IAA and regulation of Arabidopsis circadian rhythm

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Reference

IAA and regulation of Arabidopsis circadian rhythm

JOUVE, Laurent, et al.

Abstract

Decapitation of Arabidopsis floral stern suppresses elongation and any associated rate oscillation. This growth inhibition also appeared after application on intact plants of IAA transport inhibitors such as NP A. A subsequent IAA paste application on the cut surface restored growth and circadian oscillations in extension rate. These results indicate that the upper zone of the inflorescence has a major influence on floral stem extension rate and give a particular importance to auxin. Furthermore, measurement of endogenous contents of IAA and IAA-aspartate conjugate displayed that they were subjected to a circadian rhythm during Arabidopsis floral stern growth. All together, these data point out lAA as an essential factor in circadian growth rhythm regulation of Arabidopsis floral stem

JOUVE, Laurent, et al . IAA and regulation of Arabidopsis circadian rhythm. Endocytobiosis and Cell Research , 2001, vol. 14, p. 45-49

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ISE Letters

1 Reprint 1

ENDOCYTOBIOSIS

and CELL RESEARCH

Volume 14, pp. 1 - 146 July 2001

ISSN 0256-1514

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ISE Letters 2001 International Journal on

ENDOCYTOBIOSIS AND CELL RESEARCH Organ of the International Society of Endocytobiology (ISE) Executive Editors

D.C. Smith K.W. Jean H.E.A. Schenk Editorial Board V. Ahmadjian J. Bereiter-Hahn T. Cavalier-Smith K.-P. Chang J.O. Corliss A.E. Douglas L.N. Edmunds, Jr.

V. Erdmann G.E. Fox M. Galun H.-D. Gôrtz A. GraBmann J.H.P. Hackstein J.W. Hastings R. Hinde P. John L. Kies B.P. Kremer J.J. Lee U. Maier P.S.C. McAuley L. Margulis L. Muscatine P. Nardon A. Pühler G.M. Rothe P. Sitte T. Tiivel R.K. Trench K. Valentin E. Wagner D. Werner P. Wrede

Wolfson College, University of Oxford, Oxford OX2 6UD, England, UK University of Tennessee, Department of Biochemistry, Knoxville, TN 37996-0840, USA

University of Tübingen, ZMBP, Plant Physiology, Auf der Morgenstellel, D-72076 Tuebingen

(Clark University, Worcester, USA) (University of Frankfurt/M., Germany) (University of Oxford, England, UK) (URS/Chicago Medical School, USA) (University of Maryland, College Park, USA) (University of East Anglia, England, UK) (State University of New York, USA) (Free University Berlin, Germany) (University of Houston, USA) (Tel-Aviv University, Israel) (University of Stuttgart, Germany) (Free University of Berlin, Germany) (Cath. University Njmegen, The Netherlands) (Harvard University Cambridge, USA) (University of Sydney, Australia) (University of Reading, England, UK) (University of Hamburg, Germany) (University ofKôln, Germany) (City College of New York, USA) (University ofMarburg, Germany) (University of Oxford, England, UK) (University ofMass., Amherst, USA) (University of California, Los Angeles, USA) (INSA, Villeurbanne, France)

(University of Bielefeld, Germany) (University ofMainz, Germany) (University ofFreiburg, Germany) (Estonian Acad. Sc., Tallinn, Estonia) (University of California, S. Barbara, USA) (Alfred Wegener Institute, Bremerhaven, Germany) (University of Freiburg, Germany)

(University of Marburg, Germany) (Free University of Berlin, Germany)

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ENDOCYTOBIOSIS AND CELL RESEARCH ISSN 0256-1514

