POLLINATION REGULATION OF FLOWER …...fruit development. Thus, pollination delineates...

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O’NEIL LPoll ination-regulateddevelopmentAnnu.Rev. Plant Physiol. Plant Mol. Biol. 1997. 48:547–74Copyright© 1997by AnnualReviewsInc. All rightsreserved

POLLINATION REGULATION OFFLOWER DEVELOPMENT

SharmanD. O’NeillSection of Plant Biology, Division of Biological Sciences, University of California,Davis, California 95616

KEY WORDS: auxin, ethylene,gametophytedevelopment, ovuledevelopment, senescence

ABSTRACT

Pollination regulatesasyndromeof developmental responsesthat contributestosuccessful sexual reproduction in higher plants. Pollination-regulated develop-mentaleventscollectively preparetheflowerfor fertilizationandembryogenesiswhilebringing about thelossof floralorgansthat havecompleted their functionin pollen dispersalandreception. Components of this process includechangesin flowerpigmentation, senescenceand abscissionof floral organs, growth anddevelopment of the ovary, and, in certain cases,pollination alsotriggers ovuleandfemale gametophyte development in anticipation of fertil ization. Pollina-tion-regulateddevelopment is initiatedby theprimary pollination event at thestigma surface, but because developmental processes occur in distal floralorgans,the activity of interorgan signals that amplify and transmit theprimarypollinationsignal to floral organsis implicated. Interorgansignaling and signalamplifi cation involvesthe regulation of ethylenebiosynthetic geneexpressionandinterorgantransport of hormonesandtheir precursors. Thecoordination ofpollination-regulated flower developmentincluding gametophyte, embryo,andovary development; pollination signaling; themolecular regulationof ethylenebiosynthesis; andinterorgan communicationarepresented.

CONTENTSINTRODUCTION..................................................................................................................... 548POLLINATION REGULATESA SYNDROME OFDEVELOPMENTAL EVENTS.......... 549

PollinationRegulationof Perianth Senescence.................................................................. 549PollinationRegulationof Floral Pigmentation Changes.................................................... 551PollinationRegulationof FemaleGametophyteDevelopment........................................... 552PollinationRegulationof EmbryoDevelopment................................................................. 555

PollinationRegulationof OvaryDevelopment................................................................... 555POLLINATION SIGNALS...................................................................................................... 556

Primary PollinationSignals................................................................................................ 557Secondary Poll ination Signals............................................................................................. 559

REGULATION OFETHYLENEBIOSYNTHESISIN POLLINATED FLOWERS............. 561PollinationRegulationof ACCSynthase.. ......................................................................... 562PollinationRegulationof ACCOxidase... ......................................................................... 564

MODEL FORINTERORGANCOORDINATION OFPOLLINATION-REGULATEDFLOWERDEVELOPMENT........................................................................................... 565

CONCLUSIONSAND FUTURE DIRECTIONS.................................................................... 567

INTRODUCTION

Pollination regulatesa complexsyndromeof developmentaleventsin manyflowers.Becauseperianthsenescenceis themostvisible manifestation of thispollination-regulatedflower developmentandbecauseof its horticultural im-portance,a preponderanceof the researchfocusedon this phaseof flowerdevelopmenthas beenon wilting and abscissionof the corolla and calyx.However,this review focuseson the broadercontextof pollination-regulateddevelopmentalresponsesthat collectively leadto thesheddingof somefloralorgansthathaveservedtheir function in pollendispersalandreceptionwhilesimultaneouslypreparingother organsfor fertilization, embryogenesis, andfruit development.Thus,pollinationdelineatesprepollination flower develop-ment—during which the flower is specializedfor pollen dispersalandrecep-tion—from postpollination development—wherebythe flower becomesspe-cializedto ensurefertilization andnourishmentof thedevelopingembryoandseed.Developmentalprocessesassociatedwith this functional transition in-clude senescenceof the perianth,pigmentation changes,ovary maturation,ovule differentiation,andfemalegametophyte development.It hasbeenpro-posedthat perianthsenescenceand color changesof floral organsserveassignalsfor insectpollinatorsto discriminatereceptiveflowers from thosethathaveadvancedto later stagesof reproductivedevelopment, whereaspollina-tion regulationof ovule maturationservesto coordinatedevelopmentof themale and femalegametophyteafter a point wherefertilization is all but as-sured.In additionto theproposedecologicalsignificanceof pollination-regu-lated flower development, processesassociatedwith pollination-regulatedflower developmentareimportant horticulturally andoften result in a reduc-tion of the commercialquality of flowers. Severalprevious reviews haveaddressedsenescenceandpostharvestphysiology of flowers(13, 50,51), andpollination-regulatedflower developmenthasrecentlybeenreviewedfrom ahorticulturalperspective (116).

