Advertisement

Symbiosis

, Volume 79, Issue 1, pp 59–74 | Cite as

Role of putrescine (Put) in imparting salt tolerance through modulation of put metabolism, mycorrhizal and rhizobial symbioses in Cajanus cajan (L.) Millsp.

  • Neera GargEmail author
  • Amrita Sharma
Article
  • 94 Downloads

Abstract

Salt stress is a major environmental constraint that limits growth and nitrogen-fixation in legumes. Role of putrescine (Put) and arbuscular mycorrhiza (AM) in improving functional efficiency of legumes has gained importance in recent years. Present investigations assessed the impact of Put (1 mM) seed priming and/or Rhizophagus irregularis inoculation on growth, mycorrhizal and rhizobial symbioses with an emphasis to correlate the same with nodular Put metabolism in pigeonpea (Cajanus cajan L.) genotypes (Tolerant-Pusa 2001 and Sensitive-Pusa 991) under salt stress. Salinity declined plant biomass, with greater negative effects on roots than shoots which reduced the mycorrhizal colonization as well as nodulation ability of Sinorhizobium fredii AR-4. The decline in nitrogen-fixing efficiency could be correlated with increase in Na+ concentrations in roots as well as nodules. Salinity reduced endogenous Put by increasing diamine oxidase (DAO) as well as decreasing arginine decarboxylase (ADC) as well as ornithine decarboxylase (ODC) activities in nodules. Put priming enhanced per cent mycorrhizal colonization which further increased the rhizobial symbiotic efficiency, more in Pusa 2001 than Pusa 991. Both Put priming and AM inoculations reduced Na+ uptake and improved nutrient status especially P in both underground organs, with AM more effective than Put. The further decline in Na+ uptake was recorded when both amendments were given together which enhanced nitrogen-fixing ability of nodules by modulating anabolic and catabolic enzyme activities responsible for Put biosynthesis. Hence, +Put+AM can be used as an effective strategy to improve symbiotic potential and arrest nodule senescence in pigeonpea under salt stress.

Keywords

Salt stress Rhizophagus irregularis Putrescine Cajanus cajan Rhizobial and mycorrhizal symbioses 

Notes

Acknowledgments

We gratefully acknowledge the University Grants Commission and Department of Biotechnology, Government of India, for providing financial support in undertaking the research work. We are also thankful to TERI, New Delhi, and Pulse laboratory, IARI, New Delhi, for providing the biological research material.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13199_2019_621_Fig6_ESM.png (92 kb)
ESM 1

Effect of Putrescine (Put) and arbuscular mycorrhizal (AM, Rhizophagus irregularis) inoculation on a) potassium to sodium ratio (K+/Na+) and b) calcium to sodium ratio (Ca2+/Na+) in roots of differentially salt-tolerant Pusa 2001 and Pusa 991 pigeonpea genotypes under different levels of salinity stress (0–100 mM). Each value is the mean of six replicates ± standard error (SE). Different letters above each line indicate significant differences among the treatments, assessed by Duncan multiple range test, at p ≤ 0.05. –Put–AM = Put unprimed non-AM plants; +Put–AM = Put primed non-AM plants; –Put+AM = Put unprimed AM plants; +Put+AM = Put primed AM plants (PNG 91 kb)

13199_2019_621_MOESM1_ESM.tif (3.3 mb)
High Resolution Image (TIF 3403 kb)
13199_2019_621_MOESM2_ESM.docx (15 kb)
ESM 2 (DOCX 15 kb)