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Endocytobiosis & Cell Res. 14, 45-49 (2001) 45

lAA AND REGULATION OF ARABIDOPSIS CIRCADI- AN RHYTHM

L. JOUVE¹*, T. FRANCK23 , P. FAVRE1 , S. KAYALI1 , H. GREPPIN¹AND R.

DEGLI AGOSTI¹

1 Plant Biochemistry and Physiology Laboratory, University of Geneva, 3 place de l'Uni- versité, CH-1211 Geneva 4, Switzerland

2 Fundamental and Applied Hormonology Laboratory, Institute of Botany B 22, University of Liège-Sart Tilman, B-4000 Liège, Belgium

3 CRP-CU, 162A avenue de la Faïancerie, L-1511 Luxembourg, Luxembourg

*Correspondence to L. Jouve: Fax: 41-22 329 77 95, E-mail: laurent.jouve@bota.unige.ch

Keywords: Arabidopsis, floral stem, growth, auxin, polar transport, conjugation, circadian.

Summary: Decapitation of Arabidopsis floral stern suppresses elongation and any associated rate oscillation. This growth inhibition also appeared after application on intact plants of IAA transport inhibitors such as NP A. A subsequent IAA paste application on the eut surface restored growth and circadian oscillations in extension rate. These results indicate that the upper zone of the inflorescence has a major influence on floral stem extension rate and give a particular importance to auxin. Furtherrnore, rneasurement of endogenous contents of IAA and IAA-aspartate conjugate displayed that they were subjected to a circadian rhythm during Arabi- dopsis floral stern growth. Ali together, these data point out lAA as an essential factor in circadian growth rhythm regulation of Arabidopsis floral stem.

INTRODUCTION

In the last decade, considerable improvements have been made towards an understanding of the mechanisrns underlying floral evocation and rnorphogenesis of Arabidopsis thaliana. During flowering time, the most obvious morphological change between the late rosette and the earl y inflorescence is the elongation of the internodes that norrnally occurs after formation of the first floral buds (Hernpel and Feldman, 1994, Jouve et al. 1998b). However, the growth process of inflorescence shoot is poorly understood and requires more investigation in order to elucidate the underlying rnechanisrns. The fact that the circadian rhythrnicity in growth rate has been measured already during Arabidopsis floral stem elongation (Jouve et al. 1998a) asks an interesting question. It is weil known that auxin caused elongation in coleoptiles (Evans 1974) and stem segments (Barkley and Evans 1970), and it was involved in intact plant growth (Yang et al. 1993 ). The re-

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46 Jouve, Franck, Favre, Kayali, Greppin, Degli Agosti

fore, the implication of IAA in the dynamics of plant stem growth, especially in Arabidopsis, was put into question. The aim of this paper was to discuss the pos- sible role of IAA and its aspartate conjugate in the behavioural dynamics of Arabi- dopsis floral stem growth.

MATERIAL AND METHODS Abbreviations

lAA: Indole-3-acetic acid, IAA-asp: Indole-3-acetic acid aspartate conjugate, NPA: N-(1- naphthyl)phthalamic acid

Arabidopsis thaliana (L.) Heynh (Landsberg erecta ecotype) was used as plant material.

The measurement of the first inflorescence node elongation was carried out with a plant growth measuring apparatus (Degli Agosti et al. 1997), using L VDT technology.

Lano lin pastes containing lAA, IAA-aspartate (IAA-asp) or NP A were prepared as described by lino (1995).

Before IAA or lAA-asp treatments, the floral stem was decapitated above the first leaf, which was itself above the first intemode. The lano lin paste was applied, onto the eut surface of the decapitated floral stem (Jouve et al. 1999).

A ring ofNPA paste was applied using an imbibed cotton thread on the surface of the lower part ofthe second floral stem intemode, just above the first leaf (Jouve et al. 1999).

The extraction and titration of endogenous lAA and lAA-asp were done according to the technique ofNordstrôm et al. (1991 ).

