Enhanced flux of substrates into polyamine biosynthesis but not ethylene in tomato fruit engineered with yeast S-adenosylmethionine decarboxylase gene

Amino Acids

Volumn 46, Issue 3, 2014, Pages 729-742

  Lasanajak, Yi ^a,b   Minocha, Rakesh ^c   Minocha, Subhash C ^a   Goyal, Ravinder ^d,e   Fatima, Tahira ^d,f   Handa, Avtar K ^g   Mattoo, Autar K ^d  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c USDA FOREST SERVICE   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e Ag Fd Canada   (Canada)

^f UNIVERSITY OF WESTERN ONTARIO   (Canada)

^g PURDUE UNIVERSITY   (United States)

Author keywords

Fruit metabolism; In vivo flux of metabolism; Plant growth regulators; SAM decarboxylase; Tomato; Transgenics

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; ARGININE; CARBON 14; ETHYLENE; METHIONINE; ORNITHINE; ORNITHINE DECARBOXYLASE; POLYAMINE; PUTRESCINE; SPERMIDINE; SPERMINE; ETHYLENE DERIVATIVE;

AMINO ACID ANALYSIS; AMINO ACID TRANSPORT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FRUIT RIPENING; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; ISOTOPE LABELING; METABOLITE; NONHUMAN; POLYAMINE SYNTHESIS; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; SAMDC GENE; TOMATO; TRANSGENIC PLANT; YEAST; CHEMISTRY; ENZYMOLOGY; FRUIT; GENETICS; METABOLISM; STAPHYLOCOCCUS AUREUS; TISSUE ENGINEERING;

LYCOPERSICON ESCULENTUM;

ADENOSYLMETHIONINE DECARBOXYLASE; ETHYLENES; FRUIT; LYCOPERSICON ESCULENTUM; POLYAMINES; STAPHYLOCOCCUS AUREUS; TISSUE ENGINEERING;

EID: 84896314658     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1624-8     Document Type: Article

References (50)

