Advertisement

Plant Molecular Biology

, Volume 97, Issue 1–2, pp 1–21 | Cite as

Proteomic and physiological analyses reveal the role of exogenous spermidine on cucumber roots in response to Ca(NO3)2 stress

  • Jing Du
  • Shirong Guo
  • Jin Sun
  • Sheng Shu
Article

Abstract

Key message

The mechanism of exogenous Spd-induced Ca(NO3)2 stress tolerance in cucumber was studied by proteomics and physiological analyses. Protein–protein interaction network revealed 13 key proteins involved in Spd-induced Ca(NO3)2 stress resistance.

Abstract

Ca(NO3)2 stress is one of the major reasons for secondary salinization that limits cucumber plant development in greenhouse. The conferred protective role of exogenous Spd on cucumber in response to Ca(NO3)2 stress cues involves changes at the cellular and physiological levels. To investigate the molecular foundation of exogenous Spd in Ca(NO3)2 stress tolerance, a proteomic approach was performed in our work. After a 9 days period of Ca(NO3)2 stress and/or exogenous Spd, 71 differential protein spots were confidently identified. The resulting proteins were enriched in seven different categories of biological processes, including protein metabolism, carbohydrate and energy metabolism, ROS homeostasis and stress defense, cell wall related, transcription, others and unknown. Protein metabolism (31.2%), carbohydrate and energy metabolism (15.6%), ROS homeostasis and stress defense (32.5%) were the three largest functional categories in cucumber root and most of them were significantly increased by exogenous Spd. The Spd-responsive protein interaction network revealed 13 key proteins, whose accumulation changes could be critical for Spd-induced resistance; all 13 proteins were upregulated by Spd at transcriptional and protein levels in response to Ca(NO3)2 stress. Furthermore, accumulation of antioxidant enzymes, non-enzymatic antioxidant and polyamines, along with reduction of H2O2 and MDA, were detected after exogenous Spd application during Ca(NO3)2 stress. The results of these proteomic and physiological analyses in cucumber root may facilitate a better understanding of the underlying mechanism of Ca(NO3)2 stress tolerance mediated by exogenous Spd.

Keywords

Spd 2-DE Proteomic Physiology Ca(NO3)2 stress Cucumber root 

Abbreviations

2-DE

Two-dimensional electrophoresis

AKR4C9

Aldo-keto reductase family 4 member C9-like

APX

Ascorbate peroxidase

AsA

Ascorbate

AXS

UDP-d-apiose/UDP-d-xylose synthase

CyP

Cysteine proteinase RD21a

DapF

Diaminopimelate epimerase

EIF

Eukaryotic translation initiation factor 3 subunit protein

HSP70

Heat shock 70 kDa protein

LC–MS/MS

Liquid chromatography coupled to tandem mass spectrometry

MDA

Malondialdehyde

MDHAR

Monodehydroascorbate reductase

MG

Methylglyoxal

PAs

Polyamines

PDI

Protein disulfide-isomerase-like

POD

Peroxidase

Prx2F

Peroxiredoxin-2F

Put

Putrescine

RNAP II

RNA polymerase II transcription subunit 37e-like proteins

SAH

S-adenosyl-l-homo-cys

SAM

S-adenosyl-l-met

Spd

Spermidine

Spm

Spermine

TCA

Tricarboxylic acid cycle

TCTP

Translationally-controlled tumor protein homolog

Trx

Thioredoxin

XLA

Beta-xylosidase/alpha-l-arabinofuranosidase 2-like

CCoAMT1

Caffeoyl-CoA O-methyltransferase 1

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 31471869, 31272209 and 31401919), the National Key Technology R&D Program (2013BAD20B05), the Jiangsu Province Scientific and Technological Achievements into Special Fund (BA2014147), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author contributions

JD and SG designed the research and wrote the paper. SS and JS analyzed data and helped to draft the manuscript. All authors have read and approved the final manuscript.

