Plastid-associated polyamines: Their role in differentiation, structure, functioning, stress response and senescence

Plant Biology

Volumn 16, Issue 2, 2014, Pages 297-305

  Sobieszczuk Nowicka, E ^a   Legocka, J ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Chloroplast; Differentiation; Etioplast; Metabolism; Polyamines; Senescence; Stress; Transglutaminases

Indexed keywords

BIOCHEMICAL COMPOSITION; CHLOROPHYLL A; ENVIRONMENTAL STRESS; LIGHT INTENSITY; MOLECULAR ANALYSIS; PLASTID; PROTEIN; SENESCENCE;

CHLOROPHYLL; POLYAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ADAPTATION; CHLOROPLAST; DIFFERENTIATION; ETIOPLAST; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS; PLANT; REVIEW; SENESCENCE; STRESS; THYLAKOID;

CHLOROPLAST; DIFFERENTIATION; ETIOPLAST; METABOLISM; POLYAMINES; SENESCENCE; STRESS; TRANSGLUTAMINASES;

ADAPTATION, PHYSIOLOGICAL; CHLOROPHYLL; CHLOROPLASTS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; POLYAMINES; STRESS, PHYSIOLOGICAL; THYLAKOIDS;

EID: 84897645161     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12058     Document Type: Review

References (87)

