Skip to main content
SpringerLink
Log in

Local induction of senescence by darkness in Cucurbita pepo (zucchini) cotyledons or the primary leaf induces opposite effects in the adjacent illuminated organ

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Local darkening of zucchini cotyledons or the primary leaf affected in an organ-specific manner the adjacent ones which remained under the initial light regime. Individual darkening of either the pair of cotyledons or the primary leaf led to acceleration of senescence expressed by lowering of chlorophyll content and net photosynthetic rate. Darkening of the pair of cotyledons induced a reduction in total cytokinin (CK) levels and increased CK oxidase/dehydrogenase (CKX) activity in the adjacent illuminated primary leaf. In addition, abscisic acid (ABA) content was increased which correlated with reduced stomatal aperture leading to decreased stomatal conductance and transpiration rate. In contrast, darkening of the adjacent primary leaf led to increased metabolic activity in the illuminated cotyledons including increased total CK levels in parallel with decreased CKX activity, decreased ABA content in correlation with increased stomatal aperture, stomatal conductance and transpiration rate. On the other hand, the functional activity of the photosynthetic apparatus as well as the transcript levels of the three photosynthesis-related genes psbA, psaB and rbcL remained almost unaffected in both illuminated organs. Thus, compared with the primary leaves, cotyledons appeared to be much more resistant to the dark stress applied either directly or to the adjacent primary leaf. Our results indicated the involvement of CKs and ABA signalling in the control of the communication mechanisms between cotyledons and the primary leaf that could operate in response to changing environmental factors like shading during earlier stages of plant development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CK:

Cytokinin

cisZ:

cis-Zeatin

cisZR:

cis-Zeatin riboside

CKX:

Cytokinin oxidase/dehydrogenase

DHZ:

Dihydrozeatin

DHZR:

Dihydrozeatin 9-riboside

DHZ7G:

Dihydrozeatin 7-glucoside

DHZ9G:

Dihydrozeatin 9-glucoside

DHZROG:

Dihydrozeatin 9-riboside O-glucoside

DHZRMP:

Dihydrozeatin 9-riboside-5′-monophosphate

IAA:

Indole-3-acetic acid

iP:

N6-(2-isopentenyl)adenine

iPR:

N6-(2-isopentenyl)adenine 9-riboside

iP7G:

N6-(2-isopentenyl)adenine 7-glucoside

iP9G:

N6-(2-isopentenyl)adenine 9-glucoside

iPRMP:

N6-(2-isopentenyl)adenine 9-riboside-5′-monophosphate

PSII:

Photosystem II

psaB :

A gene coding for PSI apoprotein PsaB

psbA :

A gene coding for D1 protein of PSII reaction center

rbcL :

A gene coding for the large subunit of Rubisco

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SAGs:

Senescence-associated genes

Z:

trans-Zeatin

ZR:

trans-Zeatin 9-riboside

Z7G:

trans-Zeatin 7-glucoside

Z9G:

trans-Zeatin 9-glucoside

ZOG:

trans-Zeatin O-glucoside

ZROG:

trans-Zeatin 9-riboside O-glucoside

ZRMP:

trans-Zeatin 9-riboside-5′-monophosphate (abbreviations for cytokinins according to Kamínek et al. 2000)

References

  • Ananieva K, Malbeck J, Kamínek M, Van Staden J (2004) Changes in endogenous cytokinin levels in cotyledons of Cucurbita pepo (zucchini) during natural and dark-induced senescence. Physiol Plant 122:133–142

    Article  CAS  Google Scholar 

  • Ananieva K, Ananiev ED, Doncheva S, Georgieva K, Tzvetkova N, Kamínek M, Motyka V, Dobrev P, Gajdošová S, Malbeck J (2008) Senescence progression in a single darkened cotyledon depends on the light status of the other cotyledon in Cucurbita pepo (zucchini) seedlings: potential involvement of cytokinins and cytokinin oxidase/dehydrogenase activity. Physiol Plant 134:609–623

    Article  PubMed  CAS  Google Scholar 

  • Armstrong D (1994) Cytokinin oxidase and the regulation of cytokinin degradation. In: Mok DWS, Mok MC (eds) Cytokinins: chemistry, activity and function. CRC Press, Boca Raton, pp 139–154

    Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem. II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Biswal UC, Biswal B (1984) Photocontrol of leaf senescence. Photochem Photobiol 39:875–879

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  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, Page T, Harrison E, Breeze E, Lim P, Nam H, Lin J-F, Wu S-H, Swidzinski J, Ishazaki K, Leaver C (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  PubMed  CAS  Google Scholar 

  • Chatfield JM, Armstrong DJ (1986) Regulation of cytokinin oxidase activity in callus tissues of Phaseolus vulgaris L. cv Great Northern. Plant Physiol 80:493–499

    Article  PubMed  CAS  Google Scholar 

  • Chen Zh, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162

    Article  PubMed  CAS  Google Scholar 

  • Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174

    Article  PubMed  CAS  Google Scholar 

  • Conrad K, Motyka V, Schlüter T (2007) Increase in activity, glycosylation and expression of cytokinin oxidase/dehydrogenase during the senescence of barley leaf segments in the dark. Physiol Plant 130:572–579

    Article  CAS  Google Scholar 

  • Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29

    Article  PubMed  Google Scholar 

  • Dobrev PI, Havlíček L, Vágner M, Malbeck J, Kamínek M (2005) Purification and determination of plant hormones auxin and abscisic acid using solid phase extraction and two-dimensional high performance liquid chromatography. J Chromatogr A 1075:159–166

    Article  PubMed  CAS  Google Scholar 

  • Gan S (2004) The hormonal regulation of leaf senescence. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction and action. Kluwer, Dordrecht, pp 561–581

    Google Scholar 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1966–1970

    Article  Google Scholar 

  • Gan S, Amasino RM (1996) Cytokinins in plant senescence from spray and pray to clone and play. Bioessays 18:557–565

    Article  CAS  Google Scholar 

  • Gaudinová A, Dobrev PI, Šolcová B, Novák O, Strnad M, Friedecký D, Motyka V (2005) The involvement of cytokinin oxidase/dehydrogenase and zeatin reductase in regulation of cytokinin levels in pea (Pisum sativum L.) leaves. J Plant Growth Regul 24:188–200

    Article  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Hare PD, Van Staden J (1994) Cytokinin oxidase: biochemical features and physiological significance. Physiol Plant 91:128–136

    Article  CAS  Google Scholar 

  • Havlova M, Dobrev P, Motyka V, Štorchová H, Libus J, Dobrá J, Malbeck J, Gaudinová A, Vaňková R (2008) The role of cytokinins in responses to water deficit in tobacco plants. Plant Cell Environ 31:341–353

    Article  PubMed  CAS  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485

    Article  PubMed  CAS  Google Scholar 

  • Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43

    Article  PubMed  CAS  Google Scholar 

  • Kamínek M, Pačes V, Corse J, Challice JSD (1979) The effect of stereospecific hydroxylation of N6-(Δ2-isopentenyl)adenosine on cytokinin activity. Planta 145:239–245

    Article  Google Scholar 

  • Kamínek M, Motyka V, Vaňková R (1997) Regulation of cytokinin content in plant cells. Physiol Plant 101:689–700

    Article  Google Scholar 

  • Kamínek M, Březinová A, Gaudinová A, Motyka V, Vaňková R, Zažímalová E (2000) Purine cytokinins: a proposal of abbreviations. Plant Growth Regul 32:253–256

    Article  Google Scholar 

  • Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardeström P (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant Cell Environ 30:1523–1534

    Article  PubMed  CAS  Google Scholar 

  • Krause K, Falk J, Humbeck K, Krupinska K (1998) Responses of the transcriptional apparatus of barley chloroplasts to a prolonged dark period and to subsequent reillumination. Physiol Plant 104:143–152

    Article  CAS  Google Scholar 

  • Krupinska K, Humbeck K (2004) Photosynthesis and chloroplast breakdown. In: Noodén LD (ed) Plant cell death processes. Elsevier Science (USA), Academic Press, London, pp 169–187

    Google Scholar 

  • La Rocca N, Barbato R, Casadoro G, Rascio N (1996) Early degradation of photosynthetic membranes in carob and sunflower cotyledons. Physiol Plant 96:513–518

