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Plant and Soil

, Volume 400, Issue 1–2, pp 147–164 | Cite as

Temporal and spatial distributions of sodium and polyamines regulated by brassinosteroids in enhancing tomato salt resistance

  • Qingsong Zheng
  • Jinlong Liu
  • Ran Liu
  • Hao Wu
  • Chaoqiang Jiang
  • Changhai WangEmail author
  • Yongxiang GuanEmail author
Regular Article

Abstract

Aims

This study examined brassinosteroids-induced enhancement of plant salt resistance of tomato.

Methods

Pot experiment was conducted in the whole-life-cycle of cherry tomato. The effects of 24-epibrassinolide (EBL) foliar spraying on temporal and spatial distributions of ions and PAs in the whole-life-cycle of salt-stressed plants were studied.

Results

EBL could well relieve salt-induced inhibitory effects on plant growth and development in different levels, especially in the late period of tomato. EBL inhibited Na+ upward transport in salt-stressed tomato, especially in their flowers and apiculus. Salt stress decreased PAs concentration in tomato: Put > Spd > Spm, however, Spm was also the most obvious one of PAs elevated by EBL in nutritoriums of salt-stressed tomato. Also, EBL-induced an obvious increase of PAs, mainly in young leaves. EBL increased fruit-PAs concentration in mid-anaphase, and promoted the (Spd + Spm)/Put ratio in premetaphase of fruit period, improving their salt resistance.

Conclusions

EBL alleviates salt stress on tomato through regulations of Na+-root-to-shoot translocation and PAs concentrations in the whole-life-cycle, which especially showed in young vegetative organs or fruit organs, improving its salt resistance. Also, the PAs increase caused by EBL is also likely to be related to the decline of Na+ and little change of K+ in the shoots of salt-stressed tomato that were sprayed with EBL.

Keywords

Cherry tomato (Solanum lycopersicum var. cerasiforme) 24-epibrassinolide Sodium Polyamines Whole life cycle Salt resistance 

Abbreviations

BRs

Brassinosteroids

BL

Brassinolide

EBL

24-epibrassinolide

HBL

28-homobrassinolide

PAs

Polyamines

Put

Putrescine

Spd

Spermidine

Spm

Spermine

U-leaf

The third leaf near the top

M-leaf

The leaf right in the middle

L-leaf

The third leaf near the base

Notes

Acknowledgments

The authors gratefully thank for the support provided by “Jiangsu independent innovation program of agricultural science and technology [CX(15)1044-06]” and “The new project of agriculture of Jiangsu Province (SXGC[2015]291)”.