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The transition from prepollination to postpollinationdevelopment canoc-cur in the absenceof pollination as part of a temporalprogramof flowerdevelopment.However,in manyflowersthisdevelopmentaltransitionis eitherstrictly regulatedby pollinationor is acceleratedby pollination. Flowersthatdemonstratestrict pollination regulationhaveservedasexcellentmodelsys-temsto dissectthesignalsthat regulatethedevelopmental transition. A majorresearchgoalhasbeento understandthesignalsthatcoordinatediversedevel-opmental responses set in motionasthe flowerundergoes the transitionfrom aprimary role in pollen dispersaland receptionto that of fertilization andnurturing the developingembryoand seed.Becausethesediversedevelop-mentalprogramsoccurin distinct floral parts,interorgansignalsthat coordi-natetheoverallprocessareimplicated.This reviewfocusesonthecurrentstateof knowledgeof the processesand signalsthat coordinatepollination-regu-lated flowerdevelopment.

POLLINATION REGULATESA SYNDROMEOFDEVELOPMENTAL EVENTS

In manyflowers,pollinationregulatesa syndrome of developmenteventsthatcollectivelypreparetheflower for fertilizationandembryogenesiswhile shed-ding organsthat havecompletedtheir function in pollen dispersalandrecep-tion. Components of this pollination-regulatedsyndromeinclude changesinflower pigmentation, senescenceandabscissionof floral organs,andgrowthanddevelopmentof theovary.Pollination-regulateddevelopmental eventsareinitiated by a single event—pollination—but becausethey occur in distinctfloral organsthe activity of interorgansignalsthat amplify and transmit theprimarysignalto distalfloral organsis alsoimplicated.

PollinationRegulationof Perianth Senescence

A predominantfeatureof pollination-regulateddevelopmentis perianthsenes-cence, althoughthis process isstrictly regulatedby pollination in only aminority of species.More typically, senescenceoccursgraduallyaspart of atemporalprogramof flower developmentthat may beacceleratedby pollina-tion, although thereareextremeexamples,suchasdaylily flowers, in whichthe perianthsenesceswithin 12–18h after flower openingregardlessof theirpollination status(79,85). In flowersthatexhibit eitherpollination-dependentor pollination-acceleratedsenescence,pollination leadsto a rapid increaseinethyleneproductionresembling theclimactericresponseobservedin ripeningfruits (16,53, 117).In theseflowers,which includePetunia,carnation,cycla-

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men,andorchids,perianthsenescenceoccursin concertwith the increaseinendogenousethyleneproduction andcanbe preventedby treatmentsthat in-hibit ethyleneproductionor perception(18, 53,54, 106,107,111,124,159).

Very early studiesfirst noted the sensitivity of the perianth ofcertainflowersto ethylene (26).In thesestudies,treatmentof Cattleyaflowerswith aslittle as 2 ppb of ethylenefor 24 h inducedsenescencesymptoms that wereidenticalto “dried-sepalinjury,” a physiologicaldisorder thatdevelopedin theperianthof orchid flowers.This disorderwasinferredto becausedby exoge-nousethylenein greenhouses.Theassociationof endogenousethyleneproduc-tion with perianthsenescencewas madesomewhatlater during study of thefloral color changesthataccompanypollination-regulateddevelopmentin an-other orchid species,Vandacv. Miss AgnesJoaquim(2). It was notedthattheseflowersproducedethyleneendogenously, andit wascorrelatedwith thefloral color changes.Furthermore,the floral color changewasacceleratedbyexogenousethylene,suggestingthatendogenousethyleneproduction triggeredcolor fading and, by inference,also triggeredperianthsenescence(2). Theeffectsof exogenousethylenein this Vandacultivar could be mimicked byemasculationor by pollination, and this further indicatedthat this initial de-scriptionof ethylene-regulatedflower senescencereflecteda pollination-regu-latedprocess(SD O’Neill, unpublishedobservations). It is now well knownthat ethyleneplays an important rolein coordinatingpollination-regulatedperianthsenescencein manyflower species,anda numberof orchid specieshavebeenparticularlywell characterizedin this regard.For example,emascu-lation, pollination, auxin treatment,or woundingof orchid flowersstimulatesethyleneproductionandinducesperianthsenescencein severalorchidgenera,includingArachnis, Aranda,Cattleya,Cymbidium,Dendrobium,Paphiopedi-lum, Phalaenopsis, andVanda(2, 7, 20, 26, 27, 43, 58, 102–104,117, 118,165,168,175).Comprehensivestudieshavedemonstratedlargevariability insensitivity to ethyleneamongdifferent orchid specieswith Vandacv. MissJoaquimreportedto be the mostsensitive to ethylene(43). Cymbidium,Cat-tleya,andPaphiopedilumweremoderatelysensitiveto ethylene,whereasDen-drobiumandOncidiumwere relativelyinsensitive. Manyother flowerspecies,such as carnation,are also similarly sensitive to ethylene,with exogenouspropylene(an ethyleneanalog) promoting a pattern of sustained ethyleneproductionandsymptomsof perianthsenescencesimilar to endogenousethyl-eneproductionandsenescencesymptomsinducedby pollination (110).Theseresultssupporttheconclusionthatethyleneis sufficientto promotethepatternof pollination-regulatedperianthsenescencethat is observedin a numberofflowers, including orchid,carnation,andPetunia.

