Provided byRERODOCDigitalLibrary http://doc.rero.ch CORE hc hudb ie orfrt thiswork. to which shouldbecitedtorefer Published in"InternationalJournalofDevelopmentalBiology49:539-546,2005" Fax: +41-26-300-9740.e-mail:[email protected] *Address correspondence to: Introduction has beenexaminedsinceclassicalantiquity(Adler not surprisingthatthebeautyandregularityofphyllotacticpatterns accessible toanybodywithoutexpensiveequipment.Itistherefore Kuhlemeier, 2002).Phyllotaxisisabiologicalphenomenonthat (Schwabe, 1984;SteevesandSussex,1989;Reinhardt characteristic patterns,aphenomenonreferredtoasphyllotaxis throughout vegetativedevelopment.Theleavesarearrangedin However, regularorganisationisnotonlyfoundinflowers,butalso the shapeandcolouroffloralorgans,fortaxonomicanalysis. precisely regulated,ithasbeenused,besidesothertraitssuchas sepals, petals,anthersandcarpels.Sincethisarrangementis exhibit characteristicsymmetricarrangementoftheirorgans;the and multijugatesystemsresultifthreeormoreprimordia are resulting inthegenerationofdoublespirals.Higherorderwhorled phyllotaxis, theleafpairsaredivergedbyapproximately 68 in theformationof4verticalrowsleaves,whereasbijugate decussate phyllotaxis,theleafpairsaredivergedby90 bijugate ifprimordiaareformedinpairs(Fig.1).Inthecase of primordium isformedatatimeanddecussate(opposite) or lent phyllotacticpatternsaredistichous(alternate)orspiral ifone Sussex, 1989;ReinhardtandKuhlemeier,2002).Themostpreva- of leafformationattheshootapicalmeristem(Steeves and The architectureofplantsishighlyregular.Forexample,flowers Phyllotaxis isdeterminedbythespatialandtemporalregulation KEY WORDS: understanding oftheregulatorymechanismbehindphyllotaxis. paper discussessomeaspectsofphyllotacticpatternsfoundinnatureandsummarizesourcurrent resulted intheidentificationofauxinasacentralplayerorganformationandpositioning.This are laiddown.Recently,thecombinationofgenetics,moleculartoolsandmicromanipulationhas small sizeoftheshootapicalmeristem,whereplantorgansareformedandphyllotacticpatterns of themhavebeenamenabletoexperimentalexamination.Thisisduemainlythedelicacyand hypotheses toexplainthenatureofmechanisticprinciplebehindphyllotaxis,however,notall centuries beentheobjectofadmirationandscientificexamination.Therehavenumerous angiosperms. Duetoitsremarkableprecision,beautyandaccessibility,phyllotaxishasfor phyllotaxis isfoundinvirtuallyallhigherplants,frommosses,overferns,togymnospermsand floral organsarearrangedinregularpatterns,aphenomenonreferredtoasphyllotaxis.Regular ABSTRACT Plantarchitectureischaracterizedbyahighdegreeofregularity.Leaves,flowersand Dr.DidierReinhardt.PlantBiology, DepartmentofBiology,RueAlbertGockel3,CH-1700,Fribourg,Switzerland. phyllotaxis, meristem,auxin,Arabidopsis,tomato Plant Biology, Department of Biology, Fribourg, Switzerland Fribourg, Biology, of Department Biology, Plant Regulation ofphyllotaxis et al., et DIDIER REINHARDT* q , resulting 1997). q , 1 and theleaves,aswelloffloralorgans(Okada nism isinvolvedintheformationandpositioningofcotyledons flower. Geneticevidencesuggeststhatanauxin-relatedmecha- floral developmentandultimatelytowhorledphyllotaxisinthe during embryogenesistospiralphyllotaxisvegetativeor exhibit atransitionfromtheinitialdecussatephyllotaxislaiddown during plantontogeny.Forexample,mostdicotyledonousplants distichous phyllotaxisismaize.Phyllotacticpatternscanchange tobacco andtomato.Animportantmodelsystemforthestudyof 1994). Furthermore,themonocotmaize,liketomato and between thebranchesofanindividualtree(Zagorska-Marek, diversity ofphyllotacticsolutionsinapopulationtreesand even Arabidopsis Hardtke andBerleth,1998;Reinhardt pattern andisfoundinmodelplantspeciessuchas formed simultaneously.Spiralphyllotaxisisthemostcommon able caseisrepresentedby primordia areformedpernode,insteadoftwo(Fig.2).Aremark- branches withspiralortricussatephyllotaxiswhenone three lotactic patterns.Forinstance,decussateplantsoccasionally form branches ofanindividualplantshowfundamentallydifferent phyl- phyllotactic