References

  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249CrossRefPubMedGoogle Scholar
  2. Ali AA, Abdel-Fattah RI (2006) Osmolytes-antioxidant behaviour in Phaseolus vulgaris and Hordeum vulgare with brassinosteroid under salt stress. J Agron 5:167–174CrossRefGoogle Scholar
  3. Arora N, Bhardwaj R, Sharma P, Arora HK (2008) Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress. Acta Physiol Plant 30:833–839CrossRefGoogle Scholar
  4. Bassard JE, Ullmann P, Bernier F, Werck-Reichhart D (2010) Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808–1824CrossRefPubMedGoogle Scholar
  5. Chai Y, Zhang Q, Tian L, Li CL, Xing Y, Qin L, Shen YY (2013) Brassinosteroid is involved in strawberry fruit ripening. Plant Growth Regul 69(1):63–69CrossRefGoogle Scholar
  6. Chérel I, Michard E, Platet N, Mouline K, Alcon C, Sentenac H, Thibaud JB (2002) Physical and functional interaction of the Arabidopsis K+ channel AKT2 and phosphatase AtPP2CA. Plant Cell 14:1133–1146PubMedCentralCrossRefPubMedGoogle Scholar
  7. Choudhary SP, Bhardwaj R, Gupta BD, Dutt P, Gupta RK, Biondi S, Kanwar M (2010) Epibrassinolide induces changes in indole-3-acetic acid, abscisic acid and polyamine concentrations and enhances antioxidant potential of radish seedlings under copper stress. Physiol Plant 140:280–296PubMedGoogle Scholar
  8. Choudhary SP, Bhardwaj R, Gupta BD, Dutt P, Kanwar M, Arora P (2009) Epibrassinolide regulated synthesis of polyamines and auxins in Raphanus sativus L. seedlings under Cu metal stress. Braz J Plant Physiol 21:25–32CrossRefGoogle Scholar
  9. Choudhary SP, Kanwar M, Bhardwaj R, Gupta BD, Gupta RK (2011) Epibrassinolide ameliorates Cr (VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 84:592–600CrossRefPubMedGoogle Scholar
  10. Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LS (2012a) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 7(3):e33210PubMedCentralCrossRefPubMedGoogle Scholar
  11. Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LS (2012b) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63(15):5659–5675PubMedCentralCrossRefPubMedGoogle Scholar
  12. Choudhary SP, Yu JQ, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2012c) Benefits of brassinosteroid crosstalk. Trends Plant Sci 17(10):594–605CrossRefPubMedGoogle Scholar
  13. Clouse SD (2008) Themolecular intersection of brassinosteroid-regulated growth and flowering in Arabidopsis. Proc Natl Acad Sci U S A 105(21):7345–7346PubMedCentralCrossRefPubMedGoogle Scholar
  14. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q (2012) Arabidopsis Ubiquitin Conjugase UBC32 is an ERAD component that functions in brassinosteroid- mediated salt stress tolerance. Plant Cell 24:233–244PubMedCentralCrossRefPubMedGoogle Scholar
  15. Das KC, Misra HP (2004) Hydroxyl radical scavenging and singlet oxygen quenching properties of polyamines. Mol Cell Biochem 262:127–133CrossRefPubMedGoogle Scholar
  16. de Cantú LB, Kandeler R (1989) Significance of polyamines for flowering in Spirodela punctata. Plant Cell Physiol 30:455–458Google Scholar
  17. Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151–164PubMedCentralCrossRefPubMedGoogle Scholar
  18. Eleiwa ME, Bafeel SO, Ibrahim SA (2011) Influence of brassinosteroids on wheat plant (Triticum aestivum L.) production under salinity stress conditions. I-Growth parameters and photosynthetic pigments. Aus J Basic Appl Sci 5(5):58–65Google Scholar
  19. El-Khallal SM, Hathout TA, Ashour AA, Kerrit AA (2009) Brassinolide and salicylic acid induced growth, biochemical activities and productivity of maize plants grown under salt stress. Res J Agric Biol Sci 5:380–390Google Scholar
  20. El-Mashad AA, Mohamed HI (2012) Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 249:625–635CrossRefPubMedGoogle Scholar
  21. Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 40:235–269CrossRefGoogle Scholar
  22. Fariduddin Q, Khalil RRAE, Mir BA, Yusuf M, Ahmad A (2013) 24-epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856CrossRefPubMedGoogle Scholar
  23. Friedrichsen D, Chory J (2001) Steroid signaling in plants: from the cell surface to the nucleus. Bioessays 23:1028–1036CrossRefPubMedGoogle Scholar
  24. Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 59(9):2299–2308PubMedCentralCrossRefPubMedGoogle Scholar
  25. Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant Cell Physiol 48:434–440CrossRefPubMedGoogle Scholar