References

  1. Abd-Alla MH, El-Enany AWE, Nafady NA, Khalaf DM, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. Viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169(1):49–58Google Scholar
  2. Ali RM (2000) Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Sci 152(2):173–179Google Scholar
  3. Ali Z, Salam A, Azhar FM, Khan IA (2007) Genotypic variation in salinity tolerance among spring and winter wheat (Triticum aestivum L.) accessions. South Afr J Bot 73:70–75Google Scholar
  4. Allen SF, Grimshaw HF, Rowl AB (1984) Chemical analysis. In: Moor PD, Chapman SB (eds) Methods in plant ecology. Blackwell, Oxford, pp 185–344Google Scholar
  5. Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44(5):384–395Google Scholar
  6. Becerra-Rivera VA, Bergström E, Thomas-Oates J, Dunn MF (2018) Polyamines are required for normal growth in Sinorhizobium meliloti. Microbiology 164(4):600–613Google Scholar
  7. Benavides MP, Aizencang G, Tomaro ML (1997) Polyamines in Helianthus annuus L. during germination under salt stress. J Plant Growth Regul 16(4):205–211Google Scholar
  8. Braeken K, Daniels R, Vos K, Fauvart M, Bachaspatimayum D, Vanderleyden J, Michiels J (2008) Genetic determinants of swarming in Rhizobium etli. Microb Ecol 55(1):54–64Google Scholar
  9. Bruning B, Rozema J (2013) Symbiotic nitrogen fixation in legumes: perspectives for saline agriculture. Environ Exp Bot 92:134–143Google Scholar
  10. Céccoli G, Ramos JC, Ortega LI, Acosta JM, Perreta MG (2011) Salinity induced anatomical and morphological changes in Chloris gayana Kunth roots. Biocell 35(1):9–17Google Scholar
  11. Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15–16):4245–4255Google Scholar
  12. Cheng Y, Ma W, Li X, Miao W, Zheng L, Cheng B (2012) Polyamines stimulate hyphal branching and infection in the early stage of Glomus etunicatum colonization. World J Microbiol Biotechnol 28(4):1615–1621Google Scholar
  13. Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann Bot 106(5):791–802Google Scholar
  14. Djanaguiraman M, Prasad PV (2013) Effects of salinity on ion transport, water relations and oxidative damage. In: Ecophysiology and responses of plants under salt stress. Springer, New York, pp 89–114Google Scholar
  15. Do PT, Drechsel O, Heyer AG, Hincha DK, Zuther E (2014) Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought. Front Plant Sci 5:182Google Scholar
  16. Egamberdieva D, Li L, Lindström K, Räsänen LA (2016) A synergistic interaction between salt-tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis fish.) under salt stress. Appl Microbiol Biotechnol 100(6):2829–2841Google Scholar
  17. El Ghachtouli N, Martin-Tanguy J, Paynot M, Gianinazzi S (1996) First-report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic acid treatment. FEBS Lett 385(3):189–192Google Scholar
  18. El Ghachtouli N, Paynot M, Morandi D, Martin-Tanguy J, Gianinazzi S (1995) The effect of polyamines on endomycorrhizal infection of wild-type Pisum sativum, cv. Frisson (nod+ myc+) and two mutants (nod− myc+ and nod− myc−). Mycorrhiza 5(3):189–192Google Scholar
  19. Estrada B, Aroca R, Maathuis FJ, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36(10):1771–1782Google Scholar
  20. Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22(3):203–217Google Scholar
  21. Fahmi AI, Nagaty HH, Eissa RA, Hassan MM (2011) Effects of salt stress on some nitrogen fixation parameters in faba bean. Pak J Biol Sci 14(6):385Google Scholar
  22. FAOSTAT (2018) http://www.fao.org/faostat/en/#data/QC [Accessed 23 Oct. 2018]
  23. Fariduddin Q, Mir BA, Yusuf M, Ahmad A (2014) 24-Epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica 52(3):464–474Google Scholar
  24. Farooq M, Gogoi N, Hussain M, Barthakur S, Paul S, Bharadwaj N, Migdadi HM, Alghamdi SS, Siddique KH (2017) Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiol Biochem 118:199–217Google Scholar
  25. Flores HE, Galston A (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69(3):701–706Google Scholar