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Perianthsenescenceis anactiveprocessthat is accompaniedby changesingeneexpression(13, 77, 78, 170).ThreecDNAs (SR5,SR8,andSR12)wereinitially isolatedfrom senescingcarnationpetals.Two wereregulatedby eth-ylene andthe thirdby bothethylene andby temporalcues(77, 78). Twoof thesenescence-relatedcDNAs are likely to encodeβ-galactosidase(SR12)andglutathione S-transferase(SR5)(90). The potential role of β-galactosidaseinsenescingflower petalsis likely to be in cell wall disassemblythataccompa-nies most senescenceprocesses.The role of glutathione S-transferasewassuggestedto bein thedetoxificationof lipid andDNA hydroperoxidesassoci-atedwith senescence-inducedoxidativeprocesses(146).As discussedbelow,genesencodingkey ethylenebiosynthetic enzymesarealsoregulatedby polli-nationandassociatedpollinationsignalsin severalflower species,thusprovid-ing the signaling linkagebetweenpollination,ethylene,andthe regulationofgenesthat contributeto perianthsenescence(101,117,119,147,149).Over-all, theseresultsindicatethat specificbiochemical eventsareregulatedat thelevel of geneexpressionduringperianthsenescenceandthat thesegenes,likethe overallprocess, are regulatedby ethylene.

PollinationRegulationof Floral PigmentationChanges

It hasbeenreportedthat over 74 angiospermfamilies exhibit floral pigmentchangesin responseto pollination or flower agingandproposedthatpollina-tors recognizecolor changesand preferentiallyvisit previouslyunpollinatedflowers (44, 157). Pollination can induce diversepatternsof pigmentationchangesincluding color fading, enhancedpigmentation, or intensification ofpigmentation in discreetspots.In Cymbidium orchid flowers, pollination in-ducesanthocyaninformation, and this processhasbeenwell studiedas thefirst visible manifestation of pollination-regulatedflower development thatalsoleadsto perianthsenescence(4–9,166,167).The changein Cymbidiumlip colorationcanbeacceleratedby pollination,emasculation,or treatmentofthestigmawith auxin(7).Subsequentstudiesin Cymbidiumalsodemonstratedthat a small incision at the baseof the lip preventedemasculation-inducedcolorationand that treatmentof completelyexcisedlips with 1-aminocyclo-propane-1-carboxylicacid (ACC) or ethylenepromotedanthocyaninaccumu-lation,suggestingthat lip colorationresultedfrom thetranslocationof ACC tothelip whereit wasconvertedto ethylenein situ (167).Pigmentationchangesin Vanda orchid flowers are also associatedwith pollination and ethyleneproductionbut, in contrastwith Cymbidium, Vanda flowers undergorapidcolor fading (2). In lupine flowers, thecolor of thebannerspotchangesfromyellow to magentaasthe flower ages(140).This changein bannerspotcolor


also appearsto be regulatedby ethyleneand is most likely acceleratedbypollination. The changein bannerspotcolor precedesflower wilting by sev-eraldaysandmayserveto maintain theattractivenessof a largefloral displayfrom a distancebut still provide a signalfor pollinatorsat close range.

Relatively litt le is knownaboutthespecificbiochemical eventsthatunder-lie the processof floral pigmentation changes,althoughcertainfloral organpigmentation changeshavebeenassociatedwith carotenoidor anthocyaninbiosynthesis (95),anthocyanindegradation(126),or changesin tissuepH (10).Becauseof thediversity in patternsof pigmentationchangesthatarepollina-tion regulated,it is likely thatdifferentbiochemicalmechanisms contributetothe changesobservedin different flowers. It hasbeensuggestedthat pollina-tion-regulatedcolor changesevolvedindependentlyin angiospermsmanydif-ferenttimes (157),suggesting thattheunderlying biochemicalmechanismsarelikely to differ amongtaxa.