1. Alcazar R., Altabella T., Marco F., Bortolotii C., Reymond M., Koncz C., Carrasco P., Tiburcio A.F. (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237-1249.
2. Andreadakis A., Kotzabasis K. (1996) Changes in the biosynthesis and catabolism of polyamines in isolated plastids during chloroplast photodevelopment. Journal of Photochemistry and Photobiology B: Biology, 33, 163-170.
3. Bagni N., Serafini-Fracassini D. (1974) The role of polyamines as growth factors in higher plants and their mechanism of action. In: Galston A.W., Smith T.A. (Eds), Plant growth substances. Hirokawa Publ. Co. Inc, Tokyo, Japan, pp 1205-1217.
4. Bais H.P., Ravishankar G.A. (2002) Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell, Tissue and Organ Culture, 69, 1-34.
5. Beauchemin R., Harnois J., Rouillon R., Tajmir-Riahi H.A., Carpentier R. (2007) Interaction of polyamines with proteins of photosystem II: cation binding and photosynthetic oxygen evolution. Journal of Molecular Structure, 833, 169-174.
6. Beigbeder A., Vavadakis M., Navakoudis E., Kotzabasis K. (1995) Influence of polyamine inhibitors on light-independent and light-dependent chlorophyll biosynthesis and on the photosynthetic rate. Journal of Photochemistry and Photobiology B: Biology, 28, 235-242.
7. Besford R.D., Richardson C.M., Campos J.L., Tiburcio A.F. (1993) Effect of polyamines on stabilisation complexes in thylakoid membranes of osmotically stressed oat leaves. Planta, 189, 201-206.
8. Biswal B., Udaya C., Raval M.K. (Eds), (2003) Chloroplast biogenesis. From proplastid to gerontoplast. Springer, Berlin, Germany, pp 19-72.
9. Borrell A., Culiaez-Macia F.A., Altabella T., Besford R.T. (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiology, 109, 771-776.
10. Bortolotti C., Cordeiro A., Alcazar R., Borrell A., Culianez-Macia F.A., Tiburcio A.F., Altabella T. (2004) Localization of arginine decarboxylase in tobacco plants. Physiologia Plantarum, 120, 84-92.
11. Campos A., Carvajal-Vallejos P.K., Villalobos E., Franco C.F., Almeida A.M., Coelho A.V., Torne J.M., Santos M. (2009) Characterisation of Zea mays L. plastidial transglutaminase: interactions with thylakoid membrane proteins. Plant Biology, 12, 708-716.
12. Campos N., Villalobos E., Fontanet P., Torné J.M., Santos M. (2012) A peptide of 17 amino acids from the N-terminal region of maize plastidial transglutaminase is essential for chloroplast targeting. American Journal of Molecular Biology, 2, 245-257.
13. Campos N., Castanón S., Urreta I., Santos M., Torné J.M. (2013) Rice transglutaminase gene: identification, protein expression, functionality, light dependence and specific cell location. Plant Science, 206, 97-110.
14. Davies P.J. (Ed.), (2006) Plant hormones. Kluwer Academic, Dordrecht, the Netherlands.
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 L. Planta, 193, 283-289.
16. Della Mea M., Caparros-Ruiz D., Claparolos I., Serafini-Fracassini D., Rigau J. (2004) AtPng1p. The first plant transglutaminase. Plant Physiology, 135, 2046-2054.
17. Della Mea M., De Filippis F., Genovesu V., Serafini-Fracassini D., Del Duca S. (2007) The acropetal wave of developmental cell death of tobacco corolla is preceded by activation of transglutaminase in different cell compartments. Plant Physiology, 144, 1211-1222.
18. Demetriou G., Neonaki C., Navakoudis E., Kotzabasis K. (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus - The protective role of polyamines. Biochimica et Biophysica Acta, 1767, 272-280.
19. Dondini L., Del Duca S., Dall'Agata L., Bassi R., Gastaldelli M., Della Mea M., Di Sandro A., Claparos I., Serafini-Fracassini D. (2003) Suborganellar localisation and effect of light on Helianthus tuberosus chloroplast transglutaminases and their substrates. Planta, 217, 84-95.
20. Duan H.G., Yuan S., Liu W.J., Xi D.H., Qing D.H., Liang H.G., Lin H.H. (2006) Effects of exogenous spermidine on photosystem II of wheat seedlings under water stress. Journal of Integrative Plant Biology, 48, 920-927.
21. Farooq M., Wahid A., Lee D.J. (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiologiae Plantarum, 31, 937-945.
