Abstract
With the short-day plant Chenopodium rubrum and the long-day plant Chenopodium murale, growth and behavior have been studied in response to photo- and thermoperiod. With time-lapse photography, rhythmic integration of the plant as a whole could be monitored. Upon photoperiodic flower initiation, rhythmic stem extension rate (SER) and leaf movements (LM) change their phase relationship in a specific way. Flower induction correlates with a threshold value for the ratio between integral growth during the dark-time span and integral growth during the light-time span. This precise output displayed in the growth pattern of the plant is therefore an accurate reflection of all available environmental inputs. Analysis of flower induction in Chenopodium spp. showed that 2 h after the end of the critical dark period, the patterns of cytoplasmic pH and Ca2+ change at the shoot apical meristem (SAM), possibly indicating the arrival of the flower-inducing signal. Changes in LEAFY (a florigenic transcription factor) and aquaporin expression can also be recorded during this phase. The perception of a flower-inducing dark period leads to a change in electrochemical, hydraulic signaling between the leaves and SAM, thereby determining polarity in the whole plant and paving the way for “florigen” . Leaves from flowering plants can be grafted on non-induced plants (short- or long-day species) to induce flowering in the recipient plant. Flowering could even be induced using a different donor and recipient species (inter-species signaling). A rhythmic integration over the whole plant, as seen for SER and LM, most likely involves modulation of turgor pressure via stretch-activated ion channels and concomitant changes in membrane potential, making the plant a hydro-electrochemical signal transducer. Regulation of hydraulics and electrochemistry, two coupled physicochemical processes, was an achievement of early evolution as well as metabolic circadian regulation of transcriptional translational control loops (TTCL). Circadian rhythms (CRs) in energy metabolism are gating inputs and outputs to the TTCL, resulting in a CR of protein synthesis and turnover. Evolution of latitudinal ecotypes with different CR period lengths will depend on specific proteins, as is evident from early crossing experiments. The control of the ionic composition of the cell is crucial for the survival and requires energy to maintain a resting potential of the plasma membrane. This, in turn, enables the generation of action potentials and, hence, a fast systemic communication between plant organs, in particular the root and shoot meristems (RAM and SAM).
Dedicated to the 80th anniversary of Hubert Greppin.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aimi R, Shibasaki S (1975) Diurnal change in bioelectric potential of Phaseolus plant in relation to the leaf movement and light conditions. Plant Cell Physiol 16:1157–1162
Albrechtová JTP, Wagner E (2004) Mechanisms of changing organogenesis at the apex of Chenopodium rubrum during photoperiodic flower induction. Flowering Newslett 38:27–33
Albrechtová JTP, Metzger C, Wagner E (2001) pH-patterning at the shoot apical meristem as related to time of day during different light treatments. Plant Physiol Biochem 39:115–120
Albrechtová JTP, Heilscher S, Leske L, Walczysko P, Wagner E (2003) Calcium and pH patterning at the apical meristem are specifically altered by photoperiodic flower induction in Chenopodium spp. Plant, Cell Environ 26:1985–1994
Albrechtová JTP, Dueggelin M, Dürrenberger M, Wagner E (2004) Changes in geometry of the apical meristem and concomitant changes in cell wall properties during photoperiodic induction of flowering in Chenopodium rubrum. New Phytol 163:263–269
Albrechtová JTP, Veit J, Vervliet-Scheebaum M, Wagner E (2005) Signals for flower initiation—Do plants have a nervous system or mRNA/protein shuttles for signalling? Flowering Newslett 40:16–19
Albrechtová JTP, Vervliet-Scheebaum M, Normann J, Veit J, Wagner E (2006) Metabolic control of transcriptional-translational control loops (TTCL) by circadian oscillations in the redox- and phosphorylation state of cells. Biol Rhythm Res 37(4):381–389
Al-Musawi LI, Wagner E (2012) Seasonal and lunar variation in the emergence time of a population of Uca lactea annulipes (Milne-Edwards, 1837) at a shore in Kuwait. Chronobiol Int 29(4):408–414
Aon MA, Saks V, Schlattner U (eds) (2014) Systems biology of metabolic and signaling networks: energy, mass and information transfer. Springer, Berlin
