Polyamine catabolism adds fuel to leaf senescence

Amino Acids

Volumn 49, Issue 1, 2017, Pages 49-56

  Sobieszczuk Nowicka, E ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Barley; Catabolism; Leaf; Polyamines; Senescence; Transglutaminases

Indexed keywords

CHLOROPHYLL; POLYAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PUTRESCINE; REACTIVE OXYGEN METABOLITE; SPERMIDINE; SPERMINE; ETHYLENE; ETHYLENE DERIVATIVE; OXIDOREDUCTASE; POLYAMINE OXIDASE;

AMINO ACID METABOLISM; ARABIDOPSIS; DARKNESS; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE EXPRESSION; HOMEOSTASIS; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PLANT LEAF; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; PROTOPLAST; REVIEW; SENESCENCE; ETIOLATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS; DARKNESS; ETHYLENES; ETIOLATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HORDEUM; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PLANT LEAVES; PUTRESCINE; REACTIVE OXYGEN SPECIES; SPERMIDINE; SPERMINE; TRANSGLUTAMINASES;

EID: 85007499822     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-016-2377-y     Document Type: Review

References (65)

1. Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564
2. Anwar R, Mattoo A, HandaA (2015) Polyamine interactions with plant hormones: crosstalk at several levels in Kusano T, Suzuki H (eds). Polyamines a Universal Molecular Nexus for Growth, Survival and Specialized Metabolism. Tokyo: Springer, pp 267–303
3. Apelbaum A, Burgoon AL, Anderson JD, Liberman M, Ben Arie R, Mattoo AK (1981) Polyamines inhibits biosynthesis of ethylene in higher plant tissue and fruit protoplasts. Plant Physiol 68:453–456
4. Besford RD, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206
5. Cai G, Sobieszczuk-Nowicka E, Aloisi I, Fattorini L, Serafini-Fracassini D, Del Duca S (2015) Polyamines are common players in different facets of plant programmed cell death. Amino Acids 47:27–44
6. Campos A, Carvajal-Vallejos PK, Villalobos E, Franco CF, Almeida AM, Coelho AV, Torne JM, Santos M (2010) Characterisation of Zea mays L. plastidial transglutaminase: interactions with thylakoid membrane proteins. Plant Biol 12:708–716
7. Cassol T, Mattoo AK (2003) Do polyamines and ethylene interact to regulate plant growth, development and senescence? In: Nath P, Mattoo A, Ranade SR, Weil JH (eds) Molecular insights in plant biology. Science Publishers Inc, Enfield, USA, pp 121–132
8. Cejudo FJ, Ferrández J, Cano B, Puerto-Galán L, Guinea M (2012) The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling. FEBS Lett 586:2974–2980
9. Cogen SS (1998) A guide to polyamines. Oxford University Press, New York
10. Cohen AS, Popovic R, Zalik S (1979) Effects of polyamines on chlorophyll and protein content, photochemical activity, and chloroplast ultrastructure of barley leaf discs during senescence. Plant Physiol 64:717–720
11. Del Duca S, Tidu V, Bassi R, Serafini-Fracassini D, Esposito C (1994) Identification of transglutaminase activity and its substrates in isolated chloroplast of Helianthus tuberosus. Planta 193:283–289
12. Del Duca S, Serafini-Fracassini D, Cai G (2014) Senescence and programmed cell death in plants: polyamine action mediated by transglutaminase. Plant metabolism and chemodiversity. Front Plant Sci 5:120
13. Della Mea M, Di Sandro A, Dondini L, Del Duca S, Vantini F, Bergamini C, Bassi R, Serafini-Fracassini D (2004a) A Zea mays 39-kDa thylakoid transglutaminase catalyses the modification by polyamines of light-harvesting complex II in a light-dependent way. Planta 219:754–764
14. Della Mea M, Caparrós-Ruiz D, Claparols I, Serafini-Fracassini D, Rigau J (2004b) AtPng1p. The first plant transglutaminase. Plant Physiol 135:2046–2054
15. Dondini L, Del Duca S, Dall’Agata L, Bassi R, Gastaldelli M, Della Mea M, Di Sandro A, Claparols I, Serafini-Fracassini D (2003) Suborganellar localisation and effect of light on Helianthus tuberosus chloroplast transglutaminase and their substrates. Planta 217:84–95
16. Fincato P, Moschou PN, Ahou A, Angelini R, Roubelakis-Angelakis KA, Federico R et al (2012) The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue- and organ-specific expression pattern during seedling growth and flower development. Amino Acids 42:831–841
17. Fluhr R, Mattoo AK (1996) Ethylene—biosynthesis and perception. Crit Rev Plant Sci 15:479–523
18. Galston AW, Altman A, Kaur-Sawhney R (1978) Polyamines, ribonuclease and the improvement of oat leaf protoplasts. Plant Sci Lett 11:169–179
19. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R et al (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7:R76
20. Harpaz-Saad S, Yoon GM, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. Annu Plant Reviews 44:53–81
21. Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51
22. Igarashi K, Terui Y, Kashiwagi K (2015) The polyamine modulon: genes encoding proteins whose synthesis is enhanced by polyamines at the level of translation. In: Kusano T, Suzuki H (eds) Polyamines: a universal molecular nexus for growth, survival and specialized metabolism. Springer, Tokyo, pp 131–142
23. Ioannidis NE, Zschiesche W, Barth O, Kotakis C, Navakoudis E, Humbeck K, Kotzabasis K (2014) The genetic reprogramming of polyamine homeostasis during the functional assembly, maturation, and senescence: specific decline of the photosynthetic apparatus in Hordeum vulgare. J Plant Grow Regul 33:77–90
24. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17:2587–2600
25. Jing HC, Sturre MJ, Hille J, Dijkwel PP (2002) Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J 32:51–63
26. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282
