Skip to main content
Log in

Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers

  • Genetics and Genomics
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

We isolated several senescence-associated genes (SAGs) from the petals of morning glory (Ipomoea nil) flowers, with the aim of furthering our understanding of programmed cell death. Samples were taken from the closed bud stage to advanced visible senescence. Actinomycin D, an inhibitor of transcription, if given prior to 4 h after opening, suppressed the onset of visible senescence, which occurred at about 9 h after flower opening. The isolated genes all showed upregulation. Two cell-wall related genes were upregulated early, one encoding an extensin and one a caffeoyl-CoA-3-O-methyltransferase, involved in lignin production. A pectinacetylesterase was upregulated after flower opening and might be involved in cell-wall degradation. Some identified genes showed high homology with published SAGs possibly involved in remobilisation processes: an alcohol dehydrogenase and three cysteine proteases. One transcript encoded a leucine-rich repeat receptor protein kinase, putatively involved in signal transduction. Another transcript encoded a 14-3-3 protein, also a protein kinase. Two genes have apparently not been associated previously with senescence: the first encoded a putative SEC14, which is required for Golgi vesicle transport, the second was a putative ataxin-2, which has been related to RNA metabolism. Induction of the latter has been shown to result in cell death in yeast, due to defects in actin filament formation. The possible roles of these genes in programmed cell death are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ActD:

Actinomycin D

ADH:

Alcohol dehydrogenase

DAPI:

4,6-Diamino-2-phenylindole

HR:

Hypersensitive response

LTP:

Lipid transfer protein

PCD:

Programmed cell death

RACE:

Rapid amplification of cDNA ends

SAG:

Senescence-associated gene

SCA2:

Spinocerebellar ataxia type 2

References

  • Baumgartner B, Kende H, Matile P (1975) Ribonuclease in senescing morning glory. Plant Physiol 55:734–737

    Article  PubMed  CAS  Google Scholar 

  • Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960

    Article  PubMed  CAS  Google Scholar 

  • Blein JP, Coutos Thevenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signaling involved in plant defense mechanisms. Trends Plant Sci 7:293–296

    Article  PubMed  CAS  Google Scholar 

  • Bravo J, Aguilar-Henonin L, Olmedo G, Guzman P (2005) Four distinct classes of proteins as interaction partners of the PABC domain of Arabidopsis thaliana poly(A)-binding proteins. Mol Genet Genom 272:651–665

    Article  CAS  Google Scholar 

  • Breeze E, Wagstaff C, Harrison E, Bramke I, Rogers H, Stead A, Thomas B, Buchanan-Wollaston V (2004) Gene expression patterns to define stages of post-harvest senescence in Alstroemeria petals. Plant Biotech J 2:155–168

    Article  CAS  Google Scholar 

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199

    Article  Google Scholar 

  • Buchanan-Wollaston V (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotech J 1:3–22

    Article  CAS  Google Scholar 

  • Busam G, Junghanns KT, Kneusel RE, Kassemeyer HH, Matern U (1997) Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L. Plant Physiol 115:1039–1048

    Article  PubMed  CAS  Google Scholar 

  • Chen GH, Huang LT, Yap MN, Lee RH, Huang YJ, Cheng MC, Chen SC (2002) Molecular characterization of a senescence-associated gene encoding cysteine proteinase and its gene expression during leaf senescence in sweet potato. Plant Cell Physiol 43:984–991

    Article  PubMed  CAS  Google Scholar 

  • Cleves AE, McGee TP, Whitters EA, Champion KM, Aitken JR, Dowhan W, Goebl M, Bankaitis VA (1991) Mutations in the CDP-choline pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein. Cell 64:789–800

    Article  PubMed  CAS  Google Scholar 

  • Coupe SA, Sinclair BK, Watson LM, Heyes JA, Eason JR (2003) Identification of dehydration-responsive cysteine proteases during post-harvest senescence of broccoli florets. J Exp Bot 54:1045–1056

    Article  PubMed  CAS  Google Scholar 

  • Eason JR, Ryan DJ, Pinkney TT, O’Donoghue EM (2002) Programmed cell death during flower senescence: isolation and characterization of cysteine proteinases from Sandersonia aurantiaca. Funct Plant Biol 29:1055–1064

    Article  CAS  Google Scholar 

  • Eason JR, Ryan DJ, Watson LM, Hedderley D, Christey MC, Braun RH, Coupe SA (2005) Suppression of the cysteine protease, aleurain, delays floret senescence in Brassica oleracea. Plant Mol Biol 57:645–657

    Article  PubMed  CAS  Google Scholar 

  • Garabagi F, Duns G, Strommer J (2005) Selective recruitment of Adh genes for distinct enzymatic functions in Petunia hydrida. Plant Mol Biol 58:283–294