PollinationRegulationof FemaleGametophyteDevelopment

The endresultof pollination is fertilization, which leadsto zygoteformationandsubsequentembryogenesis, all of which havebeenreviewedextensively(14, 62, 68, 86, 88, 94, 114,128,130). In somespecies,femalegametophytedevelopmentis incompletebeforepollination, andthe pollination eventitselfregulatesovule and gametophyte initiation, development,and maturationinpreparationfor subsequentfertilization. In certainorchidssuchas Cattleya,Sophronitis, Epidendron, Laelia, Phalaenopsis, Dendrobium,and Doriti s,ovulesarecompletelyabsentin unpollinatedovaries,andtheirdevelopmentistriggeredby pollination(29,30,65,133,173,174,176).In manyotherorchidgenuses,suchasCypripedium,Paphiopedilum,Phragmipedium,Herminium,Epipactis,andPlatanthera,ovuleprimordiaarepresentbeforepollination butremainsuspendedat a premeioticstageuntil pollinationtriggersfurtherovuledevelopment(29, 36, 37, 138). In still otherorchid species,immature ovuleprimordiaarepresentat anthesisthat havenot yet progressedto the stageofarchesporial celldifferentiation(38,76).

Pollination-regulatedovule initiation and developmenthas beencharac-terizedin detail in Phalaenopsis (176).Within two daysafterpollination andbeforepollentubegermination, cell proliferationis initiatedalongtheplacen-tal ridgesof theovary.The placentalridges continue to elongateand branchtoform thousandsof finger-like ovuleprimordiaby approximately 40 daysafterpollination,a time still well in advanceof fertilization.At this stage,theinnerintegumentappearsasacollarlikegrowth nearthetip of theprimordia,andtheouterintegument is initiated shortly thereafter.The archesporialcell enlarges

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further to form the megasporocytethat, following meiosis,gives rise to theexpandingmegaspore.Subsequentmitotic divisionsresultin thedevelopmentof a Polygonum-type embryosacin this orchid species(14, 163, 176). Theelapsedtime betweenpollination andmaturationof theovuleandfinal fertili -zationis approximately80 daysin Phalaenopsis. Theprogressionof pollina-tion-regulatedovule developmentin Phalaenopsisis illustratedin Figure 1.The initial stagesof ovule differentiation, namely cell proliferation in theplacentalridge, occursbefore pollen tube germination,suggesting that theinitial signalsfor ovule initiation arisefrom the pollination eventandarenotdependentonpollengerminationor tube growth. Thestrict regulation ofovuledevelopmentby pollinationresultsin the synchronousdevelopmentof thou-sandsof ovulesin thePhalaenopsisovary(176).Thesynchronousovuleshaveprovidedthebasisto dissecttheprocessof ovuledevelopmentat themolecularlevel and to isolatea numberof geneswhoseexpressionis correlatedwithdiscrete stagesof ovuledifferentiation(100).

Theuniqueregulationof megagametophyte developmentby pollination ina numberof orchid specieshasbeenrelatedto their reproductiveecology.Agenerallyheld view is that orchid ovule development is not initiatedbeforepollination becauseof the low probability of pollination by highly specific

0 1 4 5.5 6.5 7 11

OVULE DEVELOPMENTFLOWERDEVELOPMENT

SEEDDEVELOPMENT

Weeks after Pollination:

Meiosis

Embryo Sac FormationPerianth Senescence

Fertilization

Pollen TubesFirst Enter Ovary

Archesporial CellDifferentiates

Integument Development

Ovule PrimordiaGrow and Branch

Ovary GrowthInitiates

Megasporocyte

Figure 1 Poll ination regulation of ovule development in Phalaenopsis. The timeline of ovuledevelopment beginningwith theevent of poll inationandending with fertilizationis presented. Thespanof time during which various developmental changesoccur is indicatedbelow the timeline.Anatomicaldiagramsacrossthetopdepict thedevelopmentalstageof theovuleprimordia,immatureovule,andfinally, the mature ovule containing the femalegametophyte (modif ied from Reference100).


pollinators, compoundedby the large investmentrequiredfor megagameto-phyteandovary maturation.The orchid reproductivestrategyonly investsinfemalereproductivedevelopmentafter pollination,whenfertilization is all butassured.Thevariationobservedin thestageof ovuledevelopmentat thetimeof anthesisin different orchid taxa has also beenproposedto relate to theenvironmentin which they grow (144). For example,epiphytic orchidsthatgrow in areaswherethegrowing seasonis long canafford theextendedtimenecessaryfor completepostpollination ovuledevelopment,whereasterrestrialspecies growing in temperate regions with a short growing season mustachievepartial femaledevelopmentbeforeanthesisto completethereproduc-tive cycle withintheseason.