patternsissupportedbycasesinwhichdifferent terns areobservedduringontogeny.Acommonbasisfordifferent at allstagesofdevelopmentandwhendifferentphyllotacticpat- This indicatesthatthesameorganogenicmechanismmayoperate al., 2000;Benjamins , exhibitsanauxin-dependentmechanismfororgan et al., et Metadata, citationandsimilarpapersatcore.ac.uk 2001;PflugerandZambryski,2004). Magnolia et al., et specieswhichexhibita 2000;Christensen Arabidopsis et al., et 1991; et , http://doc.rero.ch diverged fromthecotyledonsby90 two firsttrueleavesarealsoformedasanoppositepairthatis tion ofthecotyledonswhichareformedasanoppositepair.The of flowering. (reviewed inSchwabe,1984;SteevesandSussex,1989;Adler chemical principles,havebeenformulatedtoexplainphyllotaxis Numerous theories,basedongeometrical,biophysicalandbio- related mechanismmayregulatephyllotaxisinallfloweringplants. formation (Scanlon,2003)indicatingthataconservedauxin- i.1 hloatcpten npat.(A) Fig. 1.Phyllotacticpatternsinplants. Bromeliaceae The originofphyllotaxis onset offlowering( phyllotaxis eitherduringvegetativedevelopmentlikethe reproductive phase.Othermonocotsundergoatransitiontospiral symmetry ismaintainedduringtheentirelife-spanincluding distichous (alternate)phyllotaxisisestablishedandthebilateral initiation ofthescutellum,singlecotyledon.Ingrasses, formation andpositioning. phyllotaxis field,withtheemphasisonroleofauxininorgan gives anoverviewoverthemostrecentdevelopmentin by a star in (B). Circles in the centre represent the shoot apical meristem. apical shoot age the their to represent according centre the in numbered are Circles (B). in Primordia star a by Banasiak). Alicja by provided 1974).; Williams, from al., Bromeliaceae, Agavaceae and Arecacea and Agavaceae Bromeliaceae, with the youngest as number 1. Note that in the text primordia are primordia text the in that Note 1. number as youngest the with numbered as P1, P2 etc. The site of incipient leaf formation (L formation leaf incipient of site The etc. P2 P1, as numbered CD AB In dicotplants,bilateralsymmetryisestablishedwiththeinitia- Phyllotaxis hasbeenafieldofintenseinterestforcenturies. In monocotplants,bilateralsymmetryisestablishedwiththe 1997;ReinhardtandKuhlemeier,2002).Thepresentreview , thespiralpatternreturnstodistichousatonset (C) Orchidaceae decussate, (D) bijugate (redrawn from a picture a from (redrawn bijugate ).Conversely,inmany q Distichous, . Hence,dicotsstartwith (=palmtrees),oratthe (B) spiral (redrawn spiral 1 ) is indicated is ) Liliaceae, et 2 positions (Williams,1974;Medford third pairoftrueleaves,iftheyarenotformedinexactlyopposite transition isgradualandcanstartasearlywiththesecondor during vegetativedevelopmentorattheonsetofflowering.The but themajorityofplantsundergoesatransitiontospiralphyllotaxis Spiral phyllotaxis review focusesonspiralphyllotaxis. higher plants.Sinceithasbeenthebest-studiedpattern,this to producethestablespiralphyllotaxisfoundinmajorityof of thepreviousleafpairandresultingasymmetryispropagated situation forcesthenext(single)leaftobeformedinlargergap trees ( decussate phyllotaxis.Insomeherbs( and themeristem Phyllotaxis involvesinteractionsbetweenprimordia patterns. flank, thanontheastonishingprecisionoffinalphyllotactic on themechanismsinvolvedinleafpositioningatmeristem original patternoforganinitiation.Here,Iwouldliketofocus more system, thusthefinalphyllotacticpatternmaynotalwaysreflect the ated bythemeristemcanbecomealteredinanexpanding shoot clearly distinguished.Thephyllotacticpatternsoriginallygener- Although thetwophenomenaareobviouslyrelated,theyshouldbe process oforganinitiationandpositioningatthemeristemflank. pattern). However,thetermphyllotaxisisalsousedtodescribe arrangement oforgans(whichIprefertocallthephyllotactic spirals arealreadyclearlyprominent(Fig.3). pattern remainsrecognizableforsometime,evenafterthe5:8 to 5:8phyllotaxis(Fig.3;Williams,1975).Interestingly,the3:5 pattern oftheseedlingstartswith3:5andundergoesagradualshift higher phyllotacticnumbers,forexampleinflax,the during