Planta

, Volume 235, Issue 6, pp 1221–1237 | Cite as

Regulation of polyamine metabolism and biosynthetic gene expression during olive mature-fruit abscission

Original Article

Abstract

Exogenous ethylene and some inhibitors of polyamine biosynthesis can induce mature-fruit abscission in olive, which could be associated with decreased nitric oxide production as a signaling molecule. Whether H2O2 also plays a signaling role in mature-fruit abscission is unknown. The possible involvement of H2O2 and polyamine in ethylene-induced mature-fruit abscission was examined in the abscission zone and adjacent cells of two olive cultivars. Endogenous H2O2 showed an increase in the abscission zone during mature-fruit abscission, suggesting that accumulated H2O2 may participate in abscission signaling. On the other hand, we followed the expression of two genes involved in the polyamine biosynthesis pathway during mature-fruit abscission and in response to ethylene or inhibitors of ethylene and polyamine. OeSAMDC1 and OeSPDS1 were expressed differentially within and between the abscission zones of the two cultivars. OeSAMDC1 showed slightly lower expression in association with mature-fruit abscission. Furthermore, our data show that exogenous ethylene or inhibitors of polyamine encourage the free putrescine pool and decrease the soluble-conjugated spermidine, spermine, homospermidine, and cadaverine in the olive abscission zone, while ethylene inhibition by CoCl2 increases these soluble conjugates, but does not affect free putrescine. Although the impact of these treatments on polyamine metabolism depends on the cultivar, the results confirm that the mature-fruit abscission may be accompanied by an inhibition of S-adenosyl methionine decarboxylase activity, and the promotion of putrescine synthesis in olive abscission zone, suggesting that endogenous putrescine may play a complementary role to ethylene in the normal course of mature-fruit abscission.

Keywords

Abscission zone Ethylene Mature-fruit abscission Polyamine S-Adenosyl methionine decarboxylase Spermidine synthase 

Abbreviations

ACC

1-Aminocyclopropane-1-carboxylic acid

ACO

1-Aminocyclopropane-1-carboxylic acid oxidase

ACS

1-Aminocyclopropane-1-carboxylic acid synthase

ADC

Arginine decarboxylase

ARB

Arbequina cultivar

AZ

Abscission zone

AZ–AC

Abscission zone and adjacent cells

Cad

Cadaverine

CHA

Cyclohexylamine

CLSM

Confocal laser scanning microscopy

dcSAM

Decarboxylated S-adenosylmethionine

DCFH2-DA

Dichlorodihydrofluorescein diacetate

DAO

Diamine oxidase

EIL

EIN3-like gene

ET

Ethylene

FDF

Fruit-detachment force

HomoSpd sym

Homospermidine

HSS

Homospermidine synthase

MACC

(Malonyl)-ACC

MGBG

Methylglyoxalbis(guanylhydrazone)

NO

Nitric oxide

OeACS2

Olea europaea ACS 2

OeEIL2

Olea europaea EIL 2

OeSAMDC1

Olea europaea SAMDC 1

OeSPDS1

Olea europaea SPDS 1

ODC

Ornithine decarboxylase

PA

Polyamine

PAO

Polyamine oxidase

PIC

Picual cultivar

Put

Putrescine

ROS

Reactive oxygen species

SAM

S-Adenosylmethionine

SAMDC

S-Adenosylmethionine decarboxylase

Spd

Spermidine

SPDS

Spermidine synthase

Spm

Spermine

SPMS

Spermine synthase

Supplementary material

425_2011_1570_MOESM1_ESM.tif (784 kb)
Supplementary material 1 (TIFF 783 kb)
425_2011_1570_MOESM2_ESM.tif (783 kb)
Supplementary material 2 (TIFF 782 kb)