    Article  PubMed  CAS  Google Scholar 

  • Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MF, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J 36:629–642

    Article  PubMed  CAS  Google Scholar 

  • Godiard L, Sauviac L, Dalbin N, Liaubet L, Callard D, Czernic P, Marco Y (1998) CYP76C2, an Arabidopsis thaliana cytochrome P450 gene expressed during hypersensitive and developmental cell death. FEBS Lett 438:245–249

    Article  PubMed  CAS  Google Scholar 

  • Guerrero C, de la Calle M, Reid MS, Valpuesta V (1998) Analysis of the expression of two thiolprotease genes from daylily (Hemerocallis spp.) during flower senescence. Plant Mol Biol 36:565–571

    Article  PubMed  CAS  Google Scholar 

  • Hara M, Kumagai K, Kuboi T (2002) Characterization and expression of a water stress responsive gene from a seashore plant Calystegia soldanella. Plant Biotech 19:277–281

    CAS  Google Scholar 

  • Hashimoto H, Yamamoto KT (1998) Isolation and expression of an elongation-dependent gene of mung bean (Vigna radiata) hypocotyls. Physiol Plant 106:224–231

    Article  Google Scholar 

  • Hayden DM, Christopher DA (2004) Characterization of senescence-associated gene expression and senescence-dependent and -independent cysteine proteases differing in microsomal processing in Anthurium. Plant Sci 166:779–790

    Article  CAS  Google Scholar 

  • Henneberry AL, Lagace TA, Ridgway ND, McMaster CR (2001) Phosphatidylcholine synthesis influences the diacylglycerol homeostasis required for SEC14p-dependent Golgi function and cell growth. Mol Biol Cell 12:511–520

    PubMed  CAS  Google Scholar 

  • Hunter DA, Steele BC, Reid MS (2002) Identification of genes associated with perianth senescence in Daffodil (Narcissus pseudonarcissus L. ‘Dutch Master’. Plant Sci 163:13–21

    Article  CAS  Google Scholar 

  • Huynh DP, Yang HT, Vakharia H, Nguyen D, Pulst SM (2003) Expansion of the polyQ repeat in ataxin-2 alters its Golgi localization, disrupts the Golgi complex and causes cell death. Hum Mol Genet 12:1485–1496

    Article  PubMed  CAS  Google Scholar 

  • Ibdah M, Zhang XH, Schmidt J, Vogt T (2003) A novel Mg2+-dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. J Biol Chem 278:43961–43972

    Article  PubMed  CAS  Google Scholar 

  • Jones ML, Larsen PB, Woodson WR (1995) Ethylene-regulated expression of a carnation cysteine proteinase during flower petal senescence. Plant Mol Biol 28:505–512

    Article  PubMed  CAS  Google Scholar 

  • Jones ML (2004) Changes in gene expression during senescence. In: Noodén LD (ed) Plant cell death processes. Academic, pp 51–71

  • Kende H, Baumgartner B (1974) Regulation of aging in flowers of Ipomoea tricolor by ethylene. Planta 116:279–289

    Article  CAS  Google Scholar 

  • Koizumi M, Yamaguchi Shinozaki K, Tsuji H, Shinozaki K (1993) Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129:175–182

    Article  PubMed  CAS  Google Scholar 

  • Lapointe G, Luckevich MD, Cloutier M, Seguin A (2001) 14-3-3 gene family in hybrid poplar and its involvement in tree defence against pathogens. J Exp Bot 52:1331–1338

    Article  PubMed  CAS  Google Scholar 

  • Liu HC, Creech RG, Jenkins JN, Ma DP (2000) Cloning and promoter analysis of the cotton lipid transfer protein gene Ltp3(1). Biochim Biophys Acta 1487:106–111

    PubMed  CAS  Google Scholar 

  • Llop Tous I, Barry CS, Grierson D (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol 123:971–978

    Article  PubMed  CAS  Google Scholar 

  • Matile P, Winkenbach F (1971) Function of lysosomes and lysosomal enzymes in the senescing corolla of the morning glory (Ipomoea purpurea). J Exp Bot 22:759–771

    Article  CAS  Google Scholar 

  • Merkouropoulos G, Shirsat AH (2003) The unusual Arabidopsis extensin gene atExt1 is expressed throughout plant development and is induced by a variety of biotic and abiotic stresses. Planta 217:356–366

    Article  PubMed  CAS  Google Scholar 

  • Nam HG (1997) The molecular genetic analysis of leaf senescence. Curr Opin Biotechnol 8:200–207

    Article  PubMed  CAS  Google Scholar 

  • Noh YS, Amasino RM (1999a) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194