RESULTS AND DISCUSSION

Figure 1 schematizes the possible way of involvement of lAA in the Arabi- dopsis floral stem circadian growth rhythm. The different possible step (CD to @) in which IAA could break in on are discussed. Decapitation induced a strong inhibition of growth. Application of lAA restored the growth and its associated rate circadian oscillations (Jouve et al. 1999) as it have been already observed with non decapitated plants (Jouve et al. 1998a). This indicates that the upper zone of the inflorescence CD has a major influence on floral stem extension rate ®. The resto- ration of growth after decapitation and application of a constant lAA concentration showed that the dynamics of the synthe sis at the leve! of the apex are

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Endocytobiosis & Cell Res. 14, 45-49 (200 1)

rA~~X~

~ lAA Production

=

~

^Transport

~

^IAA

-!-~~

Conjugate (

t ···~

⁰

~L-:.~asp

Detoxifîcation Endogeuous lAA

Receptivity Oscillator

~GROWTH~

~ oc

47

Fig. 1: Mode! of the possible intervention of different steps in the IAA growth rhythm regulated metabolism. <D lAA synthesis. @ Possible dynamic production of lAA by the apex. Gl Possible constant production of lAA by the apex. ® Specifie lAA polar transport. @ Inter-conversion between lAA and its conjugates. ® Possible direct intervention of the auxin receptor in the subsequent growth rhythm. <V Possible direct or indirect intervention of an oscillator in the subsequent growth rhythm. ® Inflorescence circadian growth rhythm.

B Decapitation. - Possible location of the oscillation input. = Constant. -+ Application of an exogenous product. ""Measured oscillations. Adapted from Jouve et al. (! 999)

are not a lirniting factor. The production of lAA could be an oscillatory phenorne- non CV, but also a continuo us flux <] as it was after decapitation and subsequent IAA application.

lAA is rnainly produced in apex CD and has to be transported ® to act on subapical zone to induce growth ®l. Auxin transport occurs in a very specifie rnan- ner in a basipetal direction in stems (Lornax et al. 1995). The auxin undergoing transport is clearly involved in the regulation of stern elongation (Yang et al. 1993, Davies 1995, Jouve et al. 1999). Polar transport of endogenous (Zakrzewski 1983) or exogenous (Shen-Miller 1973) auxin has been reported as an oscillatory pheno- menon. Our results disp1ayed that IAA application, after decapitation, during con- tinuous light exposure restored circadian oscillations in growth rate as has been

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48 Jouve, Franck, Favre, Kayali, Greppin, Degli Agosti

already observed with intact plants (Jouve et al. 1998a). Auxin basipetal transport could not explain this kind of fluctuation because the measured period of lAA transport has been reported to be about 4 hours (Zajaczkowski et al. 1984).

Our results have displayed a daily oscillation in endogenous content of lAA and lAA-asp ® (Jouve et al. 1999), which has been already observed in several plants (Rama Das et al. 1964, Janardhan et al. 1973, Krekule et al. 1985). The regulation of lAA turnover involving synthesis, conjugation and catabolism is a possible means of regulating lAA action. The catabolic pathway of lAA oxidation involving its conjugation (Normanly 1997) could be responsible for the variations of endogenous free lAA, and later on, in the growth rate. lndeed, the fluctuations could be due to the inter-conversion (amide-linkage/hydrolysis) between lAA and its conjugates (Kleczkowski and Schell 1995) and to the oxidation process ®.

However, the use of IAA-asp as treatment after decapitation does not restore any growth (Jouve et al. 1999). Therefore, the hydrolytic pathway appears to be inef- ficient or diminished in our situation. The hypothesis involving lAA conjugation for storage or a further oxidation in the regulation of the growth rhythm has to be verified.

Both the perception and receptivity ® at the level of auxin binding <V and at the level of the signal transduction, involving the intervention of an unknown oscillator ® could take part in the metabolism of lAA regulating the rhythm of Arabidopsis circadian growth ®>.

REFERENCES

Barkley GM, Evans ML, 1970. Timing of auxin response in etiolated pea stem sections.