22. Fesus L., Thomazy V. (1988) Searching for the function of tissue transglutaminase: its possible involvement in the biochemical pathway of programmed cell death. Advances in Experimental Medicine and Biology, 231, 119-134.
23. Fesus L., Thomazy V., Autuori F., Ceru M.P., Tarcsa E., Piacentini M. (1989) Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action. FEBS Letters, 245, 150-154.
24. Gaensslen R., McCarly R. (1971) Amine uptake in chloroplasts. Archives of Biochemistry and Biophysics, 147, 55-65.
25. Galston A.W. (2001) Plant biology - retrospect and prospect. Current Science, 80, 150-152.
26. Griffin M., Verderio E. (2000) Tissue transglutaminase in cell death. In: Bryant J.A., Hughes S.G., Garland J.M. (Eds), Programmed cell death in animals and plants. BIOS Scientific, Oxford, UK, pp 223-240.
27. Griffin M., Casadio R., Bergamini C.M. (2002) Transglutaminases: nature's biological glues. The Biochemical Journal, 368, 377-396.
28. Guarino L.S., Cohen S.S. (1979) Uptake and accumulation of putrescine and its lethality in Anacystis nidulans. Proceedings of the National Academy of Sciences of the United States of America, 76, 3184-3188.
29. Hamdani S., Tajmir-Riahi H.A., Carpentier R. (2009) Methylamine interaction with proteins of photosystem II: a comparison with biogenic polyamines. Journal of Photochemistry and Photobiology B: Biology, 96, 201-206.
30. Hamdani S., Yaakoubi H., Carpentier R. (2011a) Polyamine interaction with thylakoid proteins during stress. Journal of Photochemistry Photobiology B: Biology, 142, 314-319.
31. Hamdani S., Gauthier A., Msilini N., Carpentier R. (2011b) Positive charges of polyamines protect PSII in isolated thylakoid membranes during photoinhibitory conditions. Plant and Cell Physiology, 52, 866-873.
32. Horton P., Ruban A.V., Walters R.G. (1994) Regulation of light harvesting in green plants: indication by non-photochemical quenching of chlorophyll fluorescence. Plant Physiology, 106, 415-420.
33. Hussain S.S., Ali M., Ahmad M., Siddique K.H.M. (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances, 29, 300-311.
34. Ioannidis N.E., Kotzabasis K. (2007) The effects of polyamines on the functionality of the photosynthetic membrane in vivo and in vitro. Biochimica et Biophysica Acta, 1767, 1372-1382.
35. Ioannidis N.E., Sfichi L., Kotzabasis K. (2006) Putrescine stimulates chemiosmotic ATP synthesis. Biochimica et Biophysica Acta, 1757, 821-828.
36. Ioannidis N.E., Ortigosa S.M., Veramendi J., Pinto-Marijuan M., Fleck I., Carvajal-Vallejos P., Kotzabasis K., Santos M., Torne J.M. (2009) Remodeling of tobacco thylakoids by over-expression of Zea mays plastidal transglutaminase. Biochimica et Biophysica Acta, 1878, 1215-1222.
37. Ioannidis N.E., Sfichi-Duke L., Kotzabasis K. (2011) Polyamines stimulate non-photochemical quenching of chlorophyll a fluorescence in Scenedesmus obliquus. Photosynthesis Reasearch, 107, 169-175.
38. Ioannidis N.E., Cruz J.A., Kotzabasis K., Kramer D.M. (2012a) Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS ONE, 7, e29864.
39. Ioannidis N.E., Tsiavos T., Kotzabasis K. (2012b) Chemical bonding of chlorophylls and plant aminic axial ligands impact harvesting of visible light and quenching of fluorescence. Photochemistry and Photobiology, 88, 98-106.
40. Ioannidis N.E., Lopera O., Santos M., Torné J.M., Kotzabasis K. (2012c) Role of plastid transglutaminase in LHCII polyamination and thylakoid electron and proton flow. PLoS ONE, 7, e41979.
41. Kamada-Nobusada T., Hayashi M., Fukazawa M., Sakakibara H., Nishimura M. (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in the polyamine catabolism in Arabidopsis thaliana. Plant and Cell Physiology, 49, 1272-1282.
42. Kotzabasis K. (1995) A role for chloroplast-associated polyamines. Botanica Acta, 109, 5-7.
43. Kotzabasis K., Fatinou C., Rubelakis-Angelakis K.A., Ghanotakis D. (1993) Polyamines in the photosynthetic apparatus. Photosystem II highly resolved subcomplexes are enriched in spermine. Photosynthesis Research, 38, 83-88.