Supplementary material

11103_2018_721_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 KB)

References

  1. Ahn JW, Verma R, Kim M, Lee JY, Kim YK, Bang JW, Reiter WD, Pai HS (2006) Depletion of UDP-d-apiose/UDP-d-xylose synthases results in rhamnogalacturonan-II deficiency, cell wall thickening, and cell death in higher plants. J Biol Chem 281(19):13708–13716CrossRefPubMedGoogle Scholar
  2. Alam I, Sharmin SA, Kim KH, Yang JK, Choi MS, Lee B (2010) Proteome analysis of soybean roots subjected to short-term drought stress. Plant Soil 333:491–505CrossRefGoogle Scholar
  3. An Y, Zhou H, Zhong M, Sun J, Shu S, Shao Q, Guo S (2016) Root proteomics reveals cucumber 24-epibrassinolide responses under Ca(NO3)2 stress. Plant Cell Rep 35(5):1081–1101CrossRefPubMedGoogle Scholar
  4. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  5. Badowiec A, Weidner S (2014) Proteomic changes in the roots of germinating Phaseolus vulgaris seeds in response to chilling stress and post-stress recovery. J Plant Physiol 171:389–398CrossRefPubMedGoogle Scholar
  6. Ben-Zvi AP, Goloubinoff P (2001) Mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 135:84–93CrossRefPubMedGoogle Scholar
  7. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546CrossRefPubMedGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  9. Bykova NV, Rampitsch C (2013) Modulating protein function through reversible oxidation: redox-mediated processes in plants revealed through proteomics. Proteomics 13:579–596CrossRefPubMedGoogle Scholar
  10. Cao X, Feng J, Wang D, Sun J, Lu X, Liu H (2012) Primary style protein expression in the self-incompatible/compatible apricot by the 2D-DIGE technique. Gene 503(1):110–117CrossRefPubMedGoogle Scholar
  11. Costa H, Gallego SM, Tomaro ML (2002) Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Sci 162:939–945CrossRefGoogle Scholar
  12. Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603CrossRefPubMedGoogle Scholar
  13. Díaz-Mendoza M, Velasco-Arroyo B, González-Melendi P, Martínez M, Díaz I (2014) C1A cysteine protease-cystatin interactions in leaf senescence. J Exp Bot 65(14):3825–3833CrossRefPubMedGoogle Scholar
  14. Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57(8):1697–1709CrossRefPubMedGoogle Scholar
  15. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3(3):3004–3011CrossRefGoogle Scholar
  16. Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71:1450–1459CrossRefPubMedGoogle Scholar
  17. Duan JJ, Li J, Guo SR, Kang YY (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635CrossRefPubMedGoogle Scholar
  18. Duncan R, Hershey JWB (1984) Evaluation of isoelectric focusing running conditions during two-dimensional isoelectric focusing/sodium dodecyl sulfate polyacrylamide gel electrophoresis: variation of gel patterns with changing conditions and optimized isoelectric focusing conditions. Anal Biochem 138:144–155CrossRefPubMedGoogle Scholar
  19. Fuda NJ, Ardehali MB, Lis JT (2009) Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461(7261):186–192CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gagyi C, Bucurenci N, Sîrbu O, Labesse G, Ionescu M, Ofiteru A, Assairi L, Landais S, Danchin A, Bârzu O, Gilles AM (2003) UMP kinase from the Gram-positive bacterium Bacillus subtilis is strongly dependent on GTP for optimal activity. Eur J Biochem 270(15):3196–3204CrossRefPubMedGoogle Scholar
  21. Grandori R, Carey J (1994) Six new candidate members of the α/β twisted open-sheet family detected by sequence similarity to flavodoxin. Protein Sci 3(12):2185–2193CrossRefPubMedPubMedCentralGoogle Scholar
  22. Grisebach HANS. (1980) Branched-chain sugars: occurrence and biosynthesis. In: The biochemistry of plants: a comprehensive treatise (USA), Academic Press, New YorkGoogle Scholar
  23. Gupta M, Yoshioka H, Ohnishi K, Mizumoto H, Hikichi Y, Kiba A (2013) A translationally controlled tumor protein negatively regulates the hypersensitive response in Nicotiana benthamiana. Plant Cell Physiol 54(8):1403–1414CrossRefPubMedGoogle Scholar