    Article  CAS  Google Scholar 

  • Leckie CP, McAinsh MR, Allen GJ, Sanders D, Hetherington AM (1998) Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95:15837–15842

    Article  PubMed  CAS  Google Scholar 

  • Letham DS, Palni LMS, Tao G-Q, Gollnow BI, Bates CM (1983) Regulators of cell division in plant tissues XXIX. The activities of cytokinin glucosides and alanine conjugates in cytokinin bioassays. J Plant Growth Regul 2:103–115

    Article  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  PubMed  CAS  Google Scholar 

  • Martin RC, Mok MC, Habben JE, Mok DWS (2001) A maize cytokinin gene encoding an O-glucosyltransferase specific to cis-zeatin. Proc Natl Acad Sci USA 98:5922–5926

    Article  PubMed  CAS  Google Scholar 

  • Masferrer A, Arro M, Manzano D, Schaller H, Fernández-Busquets X, Moncaleán P, Fernández B, Cunillera N, Boronat A, Ferrer A (2002) Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPSIS) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J 30:123–132

    Article  PubMed  CAS  Google Scholar 

  • Mishev K, Stefanov D, Ananieva K, Slavov Ch, Ananiev ED (2009) Different effects of dark treatment on pigment composition and photosystem I and II activities in intact cotyledons and primary leaves of Cucurbita pepo (zucchini). Plant Growth Regul 58:61–71

    Article  CAS  Google Scholar 

  • Mishev K, Dimitrova A, Ananiev ED (2011) Darkness affects differentially the expression of plastid-encoded genes and delays the senescence-induced down-regulation of chloroplast transcription in cotyledons of Cucurbita pepo L. (zucchini). Zeitschrift Naturforsch 66c:159–166

    Google Scholar 

  • Mok MC (1994) Cytokinins and plant development. In: Mok DWC, Mok MC (eds) Cytokinins: chemistry, activity, and function. CRC Press, Boca Raton, pp 155–166

    Google Scholar 

  • Moran R, Porath D (1980) Chlorophyll determination in intact tissues using N,N-dimethylformamide. Plant Physiol 65:478–479

    Article  PubMed  CAS  Google Scholar 

  • Motyka V, Vaňková R, Čapková V, Petrášek J, Kamínek M, Schmũlling T (2003) Cytokinin-induced upregulation of cytokinin oxidase activity in tobacco includes changes in enzyme glycosylation and secretion. Physiol Plant 117:11–21

    Article  CAS  Google Scholar 

  • Noodén LD (1988) Abscisic acid, auxin, and other regulators of senescence. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic Press, San Diego, pp 329–367

    Google Scholar 

  • Noodén LD, Letham DS (1993) Cytokinin metabolism and signalling in the soybean plant. Aust J Plant Physiol 20:639–653

    Article  Google Scholar 

  • Noodén LD, Singh S, Letham DS (1990) Correlation of xylem sap cytokinin levels with monocarpic senescence in soybean. Plant Physiol 93:33–39

    Article  PubMed  Google Scholar 

  • Noodén LD, Guiamet JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753

    Article  Google Scholar 

  • Ori N, Jackson MT, Yamaguchi J, Banowetz GM, Hake S (1999) Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted 1 under the control of a senescence-activated promoter. Plant Cell 11:1073–1080

    Article  PubMed  CAS  Google Scholar 

  • Pourtau N, Mares M, Purdy S, Quentin N, Ruel A, Wingler A (2004) Interactions of abscisic acid and sugar signaling in the regulation of leaf senescence. Planta 219:765–772

    Article  PubMed  CAS  Google Scholar 

  • Roelfsema MRG, Prins HBA (1995) Effect of abscisic acid on stomatal opening in isolated epidermal strips of abi mutants of Arabidopsis thaliana. Physiol Plant 95:373–378

    Article  CAS  Google Scholar 

  • Sakakibara H (2005) Cytokinin biosynthesis and regulation. Vitam Horm 72:271–287

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning, a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J Exp Bot 60:1439–1463

    Article  PubMed  CAS  Google Scholar 

  • Skoog F, Ghani AKBK (1981) Relative activities of cytokinins and antagonists in releasing lateral buds of Pisum from apical dominance compared to their relative activities in the regulation of growth of tobacco callus. In: Guern J, Péaud-Lenoël C (eds) Metabolism and molecular activities of cytokinins. Springer, Berlin, pp 140–150

    Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448

    Article  CAS  Google Scholar 

  • Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmülling T (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in bacterial assay. Plant Cell Physiol 45:1299–1305

    Article  PubMed  Google Scholar 

  • Tozawa Y, Teraishi M, Sasaki T, Sonoike K, Nishiyama Y, Itaya Y, Miyao A, Hirochika H (2007) The plastid sigma factor SIGI maintains photosystem I activity via regulated expression of the psaA operon in rice chloroplsts. Plant J 52:124–132

    Article  PubMed  CAS  Google Scholar 

  • Tsukaya H, Tsuge T, Uchimiya H (1994) The cotyledon–a superior system for studies of leaf development. Planta 195:309–312

    Article  CAS  Google Scholar 

  • Tyystjärvi E, Karunen J (1990) A microcomputer program and fast analog to digital converter card for the analysis of fluorescence induction transients. Photosynth Res 26:127–132

    Article  Google Scholar 

  • Van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge U-I, Kunze R (2006) Transcriptional analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792

    Article  PubMed  Google Scholar 

  • Van Staden J, Cook EL, Noodén LD (1988) Cytokinins and senescence. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic Press, San Diego, pp 281–328

    Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatments. Plant Mol Biol 37:455–469

    Article  PubMed  CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492

    Article  PubMed  CAS  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onkelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  PubMed  CAS  Google Scholar 

  • Yamagishi M, Yamamoto Y (1994) Effect of boron on nodule development and symbiotic nitrogen fixation in soybean plants. Soil Sci Plant Nutr 40:265–274

    CAS  Google Scholar 

  • Yang SH, Berberich T, Sano H, Kusano T (2001) Specific association of transcripts of tbzF and tbz17, tobacco genes encoding basic region leucine zipper-type transcriptional activators, with guard cells of senescing leaves and/or flowers. Plant Physiol 127:23–32

    Article  PubMed  CAS  Google Scholar 

  • Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol 134:1654–1661

    Article  PubMed  CAS  Google Scholar 

  • Zažímalová E, Kamínek M, Březinová A, Motyka V (1999) Control of cytokinin biosynthesis and metabolism. In: Hooykaas PJJ, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. Elsevier Science B.V., Amsterdam, pp 141–160

    Chapter  Google Scholar 

  • Zubo YO, Yamburenko MV, Selivankina SY, Shakirova FM, Avalbaev AM, Kudryakova NV, Zubkova NK, Liere K, Kulaeva ON, Kusnetsov VV, Börner T (2008) Cytokinin stimulates chloroplast transcription in detached barley leaves. Plant Physiol 148:1082–1093

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by a Bulgarian-Czech bilateral Academy of Sciences project and by GA AS CR (IAA600380701 and IAA600380805) and MEYS CR (LC06034 and 1M06030).

Author information

Authors and Affiliations

  1. Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bl. 21, 1113, Sofia, Bulgaria

    Kalina Ananieva, Snejana Doncheva, Detelin Stefanov & Kiril Mishev

  2. Department of Plant Physiology, Faculty of Biology, St. Kliment Ohridsky University of Sofia, 8 Dragan Tsankov blvd., 1164, Sofia, Bulgaria

    Evguéni D. Ananiev

  3. Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojová 263, 165 02, Prague 6, Czech Republic

    Miroslav Kamínek, Vaclav Motyka, Petre I. Dobrev & Jiři Malbeck

Authors
  1. Kalina Ananieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evguéni D. Ananiev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Snejana Doncheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Detelin Stefanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kiril Mishev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Miroslav Kamínek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vaclav Motyka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Petre I. Dobrev
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jiři Malbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kalina Ananieva or Evguéni D. Ananiev.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ananieva, K., Ananiev, E.D., Doncheva, S. et al. Local induction of senescence by darkness in Cucurbita pepo (zucchini) cotyledons or the primary leaf induces opposite effects in the adjacent illuminated organ. Plant Growth Regul 65, 459–471 (2011). https://doi.org/10.1007/s10725-011-9616-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-011-9616-8

Keywords

Search

Navigation