The Genetic Reprogramming of Polyamine Homeostasis During the Functional Assembly, Maturation, and Senescence-Specific Decline of the Photosynthetic Apparatus in Hordeum vulgare

Journal of Plant Growth Regulation

Volumn 33, Issue 1, 2014, Pages 77-90

  Ioannidis, Nikolaos E ^a,b   Zschiesche, Wiebke ^b   Barth, Olaf ^b   Kotakis, Christos ^a   Navakoudis, Eleni ^a   Humbeck, Klaus ^b   Kotzabasis, Kiriakos ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

De etiolation; Photosynthesis; Polyamines; Senescence

Indexed keywords

HORDEUM; HORDEUM VULGARE;

EID: 84897573048     PISSN: 07217595     EISSN: 14358107     Source Type: Journal    
DOI: 10.1007/s00344-013-9387-8     Document Type: Review

References (77)

1. Andreadakis A, Kotzabasis K. (1996) The role of polyamines in the chloroplast photodevelopment. Changes in the biosynthesis and catabolism of the polyamines in isolated plastids during the chloroplast photodevelopment. J Photochem Photobiol B33: 163-170.
2. Antognoni F, Fornale S, Grimma C, Komor E, Bagni N (1998) Long distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204: 520-527.
3. Barth O, Vogt S, Uhlemann R, Zschiesche W, Humbeck K (2009) Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29. Plant Mol Biol 69: 213-226.
4. - to QB. Biochim Biophys Acta 1767: 905-912.
5. Besford RT, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189: 201-206.
6. Boffey S, Selldén G, Leech R (1980) Influence of cell age on chlorophyll formation in light-grown and etiolated wheat seedlings. Plant Physiol 65: 680-684.
7. Borrell A, Culianez-Macià FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109: 771-776.
8. Caffaro SV, Scaramagli S, Antognoni F, Bagni N (1993) Polyamine content and translocation in soyabean plants. J Plant Physiol 41: 563-568.
9. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101: 9909-9914.
10. Coffino P (2001) Regulation of cellular polyamines by antizyme. Nat Rev Mol Cell Biol 2: 187-194.
11. Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York.
12. Cona A, Cenci F, Cervelli M, Federico R, Mariottini P, Moreno S, Angelini R (2003) Polyamine oxidase, a hydrogen peroxide-producing enzyme, is up-regulated by light and down-regulated by auxin in the outer tissues of the maize mesocotyl. Plant Physiol 131: 803-813.
13. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11: 80-88.
14. Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148: 1094-1105.
15. Del Duca S, Tidu V, Bassi R, Esposito C, Serafini-Fracassini D (1994) Identification of chlorophyll-a/b proteins as substrates of transglutaminase activity in isolated chloroplasts of Helianthus tuberosus. Planta 193: 283-289.
16. Dresselhaus T, Barcelo P, Hagel C, Lörz H, Humbeck K (1996) Isolation and characterization of a Tritordeum cDNA encoding S-adenosylmethionine decarboxylase that is circadian-clock-regulated. Plant Mol Biol 30: 1021-1033.
17. Eisenberg T, Knauer H, Schauer A et al (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11: 1305-1319.
18. Evans PT, Malmberg RL (1989) Do polyamines have a role in plant development? Annu Rev Plant Physiol Plant Mol Biol 40: 235-269.
19. Galston AW (2001) Plant biology-retrospect and prospect. Curr Sci 80: 150-152.
20. Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol (Stuttg) 10: 37-49.
21. Griffiths WT (1978) Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem J 174: 681-692.
22. Holloway PJ, Maclean DJ, Scott KJ (1983) Rate-limiting steps of electron transport in chloroplasts during ontogeny and senescence of barley. Plant Physiol 72: 795-801.
23. Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53: 927-937.
24. Hu WW, Gong H, Pua EC (2005) The pivotal roles of the plant S-adenosylmethionine decarboxylase 5′ untranslated leader sequence in regulation of gene expression at the transcriptional and posttranscriptional levels. Plant Physiol 138: 276-286.
25. Humbeck K, Krupinska K (2003) The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light. J Exp Bot 54: 375-383.
26. Humbeck K, Quast S, Krupinska K (1996) Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant Cell Environ 19: 337-344.
27. Inada N, Sakai A, Kuroiwa H, Kuroiwa T (1998) Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles. Investigations of tissues and cells by fluorescence microscopy. Planta 205: 153-164.
28. Ioannidis N.E., Kotzabasis K. (2007) The effects of the polyamines on the functionality of the photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767: 1372-1382.
29. Ioannidis NE, Sfichi L, Kotzabasis K (2006) Putrescine stimulates chemiosmotic ATP synthesis. Biochim Biophys Acta 1757: 821-828.
30. Ioannidis NE, Ortigosa S, Veramendi J, Pintó-Marijuan M, Fleck I, Carvajal P, Kotzabasis K, Santos M, Torné JM (2009) Remodeling of tobacco thylakoids by over-expression of maize plastidial transglutaminase. Biochim Biophys Acta 1787: 1215-1222.
31. Ioannidis NE, Cruz JA, Kotzabasis K, Kramer DM (2012) Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS One 7: e29864.
32. Jumtee K, Bamba T, Okazawa A, Fukusaki E, Kobayashi A (2008) Integrated metabolite and gene expression profiling revealing phytochrome a regulation of polyamine biosynthesis of Arabidopsis thaliana. J Exp Bot 59: 1187-1200.
33. Kahana C (2009) Antizyme and antizyme inhibitor, a regulatory tango. Cell Mol Life Sci 66: 2479-2488.
34. Kasukabe Y, He LX, 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: 712-722.
35. Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW (2003) Polyamines in plants: an overview. J Cell Mol Biol 2: 1-12.