1. Alcázar R, Garcia-Martinez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J 43:425-436 (Pubitemid 41577009)
2. Apelbaum A, Goldlust A, Icekson I (1985) Control by ethylene of arginine decarboxylase activity in pea (Pisum sativum cultivar Kelvedon Wonder) seedlings and its implication for hormone regulation of plant growth. Plant Physiol 79:635-640
3. Bastola DR, Minocha SC (1995) Increased putrescine biosynthesis through transfer of mouse ornithine decarboxylase cDNA in carrot promotes somatic embryogenesis. Plant Physiol 109:63-71
4. Bhatnagar P, Glasheen B, Bains S, Long S, Minocha R, Walter C, Minocha S (2001) Transgenic manipulation of the metabolism of polyamines in poplar cells. Plant Physiol 125:2139-2153 (Pubitemid 32375794)
5. Bhatnagar P, Minocha R, Minocha S (2002) Genetic manipulation of the metabolism of polyamines in poplar cells: the regulation of putrescine catabolism. Plant Physiol 128:1455-1469 (Pubitemid 34305797)
6. Bürstenbinder K, Rzewuski G, Wirtz M et al (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J 49:238-249 (Pubitemid 46058950)
7. Bürstenbinder K, Waduwara I, Schoor S, Moffatt BA, Wirtz M, Minocha SC, Oppermann Y, Bouchereau A, Hell R, Sauter M (2010) Inhibition of 5′-methylthioadenosine metabolism in the Yang cycle alters polyamine levels, and impairs seedling growth and reproduction in Arabidopsis. Plant J 62:977-988
8. Caffaro S, Scaramagli S, Antognoni F, Bagni N (1993) Polyamine content and translocation in soybean plants. Plant Physiol 101:563-568
9. Cassol T, Mattoo AK (2003) Do polyamines and ethylene interact to regulate plant growth, development and senescence? In: Nath P, Mattoo AK, Ranade SA, Weil JH (eds) Molecular insight in plant biology. Science Publ Inc, Enfield, pp 121-132
10. Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York
11. De Agazio M, Zacchini M, Cesare F, Cellai L, Rizea-Savu S, Silvestro L (1996) 1-N-acetylspermidine in roots of maize seedlings. Plant Sci 121:143-149
12. DeScenzo RA, Minocha SC (1993) Modulation of cellular polyamines in tobacco by transfer and expression of mouse ornithine decarboxylase cDNA. Plant Mol Biol 22:113-127
13. Even-Chen Z, Mattoo AK, Goren R (1982) Inhibition of ethylene biosynthesis by aminoethoxyvinylglycine and by polyamines shunts label from 3,4-[14C]methionine into spermidine in aged orange peel discs. Plant Physiol 69:385-388
14. Fluhr R, Mattoo AK (1996) Ethylene - biosynthesis and perception. Crit Rev Plant Sci 15:479-523 (Pubitemid 126485250)
15. Gupta A, Pal RK, Rajam MV (2013) Delayed ripening and improved fruit processing quality in tomato by RNAi-mediated silencing of three homologs of 1-aminopropane-1-carboxylate synthase gene. J Plant Physiol 170:987-995
16. Handa A, Srivastava A, Deng Z, Gaffe J, Arora A, Tiznado-Hernandez M-E, Goyal RK, Malladi A, Negi PS, Mattoo AK (2010) Biotechnological interventions to improve plant developmental traits. In: Transgenic crop plants. Springer-Verlag, Heidelberger, pp 199-248
17. 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
18. Hyodo H, Tanaka K (1986) Inhibition of 1-Aminocyclopropane-l-carboxylic acid synthase activity by polyamines, their related compounds and metabolites of S-adenosylmethionine. Plant Cell Physiol 27:391-398
19. Kim JH, Kim HS, Lee YH et al (2008) Polyamine biosynthesis regulated by StARD expression plays an important role in potato wound periderm formation. Plant Cell Physiol 49:1627-1632
20. Kushad MM, Yelenosky G, Knight R (1988) Interrelationship of polyamine and ethylene biosynthesis during avocado fruit development and ripening. Plant Physiol 87:463-467
21. Li N, Parsons BL, Liu D, Mattoo AK (1992) Accumulation of wound-inducible ACC synthase transcript in tomato fruit is inhibited by salicylic acid and polyamines. Plant Mol Biol 18:477-487
22. Lizada MCC, Yang SF (1979) A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Anal Biochem 100:140-145
23. Luka Z, Mudd SH, Wagner C (2009) Glycine N-methyltransferase and regulation of S-adenosylmethionine levels. J Biol Chem 284:22507-22511
24. Majumdar R, Shao L, Minocha R, Long S, Minocha SC (2013) Ornithine: the overlooked molecule in the regulation of polyamine metabolism. Plant Cell Physiol 54:990-1004
25. Mattoo AK, Handa AK (2008) Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci 174:386-393
26. Mattoo AK, Suttle JC (1991) The plant hormone ethylene. CRC Press, Boca Raton
27. 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
28. Mayer MJ, Michael AJ (2003) Polyamine homeostasis in transgenic plants overexpressing ornithine decarboxylase includes ornithine limitation. J Biochem 134:765-772 (Pubitemid 38031277)
29. Mehta R, Handa A, Mattoo A (1997) Interactions of ethylene and polyamines in regulating fruit ripening. In: Kanellis AK, Chang C, Kende H, Grierson D (eds) Biology and biotechnology of the plant hormone ethylene. Kluwer Acad Publ, Boston, pp 321-326
30. 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 (Pubitemid 34595157)
31. Minocha R, Shortle WC, Long SL, Minocha SC (1994) A rapid and reliable procedure for extraction of cellular polyamines and inorganic ions from plant tissues. J Plant Growth Regul 13:187-193
32. Minocha R, Long S, Maki H, Minocha SC (1999) Assays for the activities of polyamine biosynthetic enzymes using intact tissues. Plant Physiol Biochem 37:597-603 (Pubitemid 29432482)
33. Minocha R, Minocha SC, Long S (2004) Polyamines and their biosynthetic enzymes during somatic embryo development in red spruce (Picea rubens Sarg.). In vitro Cell Dev Biol 40:572-580
34. Morilla A, Garcia JM, Albi MA (1996) Free polyamine contents and decarboxylase activities during tomato development and ripening. J Agri Food Chem 44:2608-2611 (Pubitemid 126453547)
35. 2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708-1724
36. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008b) 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
37. Nambeesan S, Handa AK, Mattoo AK (2008) Polyamines and regulation of ripening and senescence. In: Paliyath G, Murr DP, Handa AK, Lurie S (eds) Postharvest biology and technology of fruits, vegetables and flowers. Willey-Blackwell Publ, Ames, pp 319-340
38. 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
39. Nölke G, Schneider B, Agdour S, Drossard J, Fischer R, Schillberg S (2008) Modulation of polyamine biosynthesis in transformed tobacco plants by targeting ornithine decarboxylase to an atypical subcellular compartment. Open Biotechnol J 2:183-189
40. Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61:880-894
41. Quan Y, Minocha R, Minocha SC (2002) Genetic manipulation of polyamine metabolism in poplar II: effects on ethylene biosynthesis. Plant Physiol Biochem 40:929-937 (Pubitemid 35409397)
42. Rea G, de Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, De Gara L, Federico R, Angelini R, Tavladoraki P (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiol 134:1414-1426 (Pubitemid 38527352)
43. Roberts DR, Dumbroff EB, Thompson JE (1986) Exogenous polyamines alter membrane fluidity in bean leaves - a basis for potential misinterpretation of their true physiological role. Planta 167:395-401
44. Rudus I, Sasiak M, Kȩpczyn'ski J (2013) Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene. Acta Physiol Plant 35:295-307
45. Rzewuski G, Cornell KA, Rooney L et al (2007) OsMTN encodes a 5′-methylthioadenosine nucleosidase that is up-regulated during submergence induced ethylene synthesis in rice (Oryza sativa L). J Exp Bot 58:1505-1514 (Pubitemid 47355649)
46. Saftner RA, Baldi BG (1990) Polyamine levels and tomato fruit development: possible interaction with ethylene. Plant Physiol 92:547-550 (Pubitemid 120029720)
47. Sauter M, Lorbiecke R, Ouyang B et al (2005) The immediate-early ethylene response gene OsARD1 encodes an acireductone dioxygenase involved in recycling of the ethylene precursor S-adenosylmethionine. Plant J 44:718-729
48. Shao L, Majumdar R, Minocha SC (2012) Profiling the aminopropyltransferases in plants: their structure, expression and manipulation. Amino Acids 42:813-830
49. 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 (Pubitemid 351421971)
50. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155-189