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.
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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
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
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
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
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
Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199
Buchanan-Wollaston V (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotech J 1:3–22
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
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
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
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
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
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
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
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
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
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
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
Hashimoto H, Yamamoto KT (1998) Isolation and expression of an elongation-dependent gene of mung bean (Vigna radiata) hypocotyls. Physiol Plant 106:224–231
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
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
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
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
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
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
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
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
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
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
Llop Tous I, Barry CS, Grierson D (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol 123:971–978
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
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
Nam HG (1997) The molecular genetic analysis of leaf senescence. Curr Opin Biotechnol 8:200–207
Noh YS, Amasino RM (1999a) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194
Noh YS, Amasino RM (1999b) Regulation of developmental senescence is conserved between Arabidopsis and Brassica napus. Plant Mol Biol 41:195–206
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
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
Robatzek S, Somssich IE (2002) Targets of AtWRKY regulation during plant senescence and pathogen defence. Genes Dev 16:1139–1149
Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223
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
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
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
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
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
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
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
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
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
Wiedemeyer R, Westermann F, Wittke I, Nowock J, Schwab M (2003) Ataxin-2 promotes apoptosis of human neuroblastoma cells. Oncogene 22:401–411
Wilker E, Yaffe MB (2004) 14-3-3 proteins—a focus on cancer and human disease. J Mol Cell Cardiol 37:633–642
Winkenbach F (1970) Zum Stoffwechsel der aufblühenden und welkenden Korolle der Prunkwinde Ipomoea purpurea. Ber schweiz bot Gesellsch 80:374–390
Xu FX, Chye ML (1999) Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J 17:321–327
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
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
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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
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DOI: https://doi.org/10.1007/s00299-006-0285-4
Keywords
- Actinomycin D
- DNA degradation
- Nuclear fragmentation
- Petal senescence
- Programmed cell death
- Senescence-associated genes