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Expression of polyamine biosynthesis genes during parthenocarpic fruit development in Citrus clementina

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Abstract

Polyamines have been attributed a general role in fruit development in several plants like pea and tomato. To investigate the involvement of these compounds in parthenocarpic fruit development in Citrus clementina, we have isolated three genes encoding aminopropyl transferases in this species: CcSPDS, CcSPM1 and CcACL5. The unambiguous identity of the proteins encoded by these genes was confirmed by phylogenetic analysis and by heterologous expression in yeast mutants deficient in aminopropyl transferase activity. The expression of these genes in C. clementina is not restricted to ovaries and fruits, but it is also detectable all throughout the plant. More importantly, gibberellin-induced parthenocarpic fruit set caused a decrease in CcSPDS expression in ovaries, paralleled by a decrease in spermidine; while the expression of CcSPM1 and CcACL5 was basically unaffected, resulting in the maintenance of spermine concentration during early fruit development. In addition, the variation in putrescine content was paralleled by changes in the expression of one of the two putative CcODC paralogs.

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Abbreviations

PAs:

Polyamines

Put:

Putrescine

Spd:

Spermidine

Spm:

Spermine

Syn:

Synefrine

Tspm:

Thermospermine

Tyr:

Tyramine

M-Tyr:

Methyl-tyramine

References

  • Acosta C, Perez-Amador MA, Carbonell J, Granell A (2005) The two ways to produce putrescine in tomato are cell-specific during normal development. Plant Sci 168:1053–1057

    Article  CAS  Google Scholar 

  • Alabadí D, Carbonell J (1999) Differential expression of two spermidine synthase genes during early fruit development and in vegetative tissues of pea. Plant Mol Biol 39:933–943

    Article  PubMed  Google Scholar 

  • Alabadí D, Aguero MS, Perez-Amador MA, Carbonell J (1996) Arginase, arginine decarboxylase, ornithine decarboxylase, and polyamines in tomato ovaries (changes in unpollinated ovaries and parthenocarpic fruits induced by auxin or gibberellin). Plant Physiol 112:1237–1244

    PubMed  Google Scholar 

  • Alcázar R, Cuevas JC, Patrón M, Altabella T, Tiburcio AF (2006) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455

    Article  CAS  Google Scholar 

  • Arias M, Carbonell J, Agustí M (2005) Endogenous free polyamines and their role in fruit set of low and high parthenocarpic ability citrus cultivars. J Plant Physiol 162:845–853

    Article  CAS  PubMed  Google Scholar 

  • Bagni N, Torrigiani P (1992) Polyamines: a new class of growth substances. In: Karssen CM, Van Loon LC, Vreugdenhil D (eds) Progress in plant growth regulation. Kluwer, Dordrecht, pp 264–275

    Google Scholar 

  • Bellés JM, Carbonell J, Conejero V (1991) Polyamines in plants infected by citrus exocortis viroid or treated with silver ions and etephon. Plant Physiol 96:1053–1059

    Article  PubMed  Google Scholar 

  • Biasi R, Bagni N, Costa G (1988) Endogenous polyamines in apple and their relationship to fruit set and fruit growth. Physiol Plant 73:201–205

    Article  CAS  Google Scholar 

  • Carbonell J, Blázquez MA (2009) Regulatory mechanisms of polyamine biosynthesis in plants. Genes Genomics 31:107–118

    Article  CAS  Google Scholar 

  • Carbonell J, Navarro JL (1989) Correlation of spermine levels with ovary senescence and with fruit set and development in Pisum sativum L. Planta 178:482–487

    Article  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  CAS  PubMed  Google Scholar 

  • Egea-Corines M, Cohen E, Arad S, Bagni N, Mizrahi Y (1993) Polyamine levels in pollinated and auxin-induced fruit of tomato (Lycopersicon esculentum) during development. Physiol Plant 87:14–20

    Article  Google Scholar 

  • El-Otmani M, Coggins CW, Agusti J, Lovatt CJ (2000) Plant growth regulators in citriculture: world current uses. Crit Rev Plant Sci 19:395–447

