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II. Morphogenesis of Hydathodes

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II. Morphogenesis of Hydathodes Botanical Studies (2006) 47: 279-292. MORPHOLOGY Study on laminar hydathodes of Ficus formosana (Moraceae) II. Morphogenesis of hydathodes Chyi-ChuannCHENandYung-ReuiCHEN* Institute of Molecular and Cellular Biology, National Taiwan University, Taipei, TAIWAN (ReceivedSeptember16,2005;AcceptedFebruary16,2006) Abstract.ThespatialandtemporalmorphogenesisoflaminarhydathodesinFicus formosanaMaxim.f. shimadaiHayatawasexaminedatlightandelectronmicroscopiclevels.Fourmainstagesofhydathode development,includinginitiation,celldivision,cellelongationanddifferentiation,andmaturation,can beidentified.Intheearlystageofleafdevelopment,theinitialcellsoccurinthenearbyregionofagiant trichome.Inthecelldivisionstage,epidermalinitialcellsundergoanticlinaldivisiontoformepidermalcells andwaterpores.Subepidermalinitialcellsundergoanticlinalandpericlinaldivisionstoproduceagroup ofcellswhichfurtherdifferentiateintoepithem,tracheidcells,andasheathlayerofhydathodes.During thecellelongationanddifferentiationstage,epithemcellsgrowintolobe-shapedcellsandseparatefrom adjacentcellsthroughschizogeny,causedbythearrangementofthecorticalmicrotubules,thesecretionof digestingenzymesactingonthecellwall,andtheforceandtensioninducedbycellgrowth.Thesefactors notonlycausetheformationoflobedcells,butalsoenlargetheintercellularspacesoftheepithem.Thelobed epithemcellsincreasethecontactregionsbetweenthecellandtheirenvironment.Duringthefinalstage, tracheidsgraduallymaturewithintheepithemanddeveloptheirconductivefunction,bywhichwaterpasses throughthewaybetweenvein-endsandwaterporestoproduceguttation.Thepathwayofepithemdirectional differentiationandmaturationstartsatthewaterporesandmovestowardtheregionofvein-ends.Guttation isassociatedwiththematurationofwaterpores,theepithemcells,andtracheid-ends.Thisstudyprovides anatomicaldataofdevelopmentaleventsasastructuralbasisforunderstandingthehydathode’sfunction. Keywords: Epithem;Ficus formosanaMaxim.;Hydathodes;Morphogenesis;Schizogenousintercellular space;Waterpore. INTRODUCTION functionofretrievingnutrientsolutesduringguttation (KlepperandKaufmann,1966;Dieffenbachetal.,1980; Guttation,theprocessofliquidwaterexudation,is Sperry,1983;Canny,1990;Wilsonetal.,1991). drivenbythehydrostaticpressure,handlesthewater Severalreportshaveindicatedseveralgenesexpressed equilibriuminxylem,andimprovesrootabsorptionof inhydathodes—includinggenesforacidicchitinase, nutrientsolutesforplantdevelopment(Pedersen,1993; herbicidesafener-induciblegeneproduct,pyrroline- TannerandBeevers,2001;deBoerandVolkov,2003). 5-carboxylatereductase,peroxidase,andthePHO1 Guttatedsolutionisexudedthroughthehydathodes proteins—andtheirfunctionsarerelatedtoplantdefense outofleaves.Generally,hydathodesareclassifiedas andsolutetransport(SamacandShah,1991;deVeylderet eitherepidermalorepithemalhydathodes(Haberlandt, al.,1997;Huaetal.,1997;GayandTuzun,2000;Wanget 1914).Theepidermalhydathodeismadeupofagroup al.,2004).Thesestudiesimplythathydathodesmightplay ofmodifiedepidermalcells,whichsecretewaterorsalt animportantroleinnutrientretrievalandplantdefense. outoftheleafthroughanactiveprocess.Theepithemal