development.Thisresultsinagradualshiftfromlowerto 34:55. Inmanyplants,thediameterofmeristemincreases relative tothelargeflowerdisc,numberscanbeashigh such as2:3.Inasunflowercapitulum,inwhichthefloretsaresmall tomato, thephyllotacticpatternischaracterizedbylownumbers primordia andthemeristem.Ifleavesarerelativelylargelikein contact parastichiesdependsontherelativesizeofleaf numbers (0,1,2,3,5,8,13,21,34,55,etc.).Thenumberof consists oftermsthatrepresentthesumprevioustwo the Fibonacciseries(SteevesandSussex,1989).This of parastichiesineachdirectionrepresentsconsecutiveterms cerned whichruninbothdirections(Fig.3).Curiously,thenumber addition, secondaryspirals,thecontactparastichies,canbedis- which runsinclockwiseorcounter-clockwisedirection(Fig.1B).In gence angle,usually137.5 with increasingdistancefrom theprimordium,henceforminga ing tothisidea,theconcentration oftheinhibitorwoulddecrease presses leafformationinthevicinity ofexistingprimordia.Accord- exerted byadiffusibleinhibitor oforganogenesiswhichsup- Steeves andSussex,1989).This influencecouldforinstancebe involves negativeinfluencesfromolderprimordia(reviewed in: The termphyllotaxisisfrequentlyusedtoreferthefinal In spiralphyllotaxis,organsareformedwithaconstantdiver- It haslongbeenpostulatedthatthepositioningofanewleaf Aceraceae, Oleaceae Aceraceae, )thedecussatepatternismaintained, q , resultinginanontogeneticspiral et al., et Lamiaceae 1992).Thisasymmetrical ),shrubsand http://doc.rero.ch primordium) continuedtheircorrectontogeneticspiral(Reinhardt isolated fromtherestofshoot(togetherwithsmallestvisible periments whichshowedthatintomato,meristems were dium. Recently,thesefindingshavebeencomplementedbyex- future contactneighbourstowardsthesiteofisolatedprimor- by tangentialincisions.Thisresultedinthedisplacementof In theseexperiments,primordiawereseparatedfromthemeristem is determinedbythecontactneighbours(SnowandSnow,1931). classical workindicatedthatthepositionandwidthofprimordia of a3:5systemthisisP its directcontactneighboursintheparastichies.Incase At thesametime,newleafhascharacteristicdistancestowards angle of137 hence theirnames defects inorganogenesis.Their shootaxisgrowsasanakedstem, likely thatthedirectneighbours(e.g.P a largephyllotacticsystemasthesunflowercapitulum,itismore direct neighbours(thatisrelativetoP Auxin -thetriggeroforgan formation al., et Arabidopsis phyllotaxis andrequiresnospecificinducerofleafformation. attractive modelisbasedmerelyonanegativeregulatorof thus allowingleafformationtooccur.Initssimplestform,this concentration oftheinhibitorwouldfallbelowacriticalthreshold, gradient aroundeachprimordium.Atacharacteristicdistance,the numbered are (C) in Leaves spiral. (A) different phyllotacticpatterns. altissima Ailanthus Fig. 2.Branchesofoneindividual can influencethepositioningofL their exactfinalsizeandposition(Reinhardt normally determinethelateralextensionofnewprimordiaand thus larger thannormal,indicatingthatthepreexistingdirectneighbours phyllotaxis intomato.However,thenewprimordiagrew much direct contactneighboursarenotabsolutelyrequiredfor spiral enough informationtomaintaintheontogeneticspiral,thus, the together withthenextalreadydeterminedprimordium),provided a negativeinfluencefromP of thecapitulum.Onotherhand,insmallmeristeman considerable distancecorrespondingtonearlytheentirediameter ontogenetic spiral(thatisrelativetoP positioning ofL arises towhatdegreethesethreeprimordiacontributethe with 1 being the youngest (note youngest the being 1 with that this numbering does not cor- not does numbering this that respond to the numbering of pri- of numbering the to respond mordia in Fig. 1, since several since 1, Fig. in mordia unvisible primordia are not included not are primordia unvisible Decussate, Decussate, Two mutantshavebeendescribed in A newleaf(L here). (Modified from Reinhardt and Reinhardt from (Modified here). Kuhlemeier, 2002). Kuhlemeier, inpress).Hence,theonepreexistingprimordium(possibly seedling,L q fromthenextolderleafinontogeneticspiral(P (B) 1 . IsthepositionofL tricussate, 1 ) isformedwiththecharacteristicdivergence treewith pin formed1 pin 3 1 andP isformedlessthan100 (C) 1 couldeasilybeenvisaged.Early 5 (Fig.1B).Thequestionstherefore ( 1 A pin1 thanP 1 determinedatthelevelof 3 21 1 andP ;Okada , P andP Arabidopsis 2 etc)oraccordingtoits 1 whichislocatedata 5 et al., et 34 inourexample)?In ina21:34system) P et al., et m fromP 2005). ‘ withserious 1991)and 1 . Thus, B 1 ). 