44. Kumar A., Altabella T., Taylor M., Tiburcio A.F. (1997) Recent advances in polyamine research. Trends in Plant Science, 2, 124-130.
45. Kusano T., Berberich T., Tateda C., Takahashi Y. (2008) Polyamines: essentials factors for growth and survival. Planta, 228, 367-381.
46. Kuznetsov V.L.V., Radyukina N.L., Shevyakova N.I. (2005) Polyamines and stress: biological role, metabolism and regulation. Russian Journal of Plant Physiology, 53, 583-604.
47. Legocka J., Zajchert I. (1999) Role of spermidine in stabilization of the apoprotein of the light-harvesting chlorophyll a/b-protein complex of photosystem II during leaf senescence process. Acta Physiologiae Plantarum, 21, 127-132.
48. Lindemose S., Nielsen P.E., Mollegaard N.E. (2005) Polyamines preferentially interact with bent adenine tracts in double-stranded DNA. Nucleic Acids Research, 33, 1790-1803.
49. Lorand L., Graham R.M. (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nature Reviews, Molecular Cell Biology, 4, 140-156.
50. Lütz C., Navakoudis E., Seidlitz H., Kotzabasis K. (2005) Simulated solar irradiation with enhanced UV-B adjusts plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochimica et Biophysica Acta, 1710, 24-33.
51. Margosiak S.A., Dharma A., Bruce-Caver M.R., Gonzales A.P., Louie D., Kuehn G.D. (1990) Identification of the large subunit of ribulose 1, 5-bisphosphate carboxylase/oxygenase as a substrate for transglutaminase in Medicago sativa L. (alfalfa). Plant Physiology, 92, 88-96.
52. Moschou P.N., Sanmartin M., Andriopoulou A.H., Rojo E., Sanchez-Serrano J.J., Roubelakis-Angelakis K.A. (2008) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiology, 147, 1845-1857.
53. Mullineaux C.W. (2005) Function and evolution of grana. Trends in Plant Science, 10, 521-525.
54. Murakami S., Packer L. (1971) The role of cations in the organization of chloroplast membranes. Archives of Biochemistry and Biophysics, 146, 337-347.
55. 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. Biochimica et Biophysica Acta, 1767, 261-271.
56. Ortigosa S.M., Díaz-Vivancos P., Clemente-Moreno M.J., Pint́-Marijuan M., Fleck I., Veramendi J., Santos M., Hernandez J., Torné J.M. (2010) Oxidative stress induced in tobacco leaves by chloroplast over-expression of maize plastidial transglutaminase. Planta, 232, 593-605.
57. Pandey S., Ranade S.A., Nagar P.K., Kumar N. (2000) Role of polyamine and ethylene as modulators of plant senescence. Journal of Bioscience and Bioengineering, 25, 291-299.
58. Pavan G.M., Danani A., Pricl S., Smith D.K. (2009) Modeling the multivalent recognition between dendritic molecules and DNA: understanding how ligand "Sacrifice" and screening can enhance binding. Journal of American Chemical Society, 131, 9686-9694.
59. Pinto-Marijuan M., de Agazio M., Zacchini M., Santos M.A., Torne J.M., Fleck I. (2007) Response of transglutaminase activity and bound putrescine to changes in light intensity under natural and controlled conditions in Quercus ilex leaves. Physiologia Plantarum, 131, 159-169.
60. Ruban A.V., Berera R., Ilioaia C., van Stokkum I.H.M., Kennis J.T.M., Pascal A.A., van Amerongen H., Robert B., Horton P., van Grondelle R. (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature, 450, 575-578.
61. Serafini-Fracasini D., Della Mea M., Tasco G., Casadio R., Del Duca S. (2009) Plant and animal transglutaminases: do similar functions imply similar structures? Amino Acids, 36, 643-657.
62. Serafini-Fracassini D., Del Duca S. (2008) Transglutaminases: Widespread Cross-linking Enzymes in Plants. Annals of Botany, 102, 145-152.
63. Serafini-Fracassini D., Del Duca S., Monti F., Poli F., Sacchetti G., Bregoli A.M., Biondi S., Della Mea M. (2002) Transglutaminase activity during senescence and programmed cell death in the corolla of tobacco (Nicotiana tabacum) flowers. Cell Death and Differentiation, 9, 309-321.
64. Serafini-Fracassini D., Di Sandro A., Del Duca S. (2010) Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems. Plant Physiology and Biochemistry, 48, 602-611.
65. Sfakianaki M., Sfichi L., Kotzabasis K. (2006) The involvement of LHCII-associated polyamines in the response of photosynthetic apparatus to low temperature. Journal of Photochemistry and Photobiology B: Biology, 84, 181-188.