    Article  PubMed  CAS  Google Scholar 

  • Noh YS, Amasino RM (1999b) Regulation of developmental senescence is conserved between Arabidopsis and Brassica napus. Plant Mol Biol 41:195–206

    Article  PubMed  CAS  Google Scholar 

  • Pakusch AE, Kneusel RE, Matern U (1989) S-adenosyl-L-methionine: trans-caffeoyl-coenzyme A 3-O-methyltransferase from elicitor-treated parsley cell suspension cultures. Arch Biochem Biophys 271:488–494

    Article  PubMed  CAS  Google Scholar 

  • Panavas T, Pikula A, Reid PD, Rubinstein B, Walker EL (1999) Identification of senescence-associated genes from daylily petals. Plant Mol Biol 40:237–248

    Article  PubMed  CAS  Google Scholar 

  • Robatzek S, Somssich IE (2002) Targets of AtWRKY regulation during plant senescence and pathogen defence. Genes Dev 16:1139–1149

    Article  PubMed  CAS  Google Scholar 

  • Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223

    Article  PubMed  CAS  Google Scholar 

  • Satterfield TF, Jackson SM, Pallanck LJ (2002) A Drosophila homolog of the polyglutamate disease gene SCA2 is a dosage dependent regulator of actin filament formation. Genetics 162:1687–1702

    PubMed  CAS  Google Scholar 

  • Schmitt D, Pakusch AE, Matern U (1991) Molecular cloning, induction and taxonomic distribution of caffeoyl-CoA 3-O-methyltransferase, an enzyme involved in disease resistance. J Biol Chem 266:17416–17423

    PubMed  CAS  Google Scholar 

  • Smith MT, Saks Y, van Staden J (1992) Ultrastructural changes in the petals of senescing flowers of Dianthus caryophyllus L. Ann Bot 69:277–285

    Google Scholar 

  • Sreenivasulu N, Radchuk V, Stricjert M, Miersch O, Weschke W, Wobus U. (2006) Gene expression patterns reveal tissue-specific networks controlling programmed cell death and ABA-regulated maturation in barley seeds. Plant J 47:310–327

    Article  PubMed  CAS  Google Scholar 

  • Takemoto D, Yoshioka H, Doke N, Kawakita K (2003) Disease stress-inducible genes of tobacco: expression profile of elicitor-responsive genes isolated by subtractive hybridization. Physiol Plant 118:545–553

    Article  CAS  Google Scholar 

  • Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174:221–229

    Article  PubMed  CAS  Google Scholar 

  • van Doorn WG, Balk PA, van Houwelingen AM, Hoeberichts FA, Hall RD, Vorst O, Van Der Schoot C, van Wordragen MF (2003) Gene expression during anthesis and senescence in Iris flowers. Plant Mol Biol 53:845–863

    Article  PubMed  CAS  Google Scholar 

  • Wagstaff C, Leverentz MK, Griffiths G, Thomas B, Chanasut U, Stead AD, Rogers HJ (2002) Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals. J Exp Bot 53:233–240

    Article  PubMed  CAS  Google Scholar 

  • Wagstaff C, Malcolm P, Rafiq A, Leverentz M, Griffiths G, Thomas B, Stead A, Rogers H (2003) Programmed cell death (PCD) processes begin extremely early in Alstroemeria petal senescence. New Phytol 160:49–59

    Article  CAS  Google Scholar 

  • Wiedemeyer R, Westermann F, Wittke I, Nowock J, Schwab M (2003) Ataxin-2 promotes apoptosis of human neuroblastoma cells. Oncogene 22:401–411

    Article  PubMed  CAS  Google Scholar 

  • Wilker E, Yaffe MB (2004) 14-3-3 proteins—a focus on cancer and human disease. J Mol Cell Cardiol 37:633–642

    Article  PubMed  CAS  Google Scholar 

  • Winkenbach F (1970) Zum Stoffwechsel der aufblühenden und welkenden Korolle der Prunkwinde Ipomoea purpurea. Ber schweiz bot Gesellsch 80:374–390

    Google Scholar 

  • Xu FX, Chye ML (1999) Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J 17:321–327

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Takatsu Y, Kasumi M, Ichimura K, van Doorn WG (2006) Nuclear fragmentation and DNA degradation during programmed cell death in petals of morning glory (Ipomoea nil). Planta 224:1279–1290

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell Physiol 42:451–461

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tetsuya Yamada.

Additional information

Communicated by R. Schmidt

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamada, T., Ichimura, K., Kanekatsu, M. et al. Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers. Plant Cell Rep 26, 823–835 (2007). https://doi.org/10.1007/s00299-006-0285-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-006-0285-4

Keywords

Navigation