Plant Physiology 45: 143-147.

Davies PJ, 1995. The plant hormone concept: concentration, sensitivity and transport. In:

Davies PJ (ed) Plant Hormones. Physiology, Biochemistry and Molecular Biology.

Kluwer Academie Publishers, Dordrecht Boston London, pp 13-38.

Degli Agosti R, Jouve L, Greppin H, 1997. Computer-assisted measurement of plant growth with Linear Variable Differentiai Transformer (L VDT) sensors. Archives des Sciences de Genève 50: 233-244.

Evans LS, 1974. Rapid responses to plant hormones. Annual Review of Plant Physiology 25: 195-223.

Hempel FD, Feldman LJ, 1994. Bi-directional inflorescence development in Arabidopsis thaliana: acropetal initiation of flow ers and basipetal initiation of paraclades. Planta 192: 276-286.

lino M, 1995. Gravitropism and photoperiodism of maize coleoptiles: evaluation of the Cholodny-Went theory through effects of auxin application and decapitation. Plant Celland Physiology 36: 361-367.

Janardhan KV, Vasudeva N, Gopel NH, 1973. Diurnal variation of endogenous auxin in arabica coffee leaves. Journal of Plant Crops 1 (Suppl): 93-95.

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Endocytobiosis & Cell Res. 14, 45-49 (2001) 49

Jouve L, Greppin H, Degli Agosti R, 1998a. Arabidopsis thaliana floral stem elongation:

Evidence for an endogenous circadian rhythm. Plant Physiology and Biochemistry 36: 469-472.

Jouve L, Charron Y, Couderc C, Greppin H, Degli Agosti R, 1998b. Dependence of Arabidopsis thaliana floral stem growth and architecture on photoperiod. Biologia Plantarum 41: 377-386.

Jouve L, Gaspar T, Kevers C, Greppin H, Degli Agosti R, 1999. Involvement of lAA in Arabidopsis circadian growth. Planta 209: 136-142.

Kleczkowski K, Schell J, 1995. Phytohormone conjugates: Nature and function. Critical Review of Plant Science 14: 283-298.

Krekule J, Pavlova L, Souckova D, Machackova I, 1985. Auxin in flowering of short-day and long-day Chenopodium species. Biologia Plantarum 27: 310-317.

Lomax TL, Muday GK, Rubery PH, 1995. Auxin transport. In: Davies PJ (ed) Plant Hor- mones. Physiology, Biochemistry and Molecular Biology. Kluwer Academie Pub- lishers, Dordrecht Boston London, pp 509-530.

Nordstrôm AC, Alvarado Jacobs F, Eliasson L, 1991. Effects of exogenous indole-3- acetic acid and indole-3-butiric acid on interna! levels of the respective auxins and their conjugaison with aspartic acid during adventitious root formation in pea cut- tings. Plant Physiology 96: 856-861.

Normanly J, 1997. Auxin metabolism. Physiologia Plantarum 100: 431-442.

Rama Das VS, Rao JVS, Rao KR, 1964. Endogenous auxin an its diurnal rhythm in leaves. Indian Journal of Plant Physiology 7: 25-29.

Shen-Miller J, 1973. Rhythmicity in the basipetal transport in indolacetic ac id through coleoptiles. Plant Physiology 51: 615-619.

Yang T, Law DM, Davies PJ, 1993. Magnitude and kinetics of stem elongation induced by exogenous indole-3-acetic acid in intact light-grown pea seedlings. Plant Physiology 102: 717-724.

Zajaczkowski S, Wodzicki TJ, Romberger JA, 1984. Auxin waves in plant morphogenesis.

In: Scott TK (ed) Encyclopedia of Plant Physiology. Vol 10. Hormonal Regulation of Development II. Springer, Berlin Heidelberg New York Tokyo, pp 244-262.