References

  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  2. Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases ‘‘on the move’’: an update. Plant Physiol Biochem 48:560–564PubMedCrossRefGoogle Scholar
  3. Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plant. Amino Acids 20:301–317PubMedCrossRefGoogle Scholar
  4. Bennett EM, Ekstrom JL, Pegg AE, Ealick SE (2002) Monomeric S-adenosylmethionine decarboxylase from plants provides an alternative to putrescine stimulation. Biochemistry 41:14509–14517PubMedCrossRefGoogle Scholar
  5. Carbonell J, Blázquez MA (2009) Regulatory mechanisms of polyamine biosynthesis in plants. Genes Genom 31:107–118CrossRefGoogle Scholar
  6. Gomez-Jimenez MD, Garcıa-Olivares E, Matilla AJ (2001) 1-Aminocyclopropane-1-carboxylate oxidase from embryonic axes of germinating chick-pea (Cicer arietinum L.) seeds: cellular immunolocalization and alterations in its expression by indole-3-acetic acid, abscisic acid and spermine. Seed Sci Res 11:243–253Google Scholar
  7. Gomez-Jimenez MC, Paredes MA, Gallardo M, Fernandez-Garcia N, Olmos E, Sanchez-Calle IM (2010a) Tissue-specific expression of olive S-adenosyl methionine decarboxylase and spermidine synthase genes and polyamine metabolism during flower opening and early fruit development. Planta 232:629–647PubMedCrossRefGoogle Scholar
  8. Gomez-Jimenez MC, Paredes MA, Gallardo M, Sanchez-Calle IM (2010b) Mature fruit abscission is associated with upregulation of polyamine metabolism in the olive abscission zone. J Plant Physiol 167:1432–1441PubMedCrossRefGoogle Scholar
  9. Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546PubMedCrossRefGoogle Scholar
  10. Hu WW, Gong H, Pua EC (2005) Molecular cloning and characterization of S-adenosylmethionine decarboxylase genes from mustard (Brassica juncea). Plant Physiol 124:25–40CrossRefGoogle Scholar
  11. Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970PubMedCrossRefGoogle Scholar
  12. Kumar A, Taylor MA, Mad Arif SA, Davies HV (1996) Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J 9:147–158CrossRefGoogle Scholar
  13. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381PubMedCrossRefGoogle Scholar
  14. Locke JM, Bryce JH, Morris PC (2000) Contrasting effects of ethylene perception and biosynthesis inhibitors on germination and seedling growth of barley. J Exp Bot 51:1843–1849PubMedCrossRefGoogle Scholar
  15. Mattoo AK, Handa AK (2008) Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci 174:386–393CrossRefGoogle Scholar
  16. 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 38:405–413PubMedCrossRefGoogle Scholar
  17. 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 20:613–618PubMedCrossRefGoogle Scholar
  18. Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism. The state of the art. Plant Signal Behav 12:1061–1066CrossRefGoogle Scholar
  19. Muñoz de Rueda P, Gallardo M, Sanchez-Calle IM, Matilla AJ (1994) Germination of chikpea seeds in relation to manipulation of the ethylene pathway and polyamine biosynthesis by inhibitors. Plant Sci 97:31–37CrossRefGoogle Scholar
  20. 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 63:836–847PubMedCrossRefGoogle Scholar
  21. Ober D, Gibas L, Witte L, Hartmann T (2003) Evidence for general occurrence of homospermidine in plants and its supposed origin as by-product of deoxyhypusine synthase. Phytochemistry 62:339–344PubMedCrossRefGoogle Scholar
  22. Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosciences 25:291–299CrossRefGoogle Scholar
  23. Pang XM, Nada K, Liu JH, Kitashiba H, Honda C, Yamashita H, Tatsuki M, Moriguchi T (2006) Interrelationship between polyamine and ethylene in 1-methylcyclopropene treated apple fruits after harvest. Physiol Plant 128:351–359CrossRefGoogle Scholar
  24. Parra-Lobato MC, Gomez-Jimenez MC (2011) Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. J Exp Bot 62:4447–4465PubMedCrossRefGoogle Scholar
  25. 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 70:253–264PubMedCrossRefGoogle Scholar
  26. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007CrossRefGoogle Scholar
  27. Pieruzzi FP, Dias LLC, Balbuena TSl, Santa-Catarina C, dos Santos ALW, Floh EIS et al (2011) Polyamines, IAA and ABA during germination in two recalcitrant seeds: Araucaria angustifolia (Gymnosperm) and Ocotea odorifera (Angiosperm). Ann Bot 108:337–345PubMedCrossRefGoogle Scholar
  28. Quin WM, Lan WZ (2004) Fungal elicitor-induced cell death in Taxus chinensis suspension cells is mediated by ethylene and polyamines. Plant Sci 166:989–995CrossRefGoogle Scholar
  29. Sakamoto M, Munemura I, Tomita R, Kobayashi K (2008) Involvement of hydrogen peroxide in leaf abscission signaling, revealed by analysis with an in vitro abscission system in Capsicum plants. Plant J 56:13–27PubMedCrossRefGoogle Scholar
  30. Shao L, Majumdar R, Minocha SC (2011) Profiling the aminopropyltransferases in plants: their structure, expression and manipulation. Amino Acids. doi:10.1007/s00726-011-0998-8
  31. Sobieszczuk-Nowicka E, Rorat T, Legota J (2007) Polyamine metabolism and S-adenosylmethionine decarboxylase gene expression during the cytokinin-stimulated greening process. Acta Physiol Plant 29:495–502CrossRefGoogle Scholar
  32. Srivastava A, Chung SH, Fatima T, Datsenka T, Handa AK, Mattoo AK (2007) Polyamines as anabolic growth regulators revealed by transcriptome analysis and metabolite profiles of tomato fruits engineered to accumulate spermidine and spermine. Plant Biotechnol 24:57–70CrossRefGoogle Scholar
  33. Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6PubMedCrossRefGoogle Scholar
  34. Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2011) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids. doi:10.1007/s00726-011-1012-1
  35. Tiburcio AF, Altabella T, Borrell A, Masgrau C et al (1997) Polyamine metabolism and its regulation titers. Transgenic Res 17:251–263Google Scholar
  36. Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926CrossRefGoogle Scholar
  37. Wang Q, Yuan G, Sun H, Zhao P, Liu Y, Guo D (2005) Molecular cloning and expression analysis and spermidine synthase gene during sex reversal induced by Ethrel in cucumber (Cucumis sativus L.). Plant Sci 169:768–775CrossRefGoogle Scholar
  38. Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliate confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot 62:2899–2914PubMedCrossRefGoogle Scholar
  39. 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. Physiol Plant 100:664–674Google Scholar
  40. Wi SJ, Park KY (2002) Antisense expression of carnation cDNA encoding ACC synthase or ACC oxidase enhances polyamine content and abiotic stress tolerance in transgenic tobacco plants. Mol Cells 13:209–220PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Plant PhysiologyUniversity of ExtremaduraBadajozSpain

Personalised recommendations