  24. Hao JH, Dong CJ, Zhang ZG, Wang XL, Shang QM (2012) Insights into salicylic acid responses in cucumber (Cucumis sativus L.) cotyledons based on a comparative proteomic analysis. Plant Sci 187:69–82CrossRefPubMedGoogle Scholar
  25. Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427(7):1537–1548CrossRefPubMedPubMedCentralGoogle Scholar
  26. He FF, Chen Q, Jiang RF, Chen XP, Zhang FS (2007) Yield and nitrogen balance of greenhouse tomato (Lycopersium esculentum Mill.) with conventional and site-specific nitrogen management in northern china. Nutr Cycl Agroecosyst 77:1–14CrossRefGoogle Scholar
  27. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198CrossRefPubMedGoogle Scholar
  28. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468CrossRefPubMedGoogle Scholar
  29. Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25(3):385–395Google Scholar
  30. Hudson AO, Singh BK, Leustek T, Gilvarg C (2006) An LL-diaminopimelate aminotransferase defines a novel variant of the lysine biosynthesis pathway in plants. Plant Physiol 140(1):292–301CrossRefPubMedPubMedCentralGoogle Scholar
  31. Huerta-Ocampo JA, Barrera-Pacheco A, Mendoza-Hernández CS, Espitia-Rangel E, Mock HP, Barba de la Rosa AP (2014) Salt stress-induced alterations in the root proteome of Amaranthus cruentus L. J Proteome Res 13(8):3607–3627CrossRefPubMedGoogle Scholar
  32. Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81(3):802–806CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jia XY, He LH, Jing RL, Li RZ (2009) Calreticulin: conserved protein and diverse functions in plants. Physiol Plantarum 136(2):127–138CrossRefGoogle Scholar
  34. Jiang J, Clouse SD (2001) Expression of a plant gene with sequence similarity to animal TGF-beta receptor interacting protein is regulated by brassinosteroids and required for normal plant development. Plant J 26:35–45CrossRefPubMedGoogle Scholar
  35. Jiang YQ, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607CrossRefPubMedGoogle Scholar
  36. Jin CY, Sun J, Guo SR (2010) Effects of exogenous spermidine on growth and active oxygen metabolism in cucumber seedlings under Ca(NO3)2 stress. Acta Bot Boreal 30(8):1627–1633Google Scholar
  37. Jung T, Höhn A, Grune T (2014) The proteasome and the degradation of oxidized proteins: part III-redox regulation of the proteasomal system. Redox Biol 2(0):388–394CrossRefGoogle Scholar
  38. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722CrossRefPubMedGoogle Scholar
  39. Kitamura Y, Yano T, Honna T, Yamamoto S, Inosako K (2006) Causes of farmland salinization and remedial measures in the Aral Sea basin-research on water management to prevent secondary salinization in rice-based cropping system in arid land. Agr Water Manage 85:1–14CrossRefGoogle Scholar
  40. Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’orange ovular callus lines. Plant Cell Physiol 18(2):463–467CrossRefGoogle Scholar
  41. Konishi T, Ohmiya Y, Hayashi T (2004) Evidence that sucrose loaded into the phloem of a poplar leaf is used directly by sucrose synthase associated with various β-glucan synthases in the stem. Plant Physiol 134:1146–1152CrossRefPubMedPubMedCentralGoogle Scholar
  42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  43. Lee H, Guo Y, Ohta M, Xiong LM, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lenman M, Sörensson C, Andreasson E (2008) Enrichment of phosphoproteins and phosphopeptide derivatization identify universal stress proteins in elicitor-treated Arabidopsis. Mol Plant-Microbe Interact 21(10):1275–1284CrossRefPubMedGoogle Scholar
  45. Li DP, Wu ZJ, Liang CH, Chen LJ (2004) Characteristics and regulation of greenhouse soil environment. Chin J Ecol 23:192–197Google Scholar
  46. Li JL, Sulaiman M, Beckett RP, Minibayeva FV (2010) Cell wall peroxidases in the liverwort Dumortiera hirsuta are responsible for extracellular superoxide production, and can display tyrosinase activity. Physiol Plant 138(4):474–484CrossRefPubMedGoogle Scholar
  47. Li B, He L, Guo S, Li J, Yang Y, Yan B, Sun J, Li J (2013) Proteomics reveal cucumber Spd-responses under normal condition and salt stress. Plant Physiol Biochem 67:7–14CrossRefPubMedGoogle Scholar