36. Kotzabasis K, Christakis-Hampsas MD, Roubelakis-Angelakis KA (1993) A narrow bore HPLC method for the identification and quantitation of free, conjugated and bound polyamines. Anal Biochem 214: 484-489.
37. Krupinska K (2006) Fate and activities of plastids during leaf senescence. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Amsterdam, pp 433-449.
38. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228: 367-381.
39. Laurenzi M, Rea G, Federico R, Tavladoraki P, Angelini R (1999) De-etiolation causes a phytochrome-mediated increase of polyamine oxidase expression in outer tissues of the maize mesocotyl: a role in the photomodulation of growth and cell wall differentiation. Planta 208: 146-154.
40. Legocka J, Zajchert I (1999) Role of spermidine in the stabilization of the apoprotein of the light-harvesting chlorophyll a/b-protein complex of photosystem II during leaf senescence process. Acta Physiol Plant 21: 127-132.
41. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58: 115-136.
42. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372: 366-369.
43. Lütz C (1986) Prolamellar bodies. In: Staehelin LA, Arntzen CJ (eds) Photosynthesis III: photosynthetic membranes and light-harvesting systems, vol 19. Springer, Berlin, pp 683-692.
44. Martínez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10(Suppl 1): 15-22.
45. Maxwell K, Johnson G (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659-668.
46. Miersch I, Heise J, Zelmer I, Humbeck K (2000) Differential degradation of the photosynthetic apparatus during leaf senescence in barley (Hordeum vulgare L.). Plant Biol 2: 618-623.
47. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008a) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147: 1845-1857.
48. Moschou PN, Delis ID, Paschalidis KA, Roubelakis-Angelakis KA (2008b) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol Plant 133: 140-156.
49. Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39: 503-532.
50. Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim Biophys Acta 1621: 160-169.
51. Navakoudis E, Vrentzou K, Kotzabasis K (2007) A polyamine- and LHCII protease activity-based mechanism regulates the plasticity and adaptation status of the photosynthetic apparatus. Biochim Biophys Acta 1767: 261-271.
52. Ouelhadj A, Kaminski M, Mittag M, Humbeck K (2007) Receptor-like protein kinase HvLysMR1 of barley (Hordeum vulgare L.) is induced during leaf senescence and heavy metal stress. J Exp Bot 58: 1381-1396.
53. Oukarroum A, Madidi SE, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60: 438-446.
54. Paschalidis KA, Roubelakis-Angelakis KA (2005) Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiol 138: 2174-2184.
55. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
56. Robertson D, Laetsch W (1974) Structure and function of developing barley plastids. Plant Physiol 54: 148-159.
57. 2 assimilation, and plant growth by over acidification of the thylakoid lumen. Plant Cell 23: 304-321.
58. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163: 987-992.
59. Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84: 145-151.
60. Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706: 250-261.
61. Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolution. Photochem Photobiol 78: 543-557.
62. Shaw P, Henwood J, Oliver R, Griffiths T (1985) Immunogold localization of protochlorophyllide oxidoreductase in barley etioplasts. Eur J Cell Biol 39: 50-55.
63. Sood S, Nagar PK (2005) Xylem and phloem derived polyamines during flowering in two diverse rose species. J Plant Growth Regul 24: 36-40.
64. Srivastava A, Strasser RJ, Govindjee (1999) Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37: 365-392.
65. Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185-196.
66. Stamp P, Herzog H (1976) Untersuchungen zur Fahnenblattalterung und zum Kornwachstum einiger deutscher Sommerweizensorten (Triticum aestivum L.). Z Pflanzenzucht 77: 330-338.
67. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 5: 749-790.
68. Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105: 1-6.
69. Tassoni A, van Buuren M, Franceschetti M, Fornalè S, Bagni N (2000) Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiol Biochem 38: 383-393.
70. Tiburcio AF, Kaur-Sawhney R, Galston AW (1990) Polyamine metabolism. In: Miflin BJ, Lea PJ (eds), Intermediary nitrogen metabolism. The biochemistry of plants, vol. 16. Academic Press, San Diego, pp 283-325.
71. Tiburcio AF, Altabella T, Borrell A, Masgrau C (1997) Polyamine metabolism and its regulation. Physiol Plant 100: 664-674.
72. 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: 369-375.
73. Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579: 1557-1564.
74. Wellburn AR (1982) Bioenergetic and ultrastructural changes associated with chloroplast development. Int Rev Cytol 80: 133-191.
75. Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ, Honda C, Moriguchi T (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17: 251-263.
76. Wiedemuth K, Müller J, Kahlau A, Amme S, Mock H, Grzam A, Hell R, Egle K, Beschow H, Humbeck K (2005) Successive maturation and senescence of individual leaves during barley whole plant ontogeny reveals temporal and spatial regulation of photosynthetic function in conjunction with C and N metabolism. J Plant Physiol 162: 1226-1236.
77. Xiong H, Stanley BA, Tekwani BL, Pegg AE (1997) Processing of mammalian and plant S-adenosylmethionine decarboxylase proenzymes. J Biol Chem 272: 28342-28348.