  26. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334PubMedCentralCrossRefPubMedGoogle Scholar
  27. Guo DP, Sun YZ, Chen ZJ (2003) Involvement of polyamines in cytoplasmic male sterility of stem mustard (Brassica juncea var. tsatsai). Plant Growth Regul 41(1):33–40CrossRefGoogle Scholar
  28. Haubrick LL, Torsethaugen G, Assmann SM (2006) Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts. Physiol Plant 128:134–143CrossRefGoogle Scholar
  29. Hayat S, Ahmad A, Mobin M, Hussain A, Fariduddin Q (2000) Photosynthetic rate, growth, and yield of mustard plants sprayed with 28-homobrassinolide. Photosynthetica 38(3):469–471CrossRefGoogle Scholar
  30. Hayat S, Maheshwari P, Wani AS, Irfan M, Alyemeni MN, Ahmad A (2012) Comparative effect of 28-homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol Biochem 53:61–68CrossRefPubMedGoogle Scholar
  31. Houimli SIM, Denden M, Hadj SBEI (2008) Induction of salt tolerance in pepper (Capsicum annuum) by 24-epibrassinolide. EurAsian J BioSci 2:83–90Google Scholar
  32. Houimli SIM, Denden M, Mouhandes BD (2010) Effects of 24-epibrassinolide on growth, chlorophyll, electrolyte leakage and proline by pepper plants under NaCl-stress. EurAsian J BioSci 4:96–104CrossRefGoogle Scholar
  33. Huang CK, Chang BS, Wang KC, Her SJ, Chen TW, Chen YA, Cho CL, Liao LJ, Huang KL, Chen WS, Liu ZH (2004) Changes in polyamine pattern are involved in floral initiation and development in Polianthes tuberosa. J Plant Physiol 161:709–713CrossRefPubMedGoogle Scholar
  34. Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364CrossRefPubMedGoogle Scholar
  35. Kaveh H, Nemati H, Farsi M, Jartoodeh SV (2011) How salinity affect germination and emergence of tomato lines. J Biol Environ Sci 5(15):159–163Google Scholar
  36. Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10(1):51–62PubMedCentralCrossRefPubMedGoogle Scholar
  37. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381CrossRefPubMedGoogle Scholar
  38. Kwezi L, Meier S, Mungur L, Ruzvidzo O, Irving H, Gehring C (2007) The Arabidopsis thaliana brassinosteroid receptor (AtBRI1) contains a domain that functions as a guanylyl cyclase In Vitro. PLoS ONE 5:e449CrossRefGoogle Scholar
  39. Li J, Li Y, Chen S, An L (2010) Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis. J Exp Bot 61(15):4221–4230CrossRefPubMedGoogle Scholar
  40. Li D, Zhang Y, Hu X, Shen X, Ma L, Su Z, Wang T, Dong J (2011) Transcriptional profiling of Medicago truncatula under salt stress identified a novel CBF transcription factor MtCBF4 that plays an important role in abiotic stress responses. BMC Plant Biol 11:109–128PubMedCentralCrossRefPubMedGoogle Scholar
  41. Liu J, Gao H, Wang X, Zheng Q, Wang C, Wang X, Wang Q (2014) Effects of 24-epibrassinolide on plant growth, osmotic regulation and ion homeostasis of salt- stressed canola. Plant Biol 16:440–450CrossRefPubMedGoogle Scholar
  42. Liu JH, Honda C, Moriguchi T (2006) Involvement of polyamine in floral and fruit development. Jpn Agric Res Q 40:51–58CrossRefGoogle Scholar
  43. Liu JH, Moriguchi T (2007) Changes in free polyamines and gene expression during peach flower development. Biol Plant 51(3):530–532CrossRefGoogle Scholar
  44. Lorenzen I, Aberle T, Plieth C (2004) Salt stress-induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe. Plant J 38:539–544CrossRefPubMedGoogle Scholar
  45. Malmberg RL, Mcindoo J (1983) Abnormal floral development of a tobacco mutant with elevated polyamine levels. Nature 305:623–625CrossRefGoogle Scholar
  46. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724PubMedCentralCrossRefPubMedGoogle Scholar
  47. Movahed N, Eshghi S, Tafazoli E, Jamali B (2010) Effects of polyamines on vegetative characteristics, growth, flowering and yield of strawberry (‘Paros’ and ‘Selva’). Acta Hortic 926:287–293Google Scholar
  48. Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol 51:422–434CrossRefPubMedGoogle Scholar
  49. Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733PubMedCentralCrossRefPubMedGoogle Scholar
  50. Rastogi R, Sawhney VK (1990a) Polyamines and flower development in the male sterile stamenless-2 mutant of tomato (Lycopersicon esculentum Mill.). I. Level of polyamines and their biosynthesis in normal and mutant flowers. Plant Physiol 93:439–445PubMedCentralCrossRefPubMedGoogle Scholar