hydathodeconsistsofwaterpores,epithem,tracheid- Theoretically, a close relationship between the ends,andasheathlayer,anditsexudationofwateris developmentandfunctionofhydathodeforguttation causedbyrootpressurebelongingtothepassivetype. mustexist.Inotherwords,thestructuraldifferentiation The water pores are the modified stomata in hydathodes, andmaturationofthewaterporesandepitheminthe andtheyusuallyarenotregulated.Theepithemtissueof hydathodesarethebasisforjudgingwhenguttationis hydathodesarecomposedofamassofsinuousandthin- working.However,articlesabouthydathodedevelopment walled parenchyma cells that act as a filter and have the haverarelysurfaced,andonlyonehasemphasized epithemcellmorphogenesis(Galatis,1988).Itasserted *Correspondingauthor:e-mail:[email protected];Fax: thatthelobedepithemcellformationisdirectlyrelated 02-33662478. togroups’arrangementofcorticalmicrotubules.Our 280 Botanical Studies, Vol. 47, 2006 previousstudiesexaminedtheultrastructureofthelaminar Transmission electron microscopy hydathodesinFicus formosana(ChenandChen,2005).In Ultrathinsections(80nminthickness)werecutwith thepresentstudy,weusethetechniquesofLM,SEM,and adiamondknifeandpickedupontheformvar-coated75 TEMtoexaminethemorphogenesisofthehydathodes, meshgridsanddoublestainedwithaqueousuranylacetate with special emphasis on the spatial and temporal for25minandleadcitratefor5min.Thestainedsections differentiation of epithem cells. We have also quantified wereexaminedinaHitachiH-600transmissionelectron theareaofthehydathodeandthenumberofwaterpores microscope(TEM)at75kV. perhydathodethatoccurduringhydathodedevelopment. Suchdatawereprovidedtoillustrateandconfirmthe Scanning electron microscopy relationshipbetweenthematurityofhydathodesandthe validityperiodofguttation. Sample fixation and buffer washers were performed as describedabove,dehydratedthroughanethanolseriesup to100%ethanol,transferredtopureacetone,andcritical MATERIALS AND METHODS point-driedintheHitachiCriticalPointDryerHCP-2. Then,specimensweremountedonaluminumstabswith Plant material Ficus formosana Maxim.f.ShimadaiHayatawas plantedinpotsfilledwithsoilinthegreenhouseofthe BotanyDepartment,NationalTaiwanUniversity.Plants werewatereddaily,andanautomaticdevicerecorded temperatureandhumidity.Thegrowthdatafor5-15 successive leaves on the shoot were measured and recorded.Allleafgrowthdataweretransferredwiththe LMImethod(Chenetal.,2005),andthenregressedby agrowthcurvewiththesigmoidfunction(Figure1A). By analyzing the leaf growth curve through the first and secondarydifferentiationasshowninFigure1B,two refractivepointsofthesecondarydifferentiationLMI3.13 and8.37wereobtained.Basedonthesetworefractive points,wedividedthegrowthcurveintothreephases: the log, linear, and stationary phases. We identified four developmentalstages:LMIat-1.8wastheinitialstage, andthreeadditionalleafgrowthphasesrepresentedthe stagesofcelldivision,cellelongationanddifferentiation, andmaturation.Theseselectedsamplesofthe5-15 successiveleavesseparatedintofourdevelopmentalstages werecollectedforlightandelectronmicroscopicstudies andwereshownasthemarksinTable1.Eachleafsample includedthreepiecestakenfromthemiddleregionofleaf blade. Light microscopy Figure 1. Analysisofthefittedleaf-growthcurveofF. L e a f s a m p l e s o f F. formosana c o n t a i