Pollination regulationof megagametophytedevelopmentis not confinedtoorchidsbut is a featureof manyhigherplant reproductivesystems.In manyspeciesmegagametophyte developmentis almostcompletebeforepollination,and the final differentiationof cells of the megagametophyte is triggeredbypollination. For example,in Prunus dulcis (almond),ovule developmentisarrestedat themegasporocytestagebeforeanthesis,with furtherdevelopmentand enlargementof the megagametophyte occurring only after compatiblepollination (123). Studiesof ovule developmentin other Prunusspeciesinwhich the megagametophyte is immatureat anthesisindicatesthat the polarnuclei donot fuse beforepollinationandthatthis eventis pollination regulated(31, 32, 123). Experimentswith cotton ovule culture have shown that theadditionof 5.0 µM IAA to the culturemediacaninducepolar nuclei fusion,suggestingthatauxinsuppliedby thepollenmaybea naturalsignalinducingpolar nuclei fusion and perhapsother biochemicaleventsin preparationforfertilization(66).

Recently,andunexpectedly,it wasshownthat theeggcell of mostovulesin Zeamaysis not morphologically matureat thetime of pollination (96).Thefinal eventsof eggcell maturationarecompletedin themajorityof ovulesafterpollination but beforefertilization,suggestingthatpollensignalsareresponsi-ble for inducing the final stagesof megagametophyte developmentin thisspecies as well.

In barley,pollination triggerssynergiddegenerationbefore the pollentubesreachedtheovule,which allowsthepollentubeto penetratethemegagameto-phyteduring fertilization (93). It hasalsobeenshownthat calciumaccumu-latesin thesynergidsin responseto pollination.It hasbeensuggestedthatthisplaysa role in establishing a chemotropicgradientto attractthe pollen tubeand/orin causingthepollentubeto burstafter it entersthesynergidto releasethespermcells (22, 23, 56). It hasalsobeensuggestedthata signalfrom thepollen tube is communicated over ashort range to the ovuleto promote

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synergiddegenerationin Nicotiana (63). A possiblecandidatefor the pollentube–derivedsignal in this casewas suggestedby experimentsusing cottonovuleculturein which 0.5 µM gibberellin inducedsynergiddegenerationin amannersimilar to thatafterpollination (66), althoughotherhormonesassoci-ated withthepollentube mayalsocontributeto this signalingfunction(89).

PollinationRegulationof Embryo Development

Several studieshave demonstrated thatapomictic embryodevelopmentinsomespeciesis dependenton pollination. For example,in the orchid Zy-gopetalum,pollen from an incompatible species,Oncidium,that wasineffec-tive in fertilization, neverthelesstriggeredapomictic seedproduction (143).This requirement forpollinationto induceapomictic embryodevelopment wasconfirmedin anotherorchidspecies,Orchis(49).A seriesof theseandrelatedobservationsled to an early interpretationthat pollen-bornechemicalsub-stancesinducedovary growth that thenindirectly promotedembryodevelop-ment evenin the absenceof fertilization (48). Other examplesof apomicticembryodevelopment that aredependenton pollination includethe apomicticgrassPennisetum setaceum,which increasesthe set of apomictic embryoswhenpollinatedwith P. ciliare pollen,eventhoughthis pollendoesnot resultin fertilization (12, 136).Gamma-irradiatedpollen that is inefficient at fertili -zationinducesa low percentageof haploidembryosto developin applethatarepresumedto be apomictic(177).Overall, theseobservationsindicatethatwhile pollinationis not sufficient to induceembryogenesisin all species,it isrequiredfor apomictic embryodevelopment in severalplant speciesthat arepredisposedto produce apomicticembryos.

PollinationRegulationof OvaryDevelopment

Ovary developmentafter pollination dependsupona supply of auxin that istypically derivedfrom developingovulesand seeds(47). In the absenceofpollinationandembryogenesis,certainsolanaceousspeciessuchastomatoandPetuniacould be inducedto form matureseedlessfruit by treatmentof theovarieswith auxin (45). Extractsof pollen could mimic the effect of auxin,leadingto theproposalthatpollencontainedauxinandthatcontributedto theinitiation of ovarygrowth (46, 72–74).Unlike therole of developingseedsinpromotingovarygrowth, therole of pollination asa primaryeventregulatingovaryandfruit developmentis lessfirmly established.Earlystudiesof pollina-tion-regulatedorchid developmentidentified changesin the curvatureof theovaryto beoneof theearliestpollination-regulateddevelopmentalevents(29).More recently,pollination regulationof cell division in theplacentalridgehasbeenimplicatedin the formation of hair cells that expandthe centralovary