3 in tomatomeristems(Reinhardt supported bythefactthatexogenousauxintriggersectopicorgans organogenesis, butasaninstructivesignalmolecule.Thisview is auxin wouldnotsimplyactasapermissivefactorrequired for between organs(KuhlemeierandReinhardt,2001).Inthis case, at thepositionofincipientorganformation,butnotpositions tion ofauxininthemeristem.Itispossiblethataccumulates opened thepossibilitythatphyllotaxisisregulatedbydistribu- leaves ( site oforganinitiation.Analternative possibilitywouldbethatthe would bethattheymediatethe transportofauxinspecificallytothe may beexpectedtoinfluenced bytheprimordia.Onepossibility new organs(seeabove),theaccumulation ofauxininthemeristem sites. Sincethepreformedprimordia influencethepositioningof not onlytopermitorganformation, butalsotorestrictitthecorrect sion ofthisexperimentisthatauxindistributionhastoberegulated and oversized( of development.Duringembryogenesis,thecotyledonsarefused formed ( pid cotyledons (Mayer ; HardtkeandBerleth,1996),whichgotitsnamefromthefused pinoid A roleforauxininphyllotaxis tactic patterning. trigger ofleafandflowerformationasacomponentphyllo- transport ofandresponsetotheplanthormoneauxin(Gälweiler ing atallstagesofdevelopment.PIN1,PIDandMPfunctioninthe by sterility. Theseresultsshowthatthesamemechanism,mediated types (organnumber,positionandidentity),resultingincomplete leaf number(pid).Allthreemutantsexhibitstrongflowerpheno- and flowerformation(Przemeck tants orchemicallytreatedpinstructures(Reinhardt exogenous auxincouldrestoreorganformationbothonthemu- tranporters alsoabolishedorganformationandthatapplicationof 1998). Recentstudiesshowedthatchemicalinhibitorsoftheauxin (Vernoux correct spatialexpressionoforganandboundarymarkergenes In addition,theauxintransportregulatorPIN1isrequiredfor al., The discoverythatauxinactsasatriggeroforganformation PIN1 1998;Christensen,2000;Benjamins,2001;HardtkeandBerleth, and ( pid pin1 , mp pid PID et al., et ;Bennett mutantsshoworganogeneticphenotypesatallstages ).Vegetativephenotypesincludeoversizedandfused ),aberrantleafpositioning( and pin1 2000).Theseresultsestablishedauxinasthe MP et al., et and et al., et , isinvolvedinorganformationandposition- 1991),likewiseexhibitsadefectinleaf mp 1995).Athirdmutant, C ),orsupernumerarycotyledonsare et al., et et al., et 2000).The(indirect)conclu- 1996).Interestingly, pin1 , mp monopteros )andincreased et al., et 2000). pin1 ( mp et , http://doc.rero.ch et al., et Auxin transportproteinsgeneratephyllotacticpatterns acteristic spacingofleaves. meristem. However,bothmechanismswouldleadtosimilarchar- inhibitor ofleafformation,theyabsorbanactivator(auxin)fromthe the oneproposedininhibitormodel.Insteadofreleasingan Thus, theprimordiawouldactuallyhaveoppositefunctionof at characteristicminimaldistancesfrompreexistingprimordia. dium, suchthatauxinaccumulationinthemeristemcanoccuronly efficiency ofabsorptiondeclineswiththedistancefromprimor- 2002). Thelatterscenariocouldexplaintheregularspacing,if absorbing itfromtheirsurroundings(ReinhardtandKuhlemeier, primordia influencethedistributionofauxininmeristemby shoot apex.Arecentstudydescribestheexpressionandsubcel- transporters, inordertopredictthedirectionofauxinfluxes determine theexpressionandsubcellularlocalisationofauxin fied. biochemical functioninpolarauxintransportremainstobeidenti- as theinfluxandeffluxcarrier,respectively,althoughtheirprecise respectively. Therefore,Iwill,forsimplicity,refertoAUX1andPIN1 is compatiblewithaninvolvementinauxininfluxandefflux, nents ofthetransportmechanismandtheirsubcellularlocalisation tional factorsforeffectiveauxintransport,theyarecentralcompo- and