Zakrzewski J, 1983. Hormonal control of cambial activity and vesse! differentiation in Quercus robur. Physiologia Plantarum 57: 537-542.

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Endocytobiosis & Cell Res. 14, 112 (2001)

contents - continued

Evidence for bacteriophages within Neoch!amydia hartmannellae, an obligate endoparasitic bacterium of the free-living amoeba Hartmannella vermiformis

v

E.N. SCHMID, K.-D. MÜLLER, R. MICHEL 115

Cellular lipid inclusions of the symbiotic dinoflagellate harboured by the tro- pical jellyfish Catostylus sp.

T. LUONG-VAN, E. HAYWARD 121

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Cyanophora paradoxa as a mode! organism for plastid evolution

J. STEINER, YAN MA, B. PFANZAGL, W. LÔFFELHARDT 127

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Total internai reflection fluorescence microscopy (TIRFM) of acridine orange in single cells

R. SAILER, K. STOCK, W.S.L. STRAUSS, M. LYTTEK, H. SCHNECKENBURGER 129 Book Reviews

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TITLE FIGURE: Lipid transport from chloroplast to the cytoplasm of the endocytobiotic dinoflagellate of Catostylus sp. (scale bar: 200 nm (see Luong-Van & Hayward, p. 125).

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ENDOCYTOBIOSIS AND CELL RESEARCH, an international journal and organ of the Internatio- nal Society of Endocytobiology, aims to promote the flow of information and to stimula te the co- operation between SYMBIOSIS researchers and CELL biologists.

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Endocytobiosis & Cell Res. 14, 1/2 (2001) VI

ISE Letters

International Journal on

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Volume 14, Number 1/2, July 2001

CONTENTS

MASAHIRO R. ISHIDA (1926-2000), OBITUARY AND LEGACY

M. Saito, M. Sugiura, J. Obokata 1

Letter to Editor

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Decoding of the NDHH Operon from spinach: an example for the complexity of plastid gene expression in higher plants

J. LEGEN, C. SCHMITZ-LINNEWEBER, A. DRESCHER, H. HUPFER, M. TILLICH,

R.G. HERRMANN, R.M. MAIER 11

Bernard Millet Retirement Symposium, Freiburg 1998 Proceedings: Reviews and Research Articles

Introduction and Scientific Program

E. WAGNER 21

Repetitive action potentials induced with a single stimulus in the liverwort Co- cephalum conicum (L.)

P. FAVRE, T. ZA WADZKI, A. DZUBINSKA, K. TREBACZ, H. GREPPIN, R. DEGLI AGOSTI 23 Circadian gene expression in angiosperms and gymnosperms

B. PIECHULLA, M. BRINKER, K. WISSEL 33

IAA and regulation of Arabidopsis circadian rhythm

L. JOUVE, T. FRANCK, P. FAVRE, S. KA YALI, H. GREPPIN, R. DEGLI AGOSTI 45 The Localization of Endogenous Rhythm of Flowering in Chenopodium rubrum

J. KREKULE, 1. MACHACKOV A 51

Involvement of glucose in pH-regulation in cells at the apical meristem of vege- tative and flower-induced Chenopodium rubrum plants.

J.T.P. ALBRECHTOVA, T. WIEDMANN, P. WALCZYSKO, E. WAGNER 57 The adenylate kinase family in plants: Isoenzyme activity is related to flower induction

U. SCHLATTNER, E. WAGNER 67

Occurrence and possible function of melatonin in plants a review J. KOLAR, 1. MACHACKOV A

Interaction by gaseous way and development in higher plants H. GREPPIN, A. SI-AMMOUR

Research Articles and Short Communications

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A stochastic approach to the evolution of mutation rates for an infinite asexual population

A. FUKSHANSKY 91

Hartmannella vermiformis (gymnamoebia) isolated from tap water harboured simultaneously two different bacterial endocytobionts

R. HOFFMANN, R. MICHEL 103

continuation on page V (inside back cover)

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