    Article  CAS  Google Scholar 

  • Forment J, Gadea J, Huerta L, Abizanda L, Agustí J, Alamar S, Alós E, Andrés F, Arribas R, Beltrán JP, Berbel A, Blázquez MA, Brumós J, Cañas LA, Cercós M, Colmenero-Flores JM, Conesa A, Estables B, Gandía M, García-Martínez JL, Gimeno J, Gisbert A, Gómez G, González-Candelas L, Granell A, Guerri J, Lafuente MT, Madueño F, Marcos JF, Marqués MC, Martínez F, Martínez-Godoy MA, Miralles S, Moreno P, Navarro L, Pallás V, Perez-Amador MA, Pérez-Valle J, Pons C, Rodrigo I, Rodríguez PL, Royo C, Serrano R, Soler G, Tadeo F, Talón M, Terol J, Trénor M, Vaello L, Vicente O, Vidal C, Zacarías L, Conejero V (2005) Development of a citrus genome-wide EST collection and cDNA microarray as resources for genomic studies. Plant Mol Biol 57:375–391

    Article  CAS  PubMed  Google Scholar 

  • Fos M, Proaño K, Alabadí D, Nuez F, Carbonell J, García-Martínez JL (2003) Polyamine metabolism is altered in unpollinated parthenocarpic pat-2 tomato ovaries. Plant Physiol 131:359–366

    Article  CAS  PubMed  Google Scholar 

  • Fraga MF, Berdasco M, Diego LB, Rodríguez R, Cañal MJ (2004) Changes in polyamine concentration associated with aging in Pinus radiata and Prunus persica. Tree Physiol 24:1221–1226

    CAS  PubMed  Google Scholar 

  • Galston AW (1983) Polyamines as modulators of plant development. Bioscience 33:382–388

    Article  CAS  Google Scholar 

  • Gietz RD, Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534

    Article  CAS  PubMed  Google Scholar 

  • Gimeno J, Gadea J, Forment J, Pérez-Valle J, Santiago J, Martínez-Godoy MA, Yenush L, Bellés JM, Brumós J, Colmenero-Flores JM, Talón M, Serrano R (2009) Shared and novel molecular responses of mandarin to drought. Plant Mol Biol 70:403–420

    Article  CAS  PubMed  Google Scholar 

  • Guillet G, De Luca V (2005) Wound-inducible biosynthesis of phytoalexin hydroxycinnamic acid amides of tyramine in tryptophan and tyrosine decarboxylase transgenic tobacco lines. Plant Physiol 137:692–699

    Article  CAS  PubMed  Google Scholar 

  • Hamasaki-Katagiri N, Tabor CW, Tabor H (1997) Spermidine biosynthesis in Saccharomyces cerevisae: polyamine requirement of a null mutant of the SPE3 gene (spermidine synthase). Gene 187:35–43

    Article  CAS  PubMed  Google Scholar 

  • Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210:195–201

    Article  CAS  PubMed  Google Scholar 

  • Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Piñeiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256

    Article  CAS  PubMed  Google Scholar 

  • Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T (2002) Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 527:176–180

    Article  CAS  PubMed  Google Scholar 

  • Hao YJ, Zhang Z, Kitashiba H, Honda C, Ubi B, Kita M, Moriguchi T (2005) Molecular cloning and functional characterization of two apple S-adenosylmethionine decarboxylase genes and their different expression in fruit development, cell growth and stress responses. Gene 350:41–50

    Article  CAS  PubMed  Google Scholar 

  • Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573

    Article  CAS  PubMed  Google Scholar 

  • Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kasukabe Y, He L, 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

    Article  CAS  PubMed  Google Scholar 

  • Kitashiba H, Hao YJ, Honda C, Moriguchi T (2005) Two types of spermine synthase gene: MdACL5 and MdSPMS are differentially involved in apple fruit development and cell growth. Gene 361:101–111

    Article  CAS  PubMed  Google Scholar 

  • Knott JM, Romer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086

    Article  CAS  PubMed  Google Scholar 

  • Korolev S, Ikeguchi Y, Skarina T, Beasley S, Arrowsmith C, Edwards A, Joachimiak A, Pegg AE, Savchenko A (2002) The crystal structure of spermidine synthase with a multisubstrate adduct inhibitor. Nat Struct Biol 9:27–31

    Article  CAS  PubMed  Google Scholar 

  • Kushad MM, Ovros AR, Yelenosky G (1990) Relative changes in polyamine during citrus flower development. HortScience 25:946–948

    CAS  Google Scholar 

  • Mann JD, Steinhart CE, Mudd SH (1963) Alkaloids and plant metabolism. V. The distribution and formation of tyramine methylpherase during germination of barley. J Biol Chem 238:676–681

    CAS  Google Scholar 

  • Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blázquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128

    Article  CAS  PubMed  Google Scholar 

  • Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–2582

    Article  PubMed  CAS  Google Scholar 

  • Nathan R, Altman A, Monselise SP (1984) Changes in activity of polyamine biosynthetic enzymes and in polyamine contents in develo** fruit tissues of ‘Murcot’ mandarin. Sci Hortic 22:359–364