Arthur J, Guthrie J, Newell J (1930) Some effects of artificial climates on the growth and chemical composition of plants. Am J Bot 17:416–482
Baiges I, Schäffner AR, Affenzeller MJ, Mas A (2002) Plant aquaporins. Physiol Plant 115(2):175–182
Baluška F, Mancuso S, Volkmann D (eds) (2006a) Communication in plants. Neuronal aspects of plant life. Springer, Berlin, Heidelberg
Baluška F, Menzel D, Barlow PW (2006b) Cytokinesis in plant and animal cells: endosomes “shut the door”. Dev Biol 294(1):1–10
Barlow PW, Fisahn J (2012) Lunisolar tidal force and the growth of plant roots, and some other of its effects on plant movements. Ann Bot 110(2):301–318
Bonzon M, Hug M, Wagner E, Greppin H (1981) Adenine nucleotides and energy charge evolution during the induction of flowering in spinach leaves. Planta 152(3):189–194
Bonzon M, Simon P, Greppin H, Wagner E (1983) Pyridine nucleotides and redox-charge evolution during the induction of flowering in spinach leaves. Planta 159(3):254–260
Borchert R, Renner SS, Calle Z, Navarrete D, Tye A, Gautier L, von Hildebrandt P (2005) Photoperiodic induction of synchronous flowering near the Equator. Nature 433:627–629
Bünning E (1935) Zur Kenntnis der erblichen Tagesperiodizität bei den Primärblättern von Phaseolus multiflorus. Jahrb Wiss Bot 81:411–418
Bünning E (1973) The physiological clock, 3rd edn. Springer, Berlin, Heidelberg
Bünning E (1977) Die Physiologische Uhr, 3rd edn. Springer, Berlin, Heidelberg
Cumming BG (1959) Extreme sensitivity of germination and photoperiodic reaction in the genus Chenopodium (Tourn.) L. Nature 184:1044–1045
Cumming BG (1967a) Correlations between periodicities in germination of Chenopodium Botrys and variations in solar radio flux. Can J Bot 45(7):1105–1113
Cumming BG (1967b) Early-flowering plants. In: Wilt F, Wessels N (eds) Methods in developmental biology. Crowell, New York, pp 277–299
Cumming BG, Wagner E (1968) Rhythmic processes in plants. Ann Rev Plant Physiol 19:381–416
De la Fuente IM, Cortés JM, Valero E, Desroches M, Rodrigues S, Malaina I, Martínez L (2014) On the dynamics of the adenylate energy system: homeorhesis vs homeostasis. PloS One 9(10):e108676
Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933–936
Dunlap J (1999) Molecular bases for circadian clocks. Cell 96:271–290
Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485(7399):459–464
Frosch S, Wagner E (1973) Endogenous rhythmicity and energy transduction. III. Time course of phytochrome action in adenylate kinase, NAD- and NADP-linked glyceraldehyde-3- phosphate dehydrogenase in Chenopodium rubrum. Can J Bot 51:1529–1535
Frosch S, Wagner E, Cumming BG (1973) Endogeneous rhythmicity and energy transduction. I. Rhythmicity in adenylate kinase, NAD- and NADP-linked glyceraldehyde-3-phosphate dehydrogenase in Chenopodium rubrum. Can J Bot 51:1355–1367
Genoud T, Métraux J-P (1999) Crosstalk in plant cell signaling: structure and function of the genetic network. Trends Pharmacol Sci 4:503–507
Golden SS, Ishiura M, Johnson CH, Kondo T (1997) Cyanobacterial circadian rhythms. Annu Rev Plant Physiol Mol Biol 48:327–354
Goldsworthy A (1983) The evolution of plant action potentials. J Theor Biol 103:645–648
Green PB (1994) Connecting gene and hormone action to form, pattern and organogenesis: biophysical transductions. J Exp Bot 45:1775–1788
Hendricks SB (1963) Metabolic control of timing. Science 141:1–7
Highkin HR (1960) The effect of constant temperature environment and of continuous light on the growth and development of pea plants. Cold Spring Harb Symp Quant Biol 25:231–238
Highkin HR, Hanson JB (1954) Possible interaction between light-dark cycles and endogenous daily rhythms on the growth of tomato plants. Plant Physiol 29:301–302
Hillman WS (1956) Injury of tomato plants by continuous light and unfavorable photoperiodic cycles. Am J Bot 43:89–96
Huang TC, Tu J, Chow TJ, Chen TH (1990) Circadian rhythm of the prokaryote Synechococcus sp. RF-1. Plant Physiol 92:531–533
Hwang I, Chen H-C, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515
Jang J-C, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679
King RW (1975) Multiple circadian rhythms regulate photoperiodic flowering responses in Chenopodium rubrum. Can J Bot 53:2631–2638
Kloda A, Martinac B (2002) Common evolutionary origins of mechanosensitive ion channels in Archaea, Bacteria and cell-walled Eukarya. Archaea 1:35–44
Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654
Lang F, Waldegger S (1997) Regulating cell volume. Am Sci 85:456–463
Lecharny A, Wagner E (1984) Stem extension rate in light-grown plants. Evidence for an endogenous circadian rhythm in Chenopodium rubrum. Physiol Plant 60(3):437–444