27. Kaur-Sawhney R, Altman A, Galston AW (1978) Dual mechanisms in polyamine-mediated control of ribonuclease activity in oat leaf protoplasts. Plant Physiol 62:158–160
28. Kaur-Sawhney R, Shih LM, Flores HE, Galston AW (1982) Relation of polyamine synthesis and titer to aging and senescence in oat leaves. Plant Physiol 69:405–410
29. Kusano T, Suzuki H (2015) Polyamines: a universal molecular nexus for growth, survival and specialized metabolism. Springer, Tokyo
30. Lasanajak Y, Minocha R, Minocha SC, Goyal R, Fatima T, Handa AK, Mattoo AK (2014) Enhanced flux of substrates into polyamine biosynthesis but not ethylene in tomato fruit engineered with yeast S-adenosylmethionine decarboxylase gene. Amino Acids 46:729–742
31. 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
32. Legocka J, Sobieszczuk-Nowicka E, Wojtyla Ł, Samardakiewicz S (2015) Lead-stress induced changes in the content of free, thylakoid- and chromatin-bound polyamines, photosynthetic parameters and ultrastructure in greening barley leaves. J Plant Physiol 186–187:15–24
33. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Ann Rev Plant Biol 58:115–136
34. Linka N, Theodoulou FL (2013) Peroxisomes and their key role in cellular signaling and metabolism. In: Luis R (ed) Peroxisomes and their key role in cellular signaling and metabolism. Springer, Berlin, pp 169–194
35. Luka Z, Mudd SH, Wagner C (2009) Glycine N-methyltransferase and regulation of S-adenosylmethionine levels. J Biol Chem 284:22507–22511
36. Marina M, Maiale SJ, Rossi FR, Romero MF, Rivas EI, Gárriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147:2164–2178
37. Mattoo AK, Handa AK (2008) Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci 174:386–393
38. Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen-carbon interactions. Plant Physiol 142:1759–1770
39. Mattoo AK, Minocha SC, Minocha R, Handa AK (2010) Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38:405–413
40. Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality and vine life. Nat Biotechnol 20:613–618
41. Mizrahi Y, Applewhite PB, Galston AW (1989) Polyamine binding to proteins in oat and petunia protoplasts. Plant Physiol 91:738–743
42. Moschou PN, Roubelakis-Angelakis KA (2013) Polyamines and programmed cell death. J Exp Bot 3:1061–1066
43. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (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 Physiol 147:1845–1857
44. Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:695–709
45. Nambeesan S, Datsenka T, Ferruzzi MG, Malladi A, Mattoo AK, Handa AK (2010) Overexpression of yeast spermidine synthase impacts ripening, senescence and decay symptoms in tomato. Plant J 63:836–847
46. Noushina I, Nazar R, Khan MIR, Masood A, Khan NA (2011) Role of gibberellins in regulation of source-sink relations under optimal and limiting environmental conditions. Curr Sci 100:998–1007
47. Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosci 25:291–299
48. Park MH, Nishimura K, Zanelli CF, Valentini SR (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38:491–500
49. Radyukina NL, Mapelli S, Ivanov YuV, Kartashov AV, Brambilla I, Kuznetsov VIV (2009) Homeostasis of polyamines and antioxidant systems in roots and leaves of Planta go major under salt stress. Russian J Plant Physiol 56:323–331
50. Schipper JHM, Schmidt R, Wagstaff C, Jing HC (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol 169:914–930
51. Sequera-Mutiozabal MI, Erban A, Kopka J, Atanasov KE, Bastida J, Fotopoulos V, Alcázar R, Tiburcio AF (2016) Global Metabolic Profiling of Arabidopsis Polyamine Oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. Front Plant Sci 7:173. doi:10.3389/fpls.2016.00173
52. Serafini-Fracassini D, Del Duca S (2008) Transglutaminases: widespread cross-linking enzymes in plants. Ann Bot 102:145–152
53. 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 Physiol Biochem 48:602–611
54. Sobieszczuk-Nowicka E, Legocka J (2014) Plastid-associated polyamines: their role in differentiation, structure, functioning, stress response and senescence. Plant Biol 16:297–305
55. Sobieszczuk-Nowicka E, Wieczorek P, Legocka J (2009) Kinetin affects the level of chloroplast polyamines and transglutaminase activity during senescence of barley leaves. Acta Biochim Pol 56:255–259
56. Sobieszczuk-Nowicka E, Zmienko A, Samelak-Czajka A, Łuczak M, Pietrowska-Borek M, Iorio R, Del Duca S, Figlerowicz M, Legocka J (2015) Dark-induced senescence of barley leaves involves activation of plastid transglutaminases. Amino Acids 47:825–838
57. Sobieszczuk-Nowicka E, Kubala S, Zmienko A, Małecka A, Legocka J (2016) From accumulation to degradation: reprogramming polyamine metabolism facilitates dark-induced senescence in barley leaf cells. Front Plant Sci 6:1198. doi:10.3389/fpls.2015.01198
58. Takahashi T, Kakehi J (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6
59. Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A et al (2004) A subset of hypersensitive response marker genes, including HSR203 J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J 40:586–595
60. Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54:1127–1132
61. Van der Graaff E, Schwacke R, Desimone M, Flugge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792
62. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
63. Woo Hr, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death: regulation by multiple layers of control and implications for aging in general. J Cell Sci 126:4823–4833
64. Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981
65. 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 Physiol 142:193–206