  48. Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667CrossRefPubMedGoogle Scholar
  49. Liu Z, Zhu Z, Qian YR, Yu JQ (2001) Effect of iso-osmotic Ca(NO3)2 and NaCl on growth of tomato seedlings. Acta Horticulturae Sinica 28(1):31–35 (in Chinese).Google Scholar
  50. Liu SG, Zhu DZ, Chen GH, Gao XQ, Zhang XS (2012) Disrupted actin dynamics trigger an increment in the reactive oxygen species levels in the Arabidopsis root under salt stress. Plant Cell Rep 31:1219–1226CrossRefPubMedGoogle Scholar
  51. Manaa A, Ahmed HB, 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(8):2797–2813CrossRefPubMedGoogle Scholar
  52. Miernyk JA, Thelen J (2008) Biochemical approaches for discovering protein–protein interactions. Plant J 53:597–609CrossRefPubMedGoogle Scholar
  53. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2009) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467CrossRefPubMedGoogle Scholar
  54. Muller C, Bandemer J, Vindis C, Camaré C, Mucher E, Guéraud F, Larroque-Cardoso P, Bernis C, Auge N, Salvayre R, Negre-Salvayre A (2013) Protein disulfide isomerase modification and inhibition contribute to ER stress and apoptosis induced by oxidized low density lipoproteins. Antioxid Redox Sign 18(7):731–742CrossRefGoogle Scholar
  55. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880Google Scholar
  56. Ndimba BK, Chivasa S, Simon WJ, Slabas AR (2005) Identification of Arabidopsis salt and osmotic stress responsive proteins using two dimensional difference gel electrophoresis and mass spectrometry. Proteomics 5:4185–4196CrossRefPubMedGoogle Scholar
  57. Nogueira SB, Labate CA, Gozzo FC, Pilau EJ, Lajolo FM, Oliveira do Nascimento JR (2012) Proteomic analysis of papaya fruit ripening using 2DE-DIGE. J Proteomics 75(4):1428–1439CrossRefPubMedGoogle Scholar
  58. Nöll G, Kozma E, Grandori R, Carey J, Schödl T, Hauska G, Daub J (2006) Spectroelectrochemical investigation of a flavoprotein with a flavin-modified gold electrode. Langmuir 22(5):2378–2383CrossRefPubMedGoogle Scholar
  59. Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139(2):487–492CrossRefPubMedGoogle Scholar
  60. Pillai B, Moorthie VA, van Belkum MJ, Marcus SL, Cherney MM, Diaper CM, Vederas JC, James MN (2009) Crystal structure of diaminopimelate epimerase from Arabidopsis thaliana, an amino acid racemase critical for l-lysine biosynthesis. J Mol Biol 385(2):580–594CrossRefPubMedGoogle Scholar
  61. Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Front Environ Sci 3:21CrossRefGoogle Scholar
  62. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50CrossRefPubMedGoogle Scholar
  63. Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol 56(2):114–121CrossRefPubMedGoogle Scholar
  64. Shi H, Ye T, Chan Z (2013) Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the bermudagrass (Cynodon dactylon) response to salt and drought stresses. J Proteome Res 12:4951–4964CrossRefPubMedGoogle Scholar
  65. Simpson PJ, Tantitadapitak C, Reed AM, Mather OC, Bunce CM, White SA, Ride JP (2009) Characterization of two novel aldo-keto reductases from Arabidopsis: expression patterns, broad substrate specificity, and an open active-site structure suggest a role in toxicant metabolism following stress. J Biol Chem 392(2):465–480Google Scholar
  66. Sugino Y, Teraoka H, Shimono H (1996) Metabolism of deoxyribonucleotides I. Purification and properties of deoxycytidine monophosphokinase of calf thymus. J Biol Chem 241:961–969Google Scholar
  67. Sun YD, Luo WR, Li XZ, Qi AG (2009) Effects of Ca(NO3)2 stress on the growth and physiological indexes of cucumber seedlings. Environ Sci Info Appl Technol 1:268–271Google Scholar
  68. Sun L, Ren H, Liu R, Li B, Wu T, Sun F, Liu H, Wang X, Dong H (2010) An h-type thioredoxin functions in tobacco defense responses to two species of viruses and an abiotic oxidative stress. Mol Plant Microbe Interact 3(11):1470–1485CrossRefGoogle Scholar
  69. Sung D, Vierling E, Guy C (2001) Comprehensive expression profile analysis of the Arabidopsis hsp70 gene family. Plant Physiol 126:789–800CrossRefPubMedPubMedCentralGoogle Scholar