Lecharny A, Schwall M, Wagner E (1985) Stem extension rate in light-grown plants. Plant Physiol 79:625–629
Li W, Llopis J, Whitney M, Zlokarnik G, Tsien RY (1998) Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize ene expression. Nature 392:936–940
Lillo C, Meyer C, Ruoff P (2001) The nitrate reductase circadian system. The central clock dogma contra multiple oscillatory feedback loops. Plant Physiol 125:1554–1557
Lloyd D, Rossi ER (1992) Ultradian rhythms in life processes. Springer, London
Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232
Love J, Dodd AN, Webb AAR (2004) Circadian and diurnal calcium oscillations encode photo-periodic information in Arabidopsis. Plant Cell 16:956–966
Lüttge U (2003) Circadian rhythmicity: is the “biological clock” hardware or software? Progr Bot 64:277–319
McKenna JF, Tolmie F, Runions J (2014) Across the great divide: the plant cell surface continuum. Curr Opin Plant Biol 22:132–140
Merrow M, Roenneberg T (2001) Circadian clocks: running on redox. Cell 106(2):141–143
Morré DJ, Morré DM (1998) NADH oxidase activity of soybean plasma membranes inhibited by submicromolar concentrations of ATP. Plant J 16(3):277–284
Morré DJ, Morré DM (2013) ECTO-NOX proteins—growth, cancer and aging. Springer, Berlin
Morré DJ, Morré DM, Penel C, Greppin H (1999) NADH oxidase periodicity of spinach leaves synchronized by light. Int J Plant Sci 160(5):855–860
Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727–739
Nakajima M, Ito H, Kondo T (2010) In vitro regulation of circadian phosphorylation rhythm of cyanobacterial clock protein KaiC by KaiA and KaiB. FEBS Lett 584(5):898–902
Nakamura Y, Andrés F, Kanehara K, Liu Y, Dörmann P, Coupland G (2014) Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat Commun 5:3553
Normann J, Vervliet-Scheebaum M, Albrechtová JTP, Wagner E (2007) Rhythmic stem extension growth and leaf movements as markers of plant behaviour: the integral output from endogenous and environmental signals. In: Mancuso S, Shabala S (eds) Rhythms in plants: phenomenology, mechanisms, and adaptive significance. Springer, Berlin, Heidelberg
Ohya T, Hayashi Y, Tanoi K, Rai H, Nakanishi TM, Suzuki K, Wagner E (2005) Root-shoot-signalling in Chenopodium rubrum L. as studied by 15O labeled water uptake. In: Abstract symposium XVIIth international botanical congress, Vienna, Austria, 17–23 July 2005, p 313
Pickard BG (1973) Action potentials in higher plants. Bot Rev 39:172–201
Ruiz-Fernandez S, Wagner E (1989) Flowering in Chenopodium rubrum. Light control of stem elongation rate (SER) as a systemic marker for flower induction. Flowering Newslett 8:14–19
Ruiz-Fernandez S, Wagner E (1994) A new method of measurement and analysis of the stem extension growth rate to demonstrate complete synchronisation of Chenopodium rubrum plants by environmental conditions. J Plant Physiol 144:362–369
Satter RL, Galston AW (1973) Leaf movements: Rosetta stone of plant behavior? Bioscience 23:407–416
Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc Natl Acad Sci USA 110(5):1791–1796
Schlattner U, Tokarska-Schlattner M, Rousseau D, Boissan M, Mannella C, Epand R, Lacombe ML (2014) Mitochondrial cardiolipin/phospholipid trafficking: the role of membrane contact site complexes and lipid transfer proteins. Chem Phys Lipids 179:32–41
Schwall M, Kropp B, Steinmetz V, Wagner E (1985) Diurnal modulation of phototropic response by temperature and light in Chenopodium rubrum L. as related to stem extension rate and arginine decarboxylase activity. Photochem Photobiol 42:753–757
Schwenke H, Wagner E (1992) A new concept of root exudation. Plant Cell Environ 15:289–299
Shabala S (2006) Oscillations in plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Neuronal aspects of plant life. Springer, Berlin, Heidelberg, pp 261–275
Svoboda J, Hošek P (1976) Arctic sun simulator for ecophysiological studies. Arct Alp Res 8(4):393–398
Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu D-T, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425(6956):393–397
Tsuchiya T, Ishiguri Y (1981) Role of the quality of light in the photoperiodic flowering response in four latitudinal ecotypes of Chenopodium rubrum L. Plant Cell Physiol 22(3):525–532
Tu BP, Kudlicki A, Rowicka M, McKnight SL (2005) Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310(5751):1152–1158
Vigh L, Maresca B, Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23:369–374
Volkov AG (ed) (2006) Plant electrophysiology. theory and methods. Springer, Berlin, Heidelberg