cavity (176). Thesemorphological changesoccur approximatelythreedaysbeforepollengerminationandclearlydemonstratethatpollination itself, ratherthan fertilization, triggers the initial stagesof ovary development. Exo-genouslyappliedauxin and inhibitors of ethylenebiosynthesisdemonstratedthatthe elaborationof ovarywall haircells,the earliestmorphological change,wasdependenton bothauxinandethylene(176),suggesting thatpollen-borneauxin can be translocatedto the ovary (141). Pollination effects on ovarydevelopmentarenot restrictedto orchidsandhavebeenreportedin manyotherplant species, includingmuskmelon ovaries,whichdoubled insizewithin 48hafter pollination (80), as well as in Brodiaea and carnation, whereovaryexpansionwaspromotedby ethylenetreatment,which alsopromotedperianthsenescence (55,108,109,112, 113).It is possible that ovarygrowthresponsesweredirectly relatedto mobilization of carbohydratefrom thesenescing petalsto theovary andwerethusonly indirectly related topollination.

POLLINATION SIGNALS

Pollinationis first perceivedat thestigmatic surface, andpollination-regulateddevelopmentaleventsareinitiatedbeforepollengerminationor penetrationofthe style by the growing pollen tube. This suggeststhat a physical eventclosely associatedwith the pollen-stigma interactionor a pollen-bornesub-stanceis responsiblefor initiating pollination-regulatedflower development.In mostspecies,the primary pollination eventis accompaniedby an increasein ethyleneevolutionin thestigmaandstylewithin hoursafterpollination andwell beforepollengermination (39,40,42,82–84,97,110).In self-incompat-ible species, pollinationresponsesdiffer betweencompatibleandincompatiblepollinations,andthis hasprovidedsomeinsight to theprimaryandsecondarysignalsthat operatein pollination-regulatedflower development.Compatiblepollination in Petunia results in two distinct phasesof ethyleneevolutionoccurringafter approximately3 and20 h, respectively,whereasself-pollina-tion triggersonly the first phaseof ethyleneproduction(81, 137). The earlyphaseof ethyleneevolution wasattributedto directconversion ofpollen-borne1-aminocyclopropane-1-carboxylic acid (ACC) to ethyleneand the secondphaseof ethyleneevolution to endogenoussynthesisof ACC in floral organsdistalto thestigma.Theseresultsimplicatetheinvolvementof aprimary andasecondarysignalin thepollination response,thefirst of which is perceivedinthe stigma followed by a subsequentsecondarysignal that transmitsandamplifiestheprimarypollination signalto distal floral organs(115).Althoughit is likely thattheprimaryandsecondarypollination signalsaredistinct, theyarebothlinked to ethyleneevolution.

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Primary PollinationSignalsThe primary pollination signal has beenproposedto result from physicalcontactbetweenthe pollen and stigma, from pollen tube penetrationof thestigma(40, 41), or from pollen-bornechemicalmessengers(60, 137,159).InPetunia,carnation,and orchid flowers, the initial responseto pollination israpidethyleneevolution by thestigma.In eachcase,pollination-inducedethyl-eneevolution precedesgerminationof thepollentube, suggestingthatpenetra-tion of the stigmaticsurfaceby thepollentube isnot requiredfor theinductionof ethylenebiosynthesis (20,42,54,59,110,117).Furthermore,mockpollina-tion of orchidflowerswith latexbeads,apollensurrogatethathasbeenusedtostudy the role of the stylar matrix in pollen tube extension(135), failed totriggerethyleneproductionor anyotherpollination responses,indicating thatphysicalcontactaloneis insufficientto induceanycomponentsof thepollina-tion-regulateddevelopmental syndrome (176). The preponderanceof resultssuggeststhat physicalcontactbetweenthe pollen and stigma, or woundingreactionsassociatedwith pollen tubegrowth, arenot the primary pollinationsignals,andconsiderableexperimentalattention hasthusfocusedon theiden-tification of a pollen-bornechemicalthat may serveasa primary pollinationsignal. Chemicalsthat have beenidentified in pollen include ACC, auxin,pecticoligosaccharides,brassinosteroids,andmethyl jasmonate,all of whichare known inducersof ethylenebiosynthesis,making them attractivecandi-datesfor the primary pollen signalmolecule (3, 28, 33, 67, 71, 92, 131,134,151,152, 154,156,162,172).