n i n g formosanaMaxim.f.shimadai Hayata by first and secondary achlorophyllous hydathodes were fixed with 2.5% differentiations.A,Bestfittedleaf-growthcurveregression glutaraldehydein0.1Msodiumcacodylatebuffer(pH withtheWeibullfunctionf(x);B,Graphsofthefirstand 7.0)for6hatroomtemperatureandthenwashedina secondarydifferentiation.Dashlineindicatesthegraphof rinsebuffer(0.1Msodiumcacodylatebuffer)thrice. first differentiation f(x)’; d (leaf length, cm)/dt plotted against -1 Washed materials were post fixed with 1% OsO4in0.1M time,andthemaximumis1.57cm(LMI) at5.57LMI.Solid cacodylatebuffer(pH7.0)for8hatroomtemperature, lineindicatesthegraphofthesecondarydifferentiationf(x)”, washedin0.1Msodiumcacodylatebuffer,anddehydrated d (leaf-length)/dt2plottedagainsttime,andthemaximumand inanacetoneseriesandembeddedinSpurr’sresin(Spurr, minimumare0.26cm•LMI-1(at3.13LMI)and-0.46cm•LMI-1 1969).Afterpolymerizationofresinat70°Cfor8h,the (at8.37LMI),respectively.Figureabbreviations:C,chloroplast; plasticsweretrimmedandpreparedforsectioning.For CW,cellwall;E,epithemcell;ER,endoplasmicreticulum;G, light microscopic observations, plastic sections 0.75 μm Golgibody;H,hydathode;IS,intercellularspace;L,laticifer thickwerecutwithglassknivesonaReichertUltracutE cell;M,mitochondrion;Mt,microtubule;N,nucleus;O,water ultramicrotome, stainedwith1%toludineblue,observed poreaperture;P,peroxisome;PD,plasmodesmata;PT,palisade underaZeissPhotomicroscopeIII,andphotographedwith tissue;S,starch-containingplastid;SG,salt-glandulartrichome; SL,sheathlayer;ST,spongytissue;T,trichome;TC,tracheid KodakTMAX100. cell;V,Vacuole;VB,vascularbundle;WP,waterpore. CHEN and CHEN — Morphogenesis of hydathodes 281 Table 1. ThedevelopmentalstagesofthetestedleavesofFicus formosanaMaxim.f.shimadaiHayata. Leafnumber Leaflength Leafmeasuring-interval Phaseofleafgrowthcurve Developmentstageofhydathode (acropetally) (cm) index(LMI) 5* 11.4 14.3 Stationary Maturation 6* 10.7 13.2 Stationary Maturation 7 11.2 11 Stationary Maturation 8 12.2 10 Stationary Maturation 9* 11.5 8.6 Linear Cellelongationanddifferentiation 10 8.8 6.8 Linear Cellelongationanddifferentiation 11* 6.3 5.4 Linear Cellelongationanddifferentiation 12* 3.1 3.2 Linear Cellelongationanddifferentiation 13* 1.8 1.6 Log Celldivision 14* 1.1 0.2 Log Celldivision 15* 0.7 -0.8 Log Celldivision 16* 0.5 -1.8 Log Initial 17* 0.3 -2.8 Log Initial *Leaveswerecollectedforembeddingandsectioning. silverpaste,coatedwithpalladium-goldinanion-sputter collectedandseparatedintofourdevelopmentstages: coater(EikoEngineering,Ltd.IB-2ioncoater),and theinitial,thecelldivision,thecellelongationand viewedinaHitachiS-520SEM. differentiation,andthematurationstages.Meanwhile,the growthcurveofthehydathodeareaandthenumberof Cleaning method waterporesineachhydathodewereobtained(Figures2, Venationwasstudiedwithclearingleavesbyusing 3).Theyweresigmoidtype,andtheirgrowthratespeaked thetechniqueofShobeandLersten(1967).Leafblades at3.3and4.7LMI,respectively. were first cut to a size of 2 ×1cm2,depigmentedin70% ethanolsolution,bathedinboilingwaterfor10to30min, Laminar hydathode development of F. andthenplacedin5%aqueoussodiumhydroxideat60 formosana observed by SEM °Cuntiltheywerepartiallycleared.Subsequently,they
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