  26. Fujihara S, Abe H, Minakawa Y, Akao S, Yoneyama T (1994) Polyamines in nodules from various plant-microbe symbiotic associations. Plant Cell Physiol 35(8):1127–1134Google Scholar
  27. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78(3):371–387Google Scholar
  28. Garg N, Bharti A (2018) Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress. Mycorrhiza 28(8):727–746Google Scholar
  29. Garg N, Manchanda G (2008) Effect of arbuscular mycorrhizal inoculation on salt-induced nodule senescence in Cajanus cajan (pigeonpea). J Plant Growth Regul 27(2):115–124.  https://doi.org/10.1007/s00344-007-9038-z Google Scholar
  30. Garg N, Singla P (2016) Stimulation of nitrogen fixation and trehalose biosynthesis by naringenin (Nar) and arbuscular mycorrhiza (AM) in chickpea under salinity stress. Plant Growth Regul 80(1):5–22Google Scholar
  31. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500Google Scholar
  32. Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331(1–2):313–327Google Scholar
  33. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21(2):117–129Google Scholar
  34. Hammer EC, Rillig MC (2011) The influence of different stresses on glomalin levels in an arbuscular mycorrhizal fungus—salinity increases glomalin content. PLoS One 6(12):e28426Google Scholar
  35. Hartree EF (1957) Haematin compounds. In: Paech K, Tracey MV (eds) Modern methods of plant analysis. Springer, Berlin, pp 197–245Google Scholar
  36. Hasanuzzaman M, Nahar K, Fujita M, Ahmad P, Chandna R, Prasad MNV, Ozturk M (2013) Enhancing plant productivity under salt stress: relevance of poly-omics. In: Salt Stress in Plants. Springer, New York, pp 113–156Google Scholar
  37. Herdina JA, Silsbury JH (1990) Estimating nitrogenase activity of faba bean (Vicia faba) by acetylene reduction (AR) assay. Aust J Plant Physiol 17(5):489–502Google Scholar
  38. Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040Google Scholar
  39. Hršelová H, Gryndler M (2000) Effect of spermine on proliferation of hyphae of Glomus fistulosum, an arbuscular mycorrhizal fungus, in maize roots. Folia Microbiol (Praha) 45(2):167Google Scholar
  40. IAB (2000) Indian Agriculture in Brief, 27th edn. Agriculture Statistics Division, Ministry of Agriculture, Govt. of India, New DelhiGoogle Scholar
  41. Iqbal M, Ashraf M (2006) Wheat seed priming in relation to salt tolerance: growth, yield and levels of free salicylic acid and polyamines. Ann Bot Fenn 43(4):250–259Google Scholar
  42. Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68(1):405–434.  https://doi.org/10.1146/annurev-arplant-042916-040936 Google Scholar
  43. Jackson ML (1973) Soil chemical analysis. Published by Printice Hall, New Delhi, p 485Google Scholar
  44. Jiménez Bremont JF, Marina M, Guerrero-González MD, Rossi FR, Sánchez-Rangel D, Rodríguez-Kessler M, Ruiz OA, Gárriz A (2014) Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Front Plant Sci 5:95Google Scholar
  45. Kenenil A, Assefa F, Prabu PC (2010) Characterization of acid and salt tolerant rhizobial strains isolated from faba bean fields of Wollo northern Ethiopia. J Agric Sci Technol 12:365–376Google Scholar
  46. Kormanik PP, McGraw AC (1982) Quantification of vesicular-arbuscular mycorrhizae in plant roots. In: Schenk NC (ed) Methods and principles of mycorrhizal research. APS Press, MinneapolisGoogle Scholar
  47. Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91(2):500–504Google Scholar
  48. Kumar V, Khare T (2015) Individual and additive effects of Na+ and cl ions on rice under salinity stress. Arch Agron Soil Sci 61(3):381–395Google Scholar
  49. Lahiri K, Chattopadhyay S, Ghosh B (2004) Correlation of endogenous free polyamine levels with root nodule senescence in different genotypes in Vigna mungo L. J Plant Physiol 161(5):563Google Scholar
  50. Legocka J, Sobieszczuk-Nowicka E (2012) Sorbitol and NaCl stresses affect free, microsome-associated and thylakoid-associated polyamine content in Zea mays and Phaseolus vulgaris. Acta Physiol Plant 34(3):1145–1151Google Scholar
  51. Lefevre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161(5):943–952Google Scholar
  52. Lindner RC (1944) Rapid analytical method for some of the more inorganic constituents of plants tissue. Plant Physiol 19:76–89Google Scholar
  53. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153(1):137–147Google Scholar
  54. Liu JH, Inoue H, Moriguchi T (2008) Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots. Environ Exp Bot 62(1):28–35Google Scholar
  55. López-Gómez M, Cobos-Porras L, Hidalgo-Castellanos J, Lluch C (2014) Occurrence of polyamines in root nodules of Phaseolus vulgaris in symbiosis with Rhizobium tropici in response to salt stress. Phytochemistry 107:32–41Google Scholar
  56. López-Gómez M, Hidalgo-Castellanos J, Muñoz-Sánchez JR, Marín-Peña AJ, Lluch C, Herrera-Cervera JA (2017) Polyamines contribute to salinity tolerance in the symbiosis Medicago truncatula-Sinorhizobium meliloti by preventing oxidative damage. Plant Physiol Biochem 116:9–17Google Scholar
  57. Mehlich A (1953) Determination of P, ca, mg, K, Na and NH4. In: Short test methods used in soil testing division. Department of Agriculture, RaleighGoogle Scholar
  58. 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 Google Scholar
  59. Munns R, Wallace PA, Teakle NL, Colmer TD (2010) Measuring soluble ion concentrations (Na+, K+, cl) in salt-treated plants. In: Sunkar R (ed) Plant stress tolerance. Methods in Molecular Biology. Springer, Berlin, pp 371–382Google Scholar
  60. Ndoye F, Kane A, Diedhiou AG, Bakhoum N, Fall D, Sadio O, Sy MO, Noba K, Diouf D (2015) Effects of dual inoculation with arbuscular mycorrhizal fungi and rhizobia on Acacia senegal (L.) Willd. Seedling growth and soil enzyme activities in Senegal. Int J Biosci 6(2):36–48Google Scholar
  61. Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65(1):109–112Google Scholar
  62. Nogales A, Aguirreolea J, Santa María E, Camprubí A, Calvet C (2009) Response of mycorrhizal grapevine to Armillaria mellea inoculation: disease development and polyamines. Plant Soil 317(1–2):177Google Scholar
  63. Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL (ed) Methods of soil analysis, Agron. No. 9, part 2- chemical and microbiological properties, 2nd edn. American Society Agronomy, Madison, pp 403–430Google Scholar
  64. Oufdou K, Benidire L, Lyubenova L, Daoui K, Fatemi ZEA, Schröder P (2014) Enzymes of the glutathione–ascorbate cycle in leaves and roots of rhizobia-inoculated faba bean plants (Vicia faba L.) under salinity stress. Eur J Soil Biol 60:98–103Google Scholar
  65. Peng J, Li Y, Shi P, Chen X, Lin H, Zhao B (2011) The differential behavior of arbuscular mycorrhizal fungi in interaction with Astragalus sinicus L. under salt stress. Mycorrhiza 21(1):27–33Google Scholar
  66. Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161Google Scholar
  67. Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26(7):673–684Google Scholar
  68. Quinet M, Ndayiragije A, Lefevre 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(10):2719–2733Google Scholar
  69. Ren CG, Bai YJ, Kong CC, Bian B, Xie ZH (2016) Synergistic interactions between salt-tolerant rhizobia and arbuscular mycorrhizal fungi on salinity tolerance of Sesbania cannabina plants. J Plant Growth Regul 35(4):1098–1107Google Scholar
  70. Rohyadi A, Noviani R, Isnaini M (2017) Responses of cowpea genotypes to arbuscular mycorrhiza. Agrivita J Agric Sci 39(3):288–295Google Scholar
  71. 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(1):39–46Google Scholar
  72. Sa TM, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97(3):928–935Google Scholar
  73. Saxena KB, Nadarajan N (2010) Prospects of pigeonpea hybrids in Indian agriculture. Electron J Plant Breed 1(4):1107–1117Google Scholar
  74. Schübler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421Google Scholar
  75. Sengupta A, Chakraborty M, Saha J, Gupta B, Gupta K (2016) Polyamines: osmoprotectants in plant abiotic stress adaptation. In: Osmolytes and plants acclimation to changing environment: emerging omics technologies springer, New Delhi, pp 97–127Google Scholar
  76. Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581(10):1993–1999Google Scholar
  77. Shi K, Huang YY, Xia XJ, Zhang YL, Zhou YH, Yu JQ (2008) Protective role of putrescine against salt stress is partially related to the improvement of water relation and nutritional imbalance in cucumber. J Plant Nutr 31(10):1820–1831Google Scholar
  78. Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-stressed wheat (Triticum aestivum L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35(8):2601–2610Google Scholar
  79. Tejera NA, Campos R, Sanjuan J, Lluch C (2004) Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. J Plant Physiol 161(3):329Google Scholar
  80. Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240(1):1–8Google Scholar
  81. Upreti KK, Murti GSR (2010) Response of grape rootstocks to salinity: changes in root growth, polyamines and abscisic acid. Biol Plant 54(4):730–734Google Scholar
  82. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313(2):369–375Google Scholar
  83. Vales MI, Rao GR, Sudini H, Patil SB, Murdock LL (2014) Effective and economic storage of pigeonpea seed in triple layer plastic bags. J Stored Prod Res 58:29–38Google Scholar
  84. Varshney RK, Penmetsa RV, Dutta S, Kulwal PL, Saxena RK, Datta S, Sharma TR, Cook DR (2010) Pigeonpea genomics initiative (PGI): an international effort to improve crop productivity of pigeonpea (Cajanus cajan L.). Mol Breed 26(3):393–408Google Scholar
  85. Vassileva V, Ignatov G (1999) Polyamine-induced changes in symbiotic parameters of the Galega orientalis–Rhizobium galegae nitrogen-fixing system. Plant Soil 210(1):83–91Google Scholar
  86. Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils: effects of variations in digestion conditions and of organic soil constituents. Soil Sci 63(4):251–264Google Scholar
  87. Walters D (2003) Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytol 159(1):109–115Google Scholar
  88. Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11(6):1548–1561Google Scholar
  89. Wisniewski JP, Brewin NJ (2002) Possible Role for Diamine Oxidase in Infection Threads. In: Nitrogen Fixation: From Molecules to Crop Productivity Springer, Dordrecht. pp 259–259Google Scholar
  90. Wisniewski JP, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant-Microbe Interact 13(4):413–420Google Scholar
  91. Wu H, Shabala L, Barry K, Zhou M, Shabala S (2013) Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiol Plant 149(4):515–527Google Scholar
  92. Wu Q, Zou YN, He XH (2010) Exogenous putrescine, not spermine or spermidine, enhances root mycorrhizal development and plant growth of trifoliate orange (Poncirus trifoliata) seedlings. Int J Agric Biol 12:576–580Google Scholar
  93. Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68(1):27–35Google Scholar
  94. Xu Y, Shi GX, Ding CX, Xu XY (2011) Polyamine metabolism and physiological responses of Potamogeton crispus leaves under lead stress. Rus J Plant Physiol 58:460–466Google Scholar
  95. Yasuta Y, Kokubun M (2014) Salinity tolerance of super-nodulating soybean genotype En-b0-1. Plant Prod Sci 17(1):32–40Google Scholar
  96. Zeid IM (2004) Response of bean (Phaseolus vulgaris) to exogenous putrescine treatment under salinity stress. Pak J Biol Sci 7(2):219–225Google Scholar
  97. Zhang GW, Xu SC, Hu QZ, Mao WH, Gong YM (2014) Putrescine plays a positive role in salt-tolerance mechanisms by reducing oxidative damage in roots of vegetable soybean. J Integr Agric 13:349–357Google Scholar
  98. Zhang Y, Xie L, Xiong B, Zeng M, Liu J, Yu D, Yuan J (2003) Effect of polyamine on growth and development of arbuscular mycorrhizal fungi in vitro culture condition. Mycosystema 22(3):417–423Google Scholar
  99. Zhao FG, Sun C, Liu YL, Zhang WH (2003) Relationship between polyamine metabolism in roots and salt tolerance of barley seedlings. Acta Bot Sin 45:295–300Google Scholar
  100. Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of BotanyPanjab UniversityChandigarhIndia

Personalised recommendations