Shortly after the identification of ACC asthe immediatebiochemicalpre-cursor of ethylene(1), severalreportsidentified its presencein pollen andsuggestedthatACC maybe theprimarypollensignal(127,158).Therole ofpollen-borneACC in triggeringtheinitial burstof ethyleneproductionanditspotentialtranslocation toother floral organs hasnow beenextensivelystudied,especiallyin modelsystemssuchasPetuniaandcarnation(158–161).In spiteof its presence in relativelylargequantitiesin some pollen (127, 137, 158), therole of ACC in supportingthe initial ethyleneproduction in the stigma hasbeencontroversial.For example,Hoekstra& van Roekel (60) reportedthatACC contentof pollen from varioussourcesis not well correlatedwith thelevel of pollination-inducedethyleneproduction, andseveralreportsindicatedthat treatmentof thestigma with aninhibitor of ACC synthase,aminoethoxy-vinylglycine (AVG), beforepollination preventedpollination-inducedethyl-eneproduction(61,117,169,176).Thus,thesereportssuggestedthatpollina-tion-inducedethyleneproductionis derivedfrom endogenousproductionofACC ratherthanfrom exogenouspollen-borne ACC. In contrast,Singhet al


(137) reportedthat wide variationsin pollen-borneACC contentin differentPetuniagenotypeswerewell correlatedwith theinitial peakof pollination-in-ducedethyleneproductionand that this early ethyleneproductionwas notinhibited by a diff erent inhibitor of ACC synthase, aminooxyacetic acid(AOA). Thus,thesedatasuggestedthat pollen-borneACC wasthe substratefor initial pollination-inducedethyleneproduction in Petunia (137). Otherreportshavesuggestedthatthequantityof pollen-borneACC would bevastlyinsufficient to supporttheamountof ethyleneproducedin thestigma follow-ing pollination (139),andtwo reportsindicatethatdiffusion of ACC from thepollen is likely to be restrictedunderconditions that prevail in vivo, whichwould further restrict its availability to supportethyleneproduction in thestigma(60,121).Although theconflictingdataindicatethatpollen-borneACCcannotaccountfor the initial pollination-inducedethyleneproductionin thestigmaof all flowers, it is possible thatexogenouspollen-borneACC mayberesponsiblefor initiating ethyleneproductionin the stigma of at leastsomeflowers,andthis earlyethyleneproductionmaybesubsequentlyenhancedbyautocatalyticproductionof ACC in the stigma.

The contribution of pollen-borneACC to pollination regulationof flowerdevelopmenthasalso beentestedby exogenousapplication of ACC to thestigma(61,117,127).In eachcase,ACC promotedaninitial burstof ethyleneproductionbut did not acceleratewilting or perianthsenescenceunlessex-tremelyhighconcentrations wereused.ACC isnotdetectablein orchidpollen,yet pollination inducesrapid and high levels of ethyleneproductionin thestigma(117). In Petunia,compatiblepollination elicited two phasesof ethyl-eneproductionandcausedrapidperianthsenescence,whereasself-pollinationonly triggeredthe first phaseof ethyleneproduction,andperianthsenescencewasdelayedeventhoughboth compatibleandincompatible pollencontainedACC (137). Collectively, the data suggestthat pollen-borne ACC is not auniversalprimary pollen signal that is sufficient to elicit the full pollination-regulateddevelopmental response.Nevertheless,evensmallamounts of ACCmaytriggerautocatalyticethyleneproductionin thestigma andthusmayplaya role intriggeringtheinitial burstof ethyleneproductionin someflowers.

A numberof potentialprimary pollen signalshavebeentestedfor theircapacityto induceethyleneproductionandstigma closure,two earlypollina-tion-regulatedresponsesin Phalaenopsisorchid flowers (JA Nadeau& SDO’Neill, unpublishedobservations).Pollen-derivedproteins,systemin (120),pollen-derivedlipids, flavonoids,methyl jasmonate,and jasmonicacid wereall eliminatedaslikely candidatesbecausethey failed to elicit eitherethyleneproductionand/orstigmaclosureover a time frameconsistentwith a role inpollination signaling.Only auxin (both IAA andNAA) wasactivein trigger-

