP3. Int J Mol Sci 14:5025–5035.  https://doi.org/10.3390/ijms14035025 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  • Jinbiao Ma
    • 1
    • 3
  • Xinlong Xiao
    • 1
    • 2
  • Li Li
    • 1
  • Albino Maggio
    • 4
  • Dayong Zhang
    • 5
  • Osama Abdalla Abdelshafy Mohamad
    • 1
    • 6
  • Michael Van Oosten
    • 4
  • Gang Huang
    • 1
  • Yufang Sun
    • 1
    • 2
  • Changyan Tian
    • 1
  • Yinan Yao
    • 1
  1. 1.Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and GeographyChinese Academy of ScienceÜrümqiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Shanghai Key Laboratory of Bio-Energy CropsShanghaiChina
  4. 4.Department of Agricultural SciencesUniversity of Naples Federico IIPorticiItaly
  5. 5.Provincial Key Laboratory of Agrobiology, Institute of Agro-biotechnologyJiangsu Academy of Agricultural SciencesNanjingChina
  6. 6.Institute for Post Graduate Environmental Studies, Environmental Science DepartmentArish UniversityNorth SinaiEgypt

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