Volkov AG (ed) (2012) Plant electrophysiology. Signaling and responses. Springer, Berlin, Heidelberg
Wagner E (1976a) Endogenous rhythmicity in energy metabolism: basis for timer-photoreceptor-interactions in photoperiodic control. In: Hastings J, Schweiger H (eds) Dahlem Konferenzen. Aabkon Verlagsgesellschaft, Berlin, pp 215–238
Wagner E (1976b) Kinetics in metabolic control of time measurement in photoperiodism. J Interdiscipl Cycle Res 7:313–332
Wagner E (1976c) The nature of photoperiodic time measurement: energy transduction and phytochrome action in seedlings of Chenopodium rubrum. In: Smith H (ed) Light and plant development. Proceedings of 22nd Nottingham Easter School in Agricultural Sciences, Butterworth, London
Wagner E, Cumming BG (1970) Betacyanin accumulation, chlorophyll content, and flower initiation in Chenopodium rubrum as related to endogenous rhythmicity and phytochrome action. Can J Bot 48(1):1–18
Wagner E, Frosch S, Deitzer GF (1974a) Membrane oscillator hypothesis of photoperiodic control. In: De Greef J (ed) Proceedings of the annual European symposium on plant photomorphogenesis. Campus of the State University Centre, Antwerpen, pp 15–19
Wagner E, Frosch S, Deitzer GF (1974b) Metabolic control of photoperiodic time measurements. J Interdiscipl Cycle Res 5:240–246
Wagner E, Deitzer GF, Fischer S, Frosch S, Kempf O, Stoebele L (1975) Endogenous oscillations in pathways of energy transduction as related to circadian rhythmicity and photoperiodic control. BioSystems 7:68–76
Wagner E, Härtle U, Kossmann I, Frosch S (1983) Metabolic and developmental adaptation of eukaryotic cells as related to endogenous and exogenous control of translocators between subcellular compartments. In: Schenk H, Schwemmler W (eds) Endocytobiology, vol II. Walter de Gruyter, Berlin, pp 341–351
Wagner E, Fernandez Ruis S, Normann J, Bonzon M, Greppin H (1993) Chronobiology: spatio-temporal organization of living systems. In: Greppin H, Bonzon M, Degli Agosti R (eds) Some physicochemical and mathematical tools for understanding of living systems. University of Geneva, Geneva, pp 109–126
Wagner E, Normann J, Albrechtová JTP, Walczysko P, Bonzon M, Greppin H (1998) Electrochemical-hydraulic signalling in photoperiodic control of flowering: is “florigen” a frequency-coded electric signal? Flowering Newslett 26:62–74
Wagner E, Normann J, Albrechtová JTP, Greppin H (2000) From cellular micro-compartimentation to inter-organ communication. The kinetic basis for molecular controls in photoperiodism. In: Greppin H, Penel C, Broughton WJ, Strasser R (eds) Integrated plant systems. University of Geneva, Geneva, pp 293–309
Wagner E, Lehner L, Normann J, Veit J, Albrechtová JTP (2006a) Hydro-electrochemical integration of the higher plant—basis for electrogenic flower induction. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Springer, Berlin, Heidelberg
Wagner E, Lehner L, Veit J, Normann J, Vervliet-Scheebaum M, Albrechtová JTP (2006b) Control of plant development by hydro-electrochemical signal transduction: a means for understanding photoperiodic flower induction. In: Volkov (ed) Plant electrophysiology—theory & methods. Springer, Berlin, Heidelberg
Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339(6120):704–707
Walczysko P, Wagner E, Albrechtová JTP (2000) Use of co-loaded Fluo-3 and Fura Red fluorescent indicators for studying the cytosolic Ca2+ concentrations distribution in living plant tissue. Cell Calcium 28(1):23–32
Went FW (1944) Plant growth under controlled conditions. III. Correlation between various physiological processes and growth in the Tomato plant. Am J Bot 31(10):597–618
Went FW (1958) The experimental control of plant growth. Soil Sci 85(5):288
Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360:62–65
Wu L, Reddy AB (2014) Rethinking the clockwork: redox cycles and non-transcriptional control of circadian rhythms. Biochem Soc Trans 42(1):1–10
Zürcher E, Cantiani M-G, Sorbetti-Guerri F, Michel D (1998) Tree stem diameters fluctuate with tide. Nature 392(April):665–666
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Normann, J., Lehner, L., Vervliet-Scheebaum, M., Svoboda, J., Albrechtová, A., Wagner, E. (2015). Rhythmic Stem Extension Growth and Leaf Movements as Markers of Plant Behavior: How Endogenous and Environmental Signals Modulate the Root–Shoot Continuum. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_3
Download citation
DOI: https://doi.org/10.1007/978-3-319-20517-5_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-20516-8
Online ISBN: 978-3-319-20517-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)