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ing ethyleneproductionandstigmaclosurein this orchidbioassay(176).Thisresult is consistentwith very early reportsof a substance,termedpollenhor-mon, that waspresentin orchid pollen that causedwilti ng of the flower andwaslater shown tobe auxin (34,35, 99). Even beforeauxin wasidentified asacomponentof orchidpollen,it wasdemonstratedthatexogenousapplicationofauxincouldmimic pollination andinitiatemostpollination-regulateddevelop-mentalevents(25, 64). Sincethen,the capacityof auxinsto initiate pollina-tion-regulateddevelopmentaleventsin orchidshasbeenrepeatedlydemon-strated(4, 7–9,20, 21, 25, 142).Auxin wasproposedto serveastheprimarypollination signal by the direct transferof pollen-borneauxin to the stigma,from where itdiffusedto distalfloral organs andpromotedautocatalytic ethyl-ene productionthroughoutthe flower, leading to perianthsenescence(20).Auxin hasbeenidentified asa componentof Nicotiana, Antirrhinum,Cycla-men,Petunia,and Datura pollen, as well as of germinatedpollen of Pinusradiata, suggestingthat this putative primarypollination signalis presentin awide rangeof higherplantpollen(11,89,98,145).While therole of auxinastheprimarypollensignalhasbeenconsistently supported,otherreportsargueagainstthe ideathatauxindiffusesto theperianthwhereit directly stimulatesethyleneproduction,suggesting that a distinct signal transmitsthe primarypollination eventto distalorgans (141).

Although auxin is presentin orchid pollen and may act as the primarypollensignal,thelevelsof auxinin orchidpollenmaybeinsufficientto bethesole primary pollen signal. It is possible that pollen containsother forms ofauxin, such as auxin conjugates,or other pollen-bornefactors,which mayparticipatesynergistically with auxin to elicit pollination-regulatedresponsesin orchid.Arditti (4) suggestedthat the “pollenhormon” describedby Fittingmay be a mixture of biologically active molecules.A numberof candidatesignalmoleculesshouldbe examinedmoreintensivelyin this regard,includ-ing pecticcell wall fragmentsthathavebeenshownto elicit ethyleneproduc-tion (150) andthat arepotentially producedby pollen-derived polygalacturo-nase and pectatelyase (17,164).

SecondaryPollinationSignals

Developmentalchangessuchasovule initiation andfloral color changesareinitiatedin floral organsdistal to thestigmashortlyafterpollination,implicat-ing the role of secondarysignals that transduce and amplifythe primarypollination signal. The interorganregulationof the pollination-regulatedre-sponsesuggeststhatthesecondarysignalis transmissible andmovesfrom thestigma, through the style, to other floral organs.Early evidencefor suchasecondarypollination signal camefrom surgicalexperimentsdemonstrating


that a mobile wilting factor is transmittedthroughthe style to the corolla ofPetuniaflowerswithin 6 h afterpollination(42).Stylarexudatesalsopromoteperianthsenescencein Petuniaandcarnation,implicating therole of a chemi-cal messengereitherproducedin thestyleor translocatedthroughit (42,132).Becauseauxin, ethylene,and ACC havebeenimplicated in primary pollensignaling,thesesamemoleculeshavebeenextensivelyevaluatedaspotentialtransmissible signalsin pollinated flowers.

The modelof Burg & Dijkman (20) proposedthat the primary pollinationsignal,auxin, diffusedto thelabellum whereit triggeredethylenebiosynthesis.Althoughearlyexperimentsdemonstratedthat14C-IAA appliedto thestigmawasmobilizedto thecolumnandlabellum, subsequentresearchindicatedthat14C-IAA applied toAngraecumandCattleyastigmas was largelyimmobilizedat thepoint of applicationwith sometranslocationto theovary(141).Becausethe pollination signalspreadsto distal floral organs(petalsandsepals)muchfasterthanexogenously applied14C-IAA, it wasconcludedthat auxin is un-likely to bethesecondarypollinationsignal thatregulatesperianthsenescence.However,thedatathatauxinis translocatedprimarily to theovaryis consistentwith otherevidencethat auxin translocatedfrom the stigmamay specificallycontributeto the regulationof the initiation of ovule differentiation in thatorgan (176).

Ethyleneitself is a potentialtransmissible signalto floral partsdistal fromthestigma,andit hasrecently been suggestedthat diffusionof ethylenewithinthe intercellularspaces(interstitialethylene)may function in interorgancom-munication(75, 166,168). Internalethylenein theCymbidium flower centralcolumn was measuredat levels up to 15 ppm, and treatmentof the columnwith exogenous ethyleneincreasedethyleneconcentration inthe perianth,consistent with the proposal that interstitial ethylenefrom the column istranslocateddirectly to theperianth(75). In contrast,Reidet al (127)demon-stratedthat aspirationof ethyleneproducedin the gynoeciumdid not delaypetal senescencein carnation,indicating that volatile ethyleneproducedbe-causeof theprimarypollinationsignalwasnot thetransmissible signalrespon-sible for regulatingperianthsenescence.Although theseresultssuggestthepossibility that interstitial ethyleneactsasthe secondarytransmissible signalbetween floralorgans, thisdoesnotappear to be thecase in allflowers.

In spiteof the suggestionsthat ