Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones

Plant Growth Regulation

Volumn 76, Issue 1, 2015, Pages 71-82

  Li, Zhou ^a   Zhou, Hui ^a   Peng, Yan ^a   Zhang, Xinquan ^a   Ma, Xiao ^a   Huang, Linkai ^a   Yan, Yanhong ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Abscisic acid; Antioxidant enzyme; Auxin; Creeping bentgrass (Agrostis stolonifera L.); Reactive oxygen species; Regulation

Indexed keywords

EID: 84939943044     PISSN: 01676903     EISSN: 15735087     Source Type: Journal    
DOI: 10.1007/s10725-014-9978-9     Document Type: Article

References (75)

1. Alcázar R, Cuevas JC, Patron M, Altabella T, Tiburcio AF (2006) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455
2. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–13
3. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15(3):413–428
4. Bouchereau A, Aziz A, Lahrer F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125
5. 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 72:248–254
6. Chance B, Maehly AC (1955) Assay of catalase and peroxidase. Method Enzymol 2:764–775
7. Childs AC, Mehta DJ, Germer EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406
8. Cvikrova M, Gemperlova L, Dobra J, Martincova O, Prasil IT (2012) Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Sci 182:49–58
9. DaCosta M, Huang BR (2007a) Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in response to drought stress. J Am Soc Hortic Sci 132(2):319–326
10. DaCosta M, Huang BR (2007b) Drought survival and recuperative ability of bentgrass species associated with changes in abscisic acid and cytokinin production. J Am Soc Hort Sci 132:60–66
11. Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. Plant Horm A 1–15
12. Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Biol 42:55–76
13. Dhindsa RS, Dhindsa PP, Thorpe TA (1981) Leaf senescence: correlated with increased leaves of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
14. Dobra J, Motyka V, Dobrev P, Malbeck J, Prasil IT, Haisel D, Gaudinova A, Havlova M, Gubis J, Vankova R (2010) Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol 167:1360–1370
15. Du H, Wu N, Fu J, Wang S, Li X, Xiao J, Xiong L (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 63:6467–6480
16. Du H, Wu N, Chang Y, Li XH, Xiao JH, Xiong LZ (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83:475–488
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 165:1620–1635
18. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620
19. Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant 31:937–945
20. Fu JM, Huang BR (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114
21. Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314
22. Guo XL, Ma YY, Liu ZH, Liu BH (2008) Effects of exterior abscisic acid on calcium distribution of mesophyll cells and calcium concentration of guard cells in maize seedlings. Agric Sci China 7(4):438–446
23. Han YJ, Cho KC, Hwang OJ, Choi YS, Shin AY, Hwang I, Kim JI (2012) Overexpression of an Arabidosis β-glucosidase gene enhances drought resistance with dwarf phenotype in creeping bentgrass. Plant Cell Rep 31:1677–1686
24. Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355
25. Hoagland CR, Arnon DI (1950) The solution culture method for growing plants without soil. Calif Agric Exp Circ 347:1–32
26. Hu XH, Zhang Y, Shi Y, Zhang Z, Zou ZR, Zhang H, Zhao JZ (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209
27. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162
28. Javid GM, Sorooshzadeh A, Moradi F, Mohammad SA, Sanavy M, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734
29. Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273
30. Karsten HD, Macadam JW (2001) Effect of drought on growth, carbohydrates, and soil water use by perennial ryegrass, tall fescue, and white clover. Crop Sci 41:156–166
31. Kasukabe Y, He L, Nada K, Misawa S, Iharu I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stress and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722
32. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) The Polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:251–252
33. Lee TM (1997) Polyamine regulation of growth and chilling tolerance of rice (Oryza sativa L.) roots cultured in vitro. Plant Sci 122:111–117
34. Levitt LK, Stein DB, Rubinstein B (1987) Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L. Plant Physiol 85(2):318–321
35. Li CZ, Jiao J, Wang GX (2004) The important roles of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress. Plant Sci 166:303–315
36. Li Z, Peng Y, Ma X (2013a) Different response on drought tolerance and post-drought recovery between the small-leafed and the large-leafed white clover (Trifolium repens L.) associated with antioxidative enzyme protection and lignin metabolism. Acta Physiol Plant 35:213–222
37. Li Z, Shi P, Peng Y (2013b) Improved drought tolerance through drought preconditioning associated with changes in antioxidant enzyme activities, gene expression and osmoregulatory solutes accumulation in white clover (Trifolium repens L.). Plant Omics 6(6):481–489
38. 2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138
39. Ma C, Wang ZQ, Kong BB, Lin TB (2013) Exogenous trehalose differentially modulate antioxidant defense system in wheat callus during water deficit and subsequent recovery. Plant Growth Regul 70:275–285
40. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Odadoi K (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellins biosynthesis because of over expression of a putative AP2 transcription factor. Plant J 37:720–729
41. Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–51
42. Marco F, Alcázar R, Tiburcio AF, Carrasco P (2011) Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS 15:775–781
43. McCann SE, Huang BR (2008) Drought responses of kentucky bluegrass and creeping bentgrass as affected by abscisic acid and trinexapac-ethyl. J Am Soc Hortic Sci 133(1):20–26
44. Merewitz EB, Gianfagna T, Huang BR (2010) Effects of SAG12-ipt and HSP18.2-ipt expression on cytokinin production, root growth, and leaf senescence in creeping bentgrass exposed to drought stress. J Am Soc Hortic Sci 135(3):230–239
45. Merewitz EB, Gianfagna T, Huang BR (2011a) Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis in Agrostis stolonifera. J Exp Bot 62(1):383–395
46. Merewitz EB, Gianfagna T, Huang BR (2011b) Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J Exp Bot 62(15):5311–5333
47. Merewitz EB, Du HM, Yu WJ, Liu YM, Gianfagna T, Huang BR (2012) Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot 63(3):1315–1328
48. Morkunas I, Mai VC, Waskiewicz A, Formela M, Golinski P (2014) Major phytohormones under abiotooc stress. In: Ahmad A, Wani MR (eds) Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 87–135
49. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880
50. Nir I, Moshelion M, Weiss D (2014) The Arabidopsis gibberellin methyl transferase 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant, Cell Environ 37(1):113–123
51. Pemadasa MA (1981) Differential abaxial and adaxial stomatal responses to indole-3-acetic acid in Commelina communis L. New Phytol 90:209–219
52. Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol 70:253–264
53. Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65(5):1271–1283
54. Pustovoitova TN, Zhdanova NE, Zholkevich VN (2004) Changes in the levels of IAA and ABA in cucumber leaves under progressive soil drought. Russ J Plant Physiol 51(4):513–517
55. Roberts DR, Dumbroff EB, Thompson JE (1986) Exogenous polyamines alter membrane fluidity in bean leaves—a basis for their potential misinterpretation of their true physiological role. Planta 167:395–401
56. Rodrigues C, Vandenberghe LPD, de Oliveira J, Soccol CR (2011) New perspectives of gibberellic acid production: a review. Crit Rev Biotechnol 32:263–273
57. Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328
58. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658
59. Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864
60. Sudha G, Ravishankar GA (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during defense responses, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tissue Org Cult 71:181–212
61. Tiburcio AF, Besford RT, Capell T, Borell A, Testillano PS, Risueno MC (1994) Mechanism of polyamine action during senescence responses induced by osmotic stress. J Exp Bot 45:1789–1800
62. Tun NN, Santa-Catatina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47(3):346–354
63. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66
64. Volaire F, Thomas H, Bertagne N, Bourgeois E, Gautier MF, Lelievre F (1998) Survival and recovery of perennial forage grasses under prolonged Mediterranean drought: water status, solute accumulation, abscisic acid concentration and accumulation of dehydrin transcripts in bases of immature leaves. New Phytol 140:451–460
65. 3 and abscisic acid. Plant Growth Regul 26:165–173
66. Wang ZL, Huang BR (2003) Genotypic variation in abscisic acid accumulation, water relations, and gas exchange for Kentucky bluegrass exposed to drought stress. J Am Soc Hortic Sci 128:349–355
67. Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645
68. Wang YL, Ma FG, Li MJ, Liang D, Zou J (2011) Physiological responses of kiwifruit plants to exogenous ABA under drought conditions. Plant Growth Regul 64:63–74
69. Warnke S (2003) Creeping bentgrass (Agrostis stolonifera L.). In: Casler DD, Duncan RR (eds) Turfgrass biology, genetics, and breeding. Wiley, New Jersey, pp 175–185
70. Wen XP, Ban Y, Inoue H, Matsuda N, Kita M, Moriguchi T (2011) Antisense inhibition of a spermidine synthase gene highlights the role of polyamines for stress alleviation in pear shoots subjected to salinity and cadmium. Environ Exp Bot 72:157–166
71. Xu YC, Wang J, Shan L, Dong X, Li MM (2001) Effect of exogenous polyamines on glycolate oxidase activity and active oxygen species accumulation in wheat seedlings under osmotic stress. Isr J Plant Sci 49:173–178
72. Yang JC, Zhang JH, Wang ZQ, Zhu QS, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323
73. Yiu JC, Liu CW, Fang DYT, Lai YS (2009) Waterlogging tolerance of welsh onion (Allium fistulosum L.) enhanced by exogenous spermidine and spermine. Plant Physiol Biochem 47:710–716
74. Zawaski C, Busov VB (2014) Roles of Gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS ONE 9(1):e86217
75. Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–1901