    Article  CAS  Google Scholar 

  • Navas MA, Cerdan S, Gancedo JM (1993) Futile cycles in Saccharomyces cerevisiae strains expressing the gluconeogenic enzymes during growth on glucose. Proc Natl Acad Sci USA 90:1290–1294

    Article  CAS  PubMed  Google Scholar 

  • Oshima T (1979) A new polyamine, thermospermine, 1,12-diamino-4,8-diazadodecane, from an extreme thermophile. J Biol Chem 254:8720–8722

    CAS  PubMed  Google Scholar 

  • Panicot M, Minguet EG, Ferrando A, Alcázar R, Blázquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14:2539–2551

    Article  CAS  PubMed  Google Scholar 

  • Perez-Amador MA, Carbonell J (1995) Arginine decarboxylase and putrescine oxidase in ovaries of Pisum sativum L. (changes during ovary senescence and early stages of fruit development). Plant Physiol 107:865–872

    CAS  PubMed  Google Scholar 

  • Rambla JL, Vera-Sirera F, Blázquez MA, Carbonell J, Granell A (2010) Quantitation of biogenic tetraamines in Arabidopsis thaliana. Anal Biochem 397:208–211

    Article  CAS  PubMed  Google Scholar 

  • Rández-Gil F, Prieto J, Murcia A, Sanz P (1995) Construction of baker’s yeast strains that secrete Aspergillus oryzae α-amylase and their use in bread making. J Cereal Sci 21:185–193

    Article  Google Scholar 

  • Rodríguez AA, Maiale SJ, Menéndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262

    Article  PubMed  CAS  Google Scholar 

  • Saftner RA, Baldi BG (1990) Polyamine levels and tomato fruit development: possible interaction with ethylene. Plant Physiol 92:547–550

    Article  CAS  PubMed  Google Scholar 

  • Smith TA (1985) Polyamines. Annu Rev Plant Biol 36:117–143

    Article  CAS  Google Scholar 

  • Talón M, Zacarías L, Primo-Millo E (1990a) Gibberellins in Citrus sinensis: a comparison between seeded and seedless varieties. J Plant Growth Reg 9:201–206

    Article  Google Scholar 

  • Talón M, Zacarías L, Primo-Millo E (1990b) Hormonal changes associated with fruit set and development in mandarins differing in their parthenocarpic ability. Physiol Plant 79:400–406

    Article  Google Scholar 

  • Talón M, Zacarías L, Primo-Millo E (1992) Gibberellins and parthenocarpic ability in develo** ovaries of seedless mandarins. Plant Physiol 99:1575–1581

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J (2010) Role of polyamines in plant vascular development. Plant Physiol Biochem. doi:10.1016/j.plaphy.2010.01.011

  • Wheaton TA, Stewart I (1970) The distribution of tyramine, N-methyltyramine, hordenine, octopamine, and synephrine in higher plants. Lloydia 33:244–254

    CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Honda C, Kita M, Hu C, Nakayama M, Moriguchi T (2003) Structure and expression of spermidine synthase genes in apple: two cDNAs are spatially and developmentally regulated through alternative splicing. Mol Genet Genomics 268:799–807

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank F. Tadeo and M. Talón (IVIA, Valencia, Spain) for their valuable advice on Citrus biology and for providing us with the trees used in this study. We also appreciate the technical help of Mª Angeles Argomániz and helpful discussions with D. Alabadí (IBMCP, Valencia, Spain). This work was funded by the Generalitat Valenciana and the Spanish Ministry of Education and Science (GEN2001-4885-C05).

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Authors and Affiliations

  1. Instituto de Biología Molecular y Celular de Plantas (CSIC-UPV), Universidad Politécnica de Valencia, Ingeniero Fausto Elio s/n, 46022, Valencia, Spain

    Marta Trénor, Miguel A. Perez-Amador, Juan Carbonell & Miguel A. Blázquez

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  1. Marta Trénor
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  2. Miguel A. Perez-Amador
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  3. Juan Carbonell
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  4. Miguel A. Blázquez
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Correspondence to Miguel A. Blázquez.

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Trénor, M., Perez-Amador, M.A., Carbonell, J. et al. Expression of polyamine biosynthesis genes during parthenocarpic fruit development in Citrus clementina . Planta 231, 1401–1411 (2010). https://doi.org/10.1007/s00425-010-1141-x

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