66. 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. Photochemistry and Photobiology, 8, 499-506.
67. Sfichi-Duke L., Ioannidis N.E., Kotzabasis K. (2008) Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress: a comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta, 228, 341-353.
68. Shu S., Guo S.R., Sun J., Yuan L.Y. (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiologia Plantarum, 146, 285-296.
69. Shweta S., Nagar P.K. (2003) The effect of polyamines on leaf senescence in two diverse rose species. Plant Growth Regulation, 39, 155-160.
70. Sindhu R.K., Cohen S.S. (1984) Subcellular localization of spermidine synthase in the protoplast of Chinese cabbage leaves. Plant Physiology, 76, 219-223.
71. Sobieszczuk-Nowicka E., Rorat T., Legocka J. (2007a) Polyamine metabolism and S-adenosylmethionine decarboxylase gene expression during the cytokinin-stimulated greening process. Plant Growth Regulation, 39, 155-160.
72. Sobieszczuk-Nowicka E., Di Sandro A., Del Duca S., Serafini-Fracassini D., Legocka J. (2007b) Plastid-membrane-associated polyamines and thylakoid transglutaminases during etioplast-to-chloroplast transformation stimulated by kinetin. Physiologia Plantarum, 130, 590-600.
73. Sobieszczuk-Nowicka E., Krzeslowska M., Legocka J. (2008) Transglutaminases and their substrates in kinetin-stimulated etioplast-to-chloroplast transformation in Cucumis sativus cotyledons. Protoplasma, 233, 187-194.
74. Sobieszczuk-Nowicka E., Wieczorek P., Legocka J. (2009) Kinetin affects the level of chloroplast polyamines and transglutaminase activity during senescence of barley leaves. Acta Biochimica Polonica, 56, 255-259.
75. Stoynova E.Zh., Karanov E.N., Alexieva V. (1999) Subcellular aspects of the protective effect of spermine against atrazine in pea plants. Plant Growth Regulation, 29, 175-180.
76. Subhan D., Murthy S.D.S. (2001) Effect of polyamines on chlorophyll and protein contents. Photochemical activity and energy transfer in detached wheat leaves during dark incubation. Plant Biology, 44, 529-533.
77. Takahashi T., Kakehi J.I. (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany, 105, 1-6.
78. Tavladoraki P., Rossi M.N., Saccuti G., Perez-Amador M.A., Polticelli F., Angelini R., Federico R. (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiology, 149, 1519-1532.
79. Tiburcio A.F., Campos J.L., Figueras X., Besford R.T. (1993) Recent advances in the understanding of polyamine functions during plant development. Plant Growth Regulation, 12, 331-340.
80. Torrigiani P., Serafini-Fracassini D., Biondi S., Bagni N. (1986) Evidence for the subcellular localization of polyamines and their biosynthetic enzymes in plant cells. Journal of Plant Physiology, 124, 23-29.
81. Tsiavos T., Ioannidis N.E., Kotzabasis K. (2012) Polyamines induce aggregation of LHC II and quenching of fluorescence in vitro. Biochimica et Biophysica Acta, 1817, 735-743.
82. Unal D., Tuney I., Sukatar A. (2008) The role of external polyamines on photosynthetic responses, lipid peroxidation, protein and chlorophyll a content under the UV-A (352 nm) stress in Physcia semipinnata. Journal of Photochemistry and Photobiology B: Biology, 90, 64-68.
83. Van Doorn W., Yoshimoto K. (2010) Role of chloroplasts and other plastids in ageing and death of plants and animals: a tale of Vishnu and Shiva. Ageing Research Reviews, 9, 117-130.
84. Villalobos J.M., Torne J., Rigau I., Olles I., Claparos M., Santos V. (2001) Immunogold localization of transglutaminase related to grana development in different Zea mays cell types. Protoplasma, 216, 155-163.
85. Villalobos E., Santos M., Talavera D., Rodriguez-Falcon M., Torne J.M. (2004) Molecular cloning and characterization of a Zea mays transglutaminase complementary DNA. Gene, 336, 93-104.
86. Yoda H., Yamaguchi Y., Sano H. (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiology, 132, 1973-1981.
87. Yoda H., Hiroi Y., Sano H. (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiology, 142, 193-206.