Palme,2002).AlthoughAUX1PIN1mayrequireaddi- family togetherwithLIKEAUX1(LAX1),LAX2andLAX3(Parry carrier PIN1(Gälweiler RESISTANT1 (AUX1;Bennett tranport arerepresentedbytheputativeinfluxcarrierAUXIN Genetic analysishasshownthatcentralcomponentsofauxin undifferentiated tissuesoftheshootapex,thiscanbeexcluded. also takeplaceinthevasculature(Swarup export proteins(Lomax Fig. 3.Spiralphyllotaxisinflax. al., characterized by 3 counter-clockwise parastichies (one represented in red) and 5 clockwise parastichies clockwise 5 and red) in represented (one parastichies counter-clockwise 3 by characterized (3:5 phyllotaxis). 11 days later, as a result of the increase in the size of the apex, the phyllotactic pattern phyllotactic the apex, the of size the in increase the of result a as later, days 11 phyllotaxis). (3:5 has shifted to 5:8. However, the original 3 parastichies are still evident (one represented in red). in represented (one evident still are parastichies 3 original the However, 5:8. to shifted has (modified from Williams, 1974). Williams, from (modified The requirementforauxintransportorganformation(Okada Auxin istransportedthroughthetissuesbycellularimportand 2001),whereasPIN1ispartofafamilyeightmembers(Friml 1991;Reinhardt et al., et et al., et et al., et 1998).AUX1isamemberofgene 1995).Long-distancetransportmay et al., et 2000)highlightedtheneedto Left: 11 days after germination, the phyllotactic pattern is pattern phyllotactic the germination, after days 11 Left: 1996)andtheputativeefflux et al., et 2001),butinthe et 4 lular localisationofAUX1andPIN1intheshootapex as proposedinthe«auxin-sinkmodelofphyllotaxis(Reinhardt dia. Thesefindingsarecompatiblewithasinkfunctionofprimordia indicative ofdownwardstransportthroughthecentreprimor- auxin sinks(Reinhardt and providesevidenceforthehypothesisthatprimordiaactas with thenaturalauxinIAA(Reinhardt to formawhorlofseparated,evenlyspacedprimordiaifsupplied al., et (Vernoux nostic markergenesformeristem,organandboundaryidentity inferred fromthelossofphyllotacticexpressionpatternsdiag- expressed primarilyinthecellsofL can beexpectedtoaccumulateinthesecells.PIN1isalso abaxial epidermisofthedevelopingprimordia.Therefore,auxin the meristem(representingskinofmeristem)andin for meristempatterningandcangeneratedenovopatterns. active polarauxintransport,mediatedthroughPIN1,isnecessary substrate forPIN1,didnotinduceasimilarpattern.Thisshowsthat supply withthesyntheticauxinanalogue2,4-D,whichisnota of thispatternwasdependentonthePIN1gene.Moreover, that theunpatternedmeristemof the lowersideofcells,asinstem(Gälweiler corresponding tothedevelopingmid-rib)andbecomeslocalised restricted toanarrowcellfilealongthecentralaxis(probably of theprimordia.Later,PIN1expressioninprimordiabecomes primordia. Thisindicatesthelocaltransportofauxintocentre localized tothesideofcellsthatpointscentre PIN1 isinducedinincipientandyoungprimordia,whereit auxin accumulateattherightplacetoinducealeaf?Interestingly, explain howthemeristemissuppliedwithauxin,butdoes transported uptowardsthecentreofmeristemdome.Thiscan auxin whichisaccumulatedintheL the sideofcellsthatpointstomeristemcentre.Hence, A roleforactiveauxintransportinmeristempatterningis Taken together,thesedataindicatethatauxinistransportedin The influxcarrierAUX1isexpressedintheexternalL 2003;Figure4). et al., et 2000;Scanlon,2003).Moredirectly,itwasshown example, expressionintheL pears toresponddifferent inputs.For localisation? What regulatesPIN1expressionand lateral extension. neighbours, whichmayservetorestrictits main incompetitionwithitsdirect regulate furtherphyllotaxis,butitwillre- This willitselfstarttofunctionasasink late toallowanewprimordiumbeformed. the primordia,sufficientauxincanaccumu- ing primordia.Atacertaindistancefrom tion ispreventedinthevicinityofdevelop- istem bytheprimordiasuchthataccumula- and becomesredistributedwithinthemer- the meristemprimarilythroughL upregulated inyoungprimordia andits specific cues.Ontheotherhand, PIN1is meristem