  51. Rastogi R, Sawhney VK (1990b) Polyamines and flower development in the male sterile stamenless-2 mutant of tomato (Lycopersicon esculentum Mill). II. Effects of polyamines and their biosynthetic inhibitors on the development of normal and mutant floral buds cultured in vitro. Plant Physiol 93:446–452PubMedCentralCrossRefPubMedGoogle Scholar
  52. Rea G, de Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, Gara LD, Federico R, Angelini R, Tavladoraki P (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiol 134(4):1414–1426PubMedCentralCrossRefPubMedGoogle Scholar
  53. Sannazzaro AI, Echeverría M, Albertó EO, Ruiz OA, Menéndez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45:39–46CrossRefPubMedGoogle Scholar
  54. Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404CrossRefPubMedGoogle Scholar
  55. Sfakianaki M, Sfichi L, Kotzabasis K (2006) The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J Photochem Photobiol B Biol 84:181–188CrossRefGoogle Scholar
  56. Sfichi L, Ioannidis N, Kotzabasis K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting complex II changes. Photochem Photobiol 80:499–506CrossRefPubMedGoogle Scholar
  57. Shahbaz M, Ashraf M, Athar HUR (2008) Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? Plant Growth Regul 55:51–64CrossRefGoogle Scholar
  58. Shahid MA, Pervez MA, Balal RM, Mattson NS, Rashid A, Ahmad R, Ayyub CM, Abbas T (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Aust J Crop Sci 5(5):500–510Google Scholar
  59. Sharma I, Ching E, Saini S, Bhardwaj R, Pati PK (2013) Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiol Biochem 69:17–26CrossRefPubMedGoogle Scholar
  60. Shi HZ, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97:6896–6901PubMedCentralCrossRefPubMedGoogle Scholar
  61. Smith MA, Davies PJ (1985) Separation and quantitation of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol 78:89–91PubMedCentralCrossRefPubMedGoogle Scholar
  62. Sood S, Nagar PK (2004) Changes in endogenous polyamines during flower development in two diverse species of rose. Plant Growth Regul 44(2):117–123CrossRefGoogle Scholar
  63. Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J, Hu ZM, Xu Y, Chen SL (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958CrossRefPubMedGoogle Scholar
  64. Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140(1):150–158PubMedCentralCrossRefPubMedGoogle Scholar
  65. Vardhini BV, Rao SSR (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 16(7):843–847CrossRefGoogle Scholar
  66. Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24(3):842–857PubMedCentralCrossRefPubMedGoogle Scholar
  67. Wan Y, Luo S, Chen J, Xiao X, Chen L, Zeng G, Liu C, He Y (2012) Effect of endophyte- infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750CrossRefPubMedGoogle Scholar
  68. Yanelis RG, Lissy RA, Lisbel MG, Luis MMM, Miriam NV (2014) Effect of brassinosteroids and its biosynthesis inhibitor in two varieties of tomato´s seedlings under salt stress. Cultivos Tropicales 35:25–34Google Scholar
  69. Yu X, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci U S A 105(21):7618–7623PubMedCentralCrossRefPubMedGoogle Scholar
  70. Zaharah SS, Singh Z, Symons GM, Reid JB (2012) Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. J Plant Growth Regul 31(3):365–372CrossRefGoogle Scholar
  71. Zapata PJ, Serrano M, Pretel MT, Amorós A, Botella MÁ (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788CrossRefGoogle Scholar
  72. Zhang Z, Ramirez J, Reboutier D, Brault M, Trouverie J, Pennarun AM, Amiar Z, Biligui B, Galagovsky L, Rona JP (2005) Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells. Plant Cell Physiol 46:1494–1504CrossRefPubMedGoogle Scholar
  73. Zhao F, Song CP, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072PubMedCentralCrossRefPubMedGoogle Scholar
  74. Zheng QS, Liu L, Liu ZP, Chen JM, Zhao GM (2009) Comparison of the response of ion distribution in the tissues and cells of the succulent plants Aloe vera and Salicornia europaea to saline stress. J Plant Nutr Soil Sci 172:875–883CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.College of Resources and Environmental Science, Key Laboratory of Marine BiologyNanjing Agricultural UniversityNanjingChina
  2. 2.Jiangsu Station of Agro-Ecological Monitoring and ProtectionNanjingChina
  3. 3.Anhui Academy of Agricultural SciencesHefeiChina

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