  70. Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6CrossRefPubMedGoogle Scholar
  71. Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino acids 42(2–3):411–426CrossRefPubMedGoogle Scholar
  72. Tian X, Liu Y, Huang Z, Duan H, Tong J, He X, Gu W, Ma H, Xiao L (2015) Comparative proteomic analysis of seedling leaves of cold-tolerant and-sensitive spring soybean cultivars. Mol Biol Rep 42:581–601CrossRefPubMedGoogle Scholar
  73. Todorova D, Katerova Z, Sergiev I, Alexieva V (2013) Role of polyamines in alleviating salt stress. In: Ecophysiology and responses of plants under salt stress. Springer, New York, pp 355–379CrossRefGoogle Scholar
  74. Tuteja N (2007) Chapter twenty-four-mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438CrossRefPubMedGoogle Scholar
  75. Vítámvás P, Prášil IT, Kosova 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(1):68–85CrossRefPubMedGoogle Scholar
  76. Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefPubMedGoogle Scholar
  77. Wang C, Zhang L, Yuan M, Ge Y, Liu Y, Fan J, Ruan Y, Gui Z, Tong S, Zhang S (2010) The microfilament cytoskeleton plays a vital role in salt and osmotic stress tolerance in Arabidopsis. Plant Biology 12(1):70–78CrossRefPubMedGoogle Scholar
  78. Wang XC, Wang DY, Wang D, Wang HY, Chang LL, Yi XP, Peng M, Guo AP (2012) Systematic comparison of technical details in CBB methods and development of a sensitive GAP stain for comparative proteomic analysis. Electrophoresis 33:296–306CrossRefPubMedGoogle Scholar
  79. Weretilnyk EA, Alexander KJ, Drebenstedt M, Snider JD, Summers PS, Moffatt BA (2001) Maintaining methylation activities during salt stress. The involvement of adenosine kinase. Plant Physiol 125(2):856–865CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603CrossRefPubMedGoogle Scholar
  81. Xiong JS, Balland-Vanney M, Xie ZP, Schultze M, Kondorosi A, Kondorosi E, Staehelin C (2007) Molecular cloning of a bifunctional β-xylosidase/α-l-arabinosidase from alfalfa roots: heterologous expression in Medicago truncatula and substrate specificity of the purified enzyme. J Exp Bot 58(11):2799–2810CrossRefPubMedGoogle Scholar
  82. Xu TR, Lu RF, Romano D, Pitt A, Houslay MD, Milligan G, Kolch W (2012) Eukaryotic translation initiation factor 3, subunit a, regulates the extracellular signal-regulated kinase pathway. Mol Cell Biol 32(1):88–95CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244CrossRefPubMedGoogle Scholar
  84. Yang L, Zhang Y, Zhu N, Koh J, Ma C, Pan Y, Yu B, Chen S, Li H (2013a) Proteomic analysis of salt tolerance in sugar beet monosomic addition line M14. J Proteome Res 12(11):4931–4950CrossRefPubMedGoogle Scholar
  85. Yang ZB, Eticha D, Führs H, Heintz D, Ayoub D, Dorsselaer AV, Schlingmann B, Rao IM, Braun HP, Horst WJ (2013b) Proteomic and phosphoproteomic analysis of polyethylene glycol-induced osmotic stress in root tips of common bean (Phaseolus vulgaris L.). J Exp Bot 64(18): 5569–5586CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yu HY, Li TX, Zhou JM (2005) Secondary salinization of greenhouse soil and its effects on soil properties. Soils 37:581–586Google Scholar
  87. Yuan L, Yuan Y, Du J, Sun J, Guo S (2012) Effects of 24-epibrassinolide on nitrogen metabolism in cucumber seedlings under Ca(NO3)2 stress. Plant Physiol Biochem 61:29–35CrossRefPubMedGoogle Scholar
  88. Zhao Y, Du H, Wang Z, Huang B (2011) Identification of proteins associated with water-deficit tolerance in C4 perennial grass species, Cynodon dactylon × Cynodon transvaalensis and Cynodon dactylon. Physiol Plant 141:40–55CrossRefPubMedGoogle Scholar
  89. Zhao Q, Zhang H, Wang T, Chen S, Dai S (2013) Proteomics-based investigation of salt-responsive mechanisms in plant roots. J Proteom 82:230–253CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of HorticultureNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Taizhou Research InstituteJiangsu Academy Agricultural SciencesTaizhouPeople’s Republic of China

Personalised recommendations