islikelyaresponse tocelltype et al., et The regulationofPIN1expressionap- 2003). pinoid 1 layerbyAUX1appearstobe et al., et 1 layer,butitisrestrictedto mutantscanbeinduced 2003).Thegeneration 1 et al., et layerofthe Arabidopsis 1 layerof 1998), 1 layer http://doc.rero.ch to theaccomodationofmoreorgansatatime.Interestingly, inthe example, anincreaseinthecircumferenceofapexcould lead controlling thesizeofPZorprimordia. For rate, therange,ordirectionofauxinflux,butindirectly, by could beregulatednotonlydirectlybyamechanismactingon the tion andphyllotaxis.Itisthereforeconceivablethatphyllotaxis ference andthewidthofPZinevitablyinfluenceorganforma- terning mechanism(Reinhardt meristem isindependentfromtheauxin-relatedphyllotactic pat- (Steeves andSussex,1989).Itappearsthatthissubdivision ofthe which encirclesthecentralzone(CZ),siteofstem cells terning (Sachs,1981;Berleth has beenpostulatedtooperateinauxin-mediatedvascularpat- may respondtoauxinfluxes.Suchapositivefeedbackmechanism porters. Inthecaseofphyllotaxis,PIN1-localisingmechanism phyllotaxis requirerapidandreliablereorientationofauxintrans- other hand,thedynamicsofpatterninginembryogenesisand mechanism maywellinvolveaself-reinforcingcomponent.Onthe Considering thestrong,stablenatureofcellpolarityinplants, system isinformedwhereontheplasmalemmatounloaditscargo. involved. Thequestionremainsofhowthevesiculartrafficking components withspecificityforPIN1canbeexpectedto which isageneralcomponentofvesiculartrafficking,additional ments masksrapiddynamicrecyclingofPIN1.BesidesGNOM, localization ofPIN1observedinimmunocytochemicalexperi- (endosomal) compartements.Hencetheseeminglystablepolar subcellular recyclingbetweentheplasmalemmaandinternal findings haveresultedintheviewthatPIN1issubjecttocontinuous then auxintransportitself(Geldner ing vesicletrafficking(andconsequentlyPIN1localisation)rather and thatwellcharacterisedauxintranportinhibitorsactbyinfluenc- vesicle trafficking,brefeldinA(BFA),abolishesPIN1localisation 2004). Theseresultscorrelatewiththefindingthatinhibitorof regulator ofGTPasesthatareinvolvedinvesicletrafficking(Geldner, regulation ofPIN1localisationisdisturbed.GNOMencodesa the preexistingprimordialeadstoauxinaccumulationatL auxin maythereforemediateitsreiterativenature:PIN1activityin downstream (asasubstrate)ofPIN1.Inthecontextphyllotaxis, effect meansthatauxinisbothupstream(asaregulator)and lated bycytokinin-dependentcontrol ofmeristemsize(Giulini putative cytokinin-sensor,indicating thatphyllotaxiscouldberegu- son andHake,1999).The phyllotaxis isassociatedwith an increaseinmeristemsize(Jack- abphyl1 What’s more? exhibit aparticularsubcellularlocalisation(Steinmann globular embryo,PIN1isfirstexpressedinallcellsanddoesnot expression isinducedbyauxin(Reinhardt basal dimension.Inthe cells justwhentheybecomeaxialisedandelongateintheapical- The firstsignofPIN1polarisationcanbeobservedinthecentral can influenceit’sownrouteoftransport. xylem parenchymacells,respondtoexogenousauxin.Thus,auxin that theroutingofvascularstrands,includingauxinconducting in turninducesPIN1toensureproperpositioningofL Leaves areformedintheperipheralzone(PZ)ofmeristem How isthesubcellularlocalisationofPIN1regulated?In mutantofmaize,thetransition ofdistichoustodecussate gnom abphyl1 et al., et mutant,thisprocessandthelater et al., et mutantcarriesamutationin 2000).Ithasbeenestablished 2000).However,thecircum- et al., et et al., et 2001;2003).These 2003).Thislatter et al., et 2 andsoon. 1 , which 1999). et al., et 5 distichous (Schwabe,1971;Reinhardt shoot apexareassociatedwithphyllotacticchangesfromspiralto as wellsurgicaltreatmentsthatleadtotheelongationof primordia ontothemeristem(Schwabe,1984).Indeed,chemical, be importanttodeterminetherangeofinfluencefrompreexisting consequence oflocalchanges(e.g.atL a globallevel(theentiremeristem)andpatternsemergeas growth inthemeristemisrequired.Instead,regulatedat According tothisidea,nodifferentialregulationofcellidentityand principal parametersinfluencingphyllotaxis(Green,1992,1996). els invokedforcessuchastension,compressionandshearthe phyllotactic mechanismshavebeenenvisaged.Biophysicalmod- 1984; Green,1992,1996;DouadyandCouder,1996).Twomajor patterns (Mitchison,1977;VeenandLindenmayer,Meinhardt, Computer modelsofphyllotaxis influence andtherefore,L 2004). Inthe primordia moveapartandaway fromthemeristemcentreuntila concentration. Astheapexgrows andexpands,thepreexisting sition ofallinhibitoryfieldsdefines thesiteoflowestinhibitor preexisting primordiatoestablish aninhibitoryfield.Thesuperpo- models isaninhibitorofleaf formationwhichemanatesfrom 1977; Meinhardt,1984).Thecentralcomponentofmost such regulate phyllotaxis(Mitchison,1977;VeenandLindenmayer, models inwhichdiffusiblesignalmoleculesareenvisaged to a whole(Green,1992,1996). eters thatresultfromthegrowthanddevelopmentofapex as and/or therateofauxintransport. meristem organizationortissuefeatureswhichaffecttherange only directlybyauxintransport,butmoregeneralchangesof tion, P compatible withtheinterpretationthat,duetoverticalelonga- (Leyser andFurner,1992;Clark also affected.Inthiscase,however,phyllotaxisbecomesirregular ference ofthemeristemisdramaticallyincreased,phyllotaxis i.4 oe o h euaino hloai yaxn (Left) Fig. 4.Amodelfortheregulationofphyllotaxisbyauxin. right side, a new sink is established that diverts auxin away from the from away auxin diverts that established is sink new a side, right Nature Publishing Group. the to Publishing basipetally Nature transported and absorbed is auxin L left), the the by (on primordia transported acropetally is auxin meristem, meristem. Reproduced with permission from Reinhardt Reinhardt from permission with Reproduced meristem. stem (left). On the rigth side, auxin can reach the peripheral zone and zone peripheral the reach can auxin side, rigth the On (left). stem induce organ formation. formation. organ induce It hasbeenpointedoutthattheverticalspacingofprimordiamay Computer modellinghasbeenemployedtoanalysephyllotactic A contrastingviewisrepresentedbythemajorityofother These examplesshowthatphyllotaxiscouldberegulatednot 2 becametooremotefromthemeristemtoexertaninhibitory clavata and (Right) 1 fasciata wasformedoppositetoP After induction of organ formation on the on formation organ of induction After et al., et mutants,inwhichthecircum- 1993,1995). et al., et 1 ) inbiophysicalparam- 1 layer. In the preexisting the In layer. 2005).Thiseffectis et al., 1 . 2003, © 2003, In the In http://doc.rero.ch Fig. 5.Phyllotaxisinthe requires regularityforoptimal function.Besidestheformationof the functionoffinalarrangement ofthematurefoliage,that it maybetheprocessofleafformation atthemeristem,ratherthen tion alsoexhibitdefectsinleaf positioning(seeabove).Therefore, positioning. Severalmutantsaffected intheprocessofleafforma- process of—leafinitiationisintimatelylinkedwiththephyllotactic leaf arrangement.Thestudyofformationhastaughtusthat the tic arrange-ment,representsaselectiveadvantageoverrandom may indicatethatregularityitself,ratherthanthespecificphyllotac- perception doesnotrequireprecisepatternsofleafformation. adjusted post-meristematically,indicatingthatoptimisationof light therefore tendtoshadeeachother.Also,leafpositionisfrequently are formedintwoorfourrowsalongthestem(Figure1A,C) and for distichousanddecussatephyllotaxis.Inthesecases,theleaves case ofspiralphyllotaxis(Niklas,1988),itcertainlydoesnot hold Niklas, 1988).Whilethisargumentisnotentirelyconvincing inthe the absorptionofsunlightforphotosynthesis(reviewedin been proposedthatspiralarrangementsofleavesmayoptimize of pollinators,butwhywouldleafpositionhavetoberegular?Ithas conceivable thatregulararchitectureisimportantfortheattraction random arrangementoforgans.Inthecaseflowers,itis gests thattheremustbeaselectiveadvantageofregularversus Why didregularphyllotaxisevolve? approached experimentally. role ofauxinandhelptoidentifyimportantissuesthatneedbe ment ofsuchmodelswillstimulateourcriticalthinkingaboutthe give amorerealisticrepresentationofphyllotaxis.Thedevelop- phyllotaxis whichincludeallknownparametersandthereforewill nism ofphyllotaxiscannowbeusedtodevelopnewmodelsfor recent establishmentofpolarauxintransportasthecentralmecha- port fortheinvolvementofadiffusibleinhibitorinphyllotaxis.The erate variousphyllotacticpatterns,thereisnoexperimentalsup- allowing leafformationtooccur.Althoughsuchmodelscanregen- threshold isreachedatthesiteoflowestinhibitorconcentration, from Veit Veit from a Instead of distichous (alternate) phyllotaxis, phyllotaxis, (alternate) distichous of Instead AB te1 The occurrenceofseveraldistinctphyllotacticpatternsinnature The dominanceofregularphyllotacticpatternsinnaturesug- shoot axis with irregular internodes (leaves were removed). Reproduced with permission with Reproduced removed). were (leaves internodes irregular with axis shoot et al., 1998, © Nature Publishing Group. Publishing Nature © 1998, terminal ear1 terminal ( te1 te1 )mutantofmaize.(A) exhibits irregular phyllotaxis. irregular exhibits Top view of a a of view Top 6 (B) proliferation anddifferentiation. flux?) andhowthesesignalsare translatedintotissuegrowth,cell auxin signalsareinterpretedbythecells(auxinconcentration or its owntransporters?Further,itwillbeimportanttofindout how trolled? Istherearoleforthesubstrateauxininlocalization of example, howisthelocalizationofauxintransporters con- future willbethenatureoffeedbackmechanismsinvolved. For and tissuepolarizationareintimatelylinked.Keyquestionsfor the the controlof“downstream”eventslikeleafgrowth,differentiation back ontothepatterningmechanism.Therefore,phyllotaxis and terning andthefollowingdevelopmentaleventsfeedcontinuously reiterative. Thishasimportantimplications:theresultof pat- pattern. Incontrasttothisview,phyllotaxisisnothierarchical but ing andlaterfortheappropriatedevelopmentofelements ofthe the notionthatseparatemechanismsareresponsibleforpattern- Mango, 1999).Suchahierarchicalviewofdevelopmenthasledto fate mapforeachindividualcellofthebody(Labouesseand divisions andcelldifferentiationevents,resultinginastereotyped tion ofdevelopmentisreflectedinaninvariantsequencecell tip aswellforthefinalarchitectureofentireshoot. phyllotaxis maybeimportantforoptimaldevelopmentattheshoot nodes (Okada phyllotaxis frequentlyexhibitirregularandsometimescurvedinter- In thiscontext,itisinterestingtonotethatmutantswithirregular the internode.Theresultinginternodewouldthereforebecurved. Acknowledgements Conclusions andOutlook (Pick, 1998).Inthecaseof segments oftheadultbodyincorrectspatialarrangement patterning eventsthatfinallyproducethedifferentspecialized the anteriorandposteriorpoleisfollowedbyasequentialseriesof the developmentof age mechanismsthatarehierarchicallyorganised.Forexample,in Lateral view of view Lateral Theoretical conceptsofbiologicalpatterningfrequentlyenvis- I wish to thank Cris Kuhlemeier, Przemek Prusinkiewicz and Beata and Prusinkiewicz Przemek Kuhlemeier, Cris thank to wish I te1 plant. et al., et side, therewouldbelesscellsfortheformationof whole. Forexample,ifcellsweredepletedonone could potentiallyaffectshootarchitectureasa tion ofthestem,animbalancecellnumber Since themeristemisresponsibleforforma- of organogeniccellsononesidetheapex. cells, thusavoidingdepletionorover-proliferation ing the‘meristemtooptimallyallocatefounder tive advantageoverrandomleafposition,allow- Here, regularphyllotaxismayrepresentaselec- replenish thecellsengagedinorganogenesis. of cellsattherightpositionandtimeto meristem hastoprovideexactlytherightnumber at specificsitesintheperipheralzone.Thus, rial fororganogenesis.Foundercellsareselected where theycontinuouslyproducenewcellmate- nance resideinthecentralzoneofmeristem, odes. Thestemcellsrequiredforself-mainte- self-maintenance andtheformationofintern- least twoadditionalimportantfunctions,namely leaves andflowers,themeristemcarriesoutat 1991;Veit Drosophila C. elegans C. et al., et embryo,theestablishmentof 1998;Figure5).Thus,regular , thehierarchicalorganiza- http://doc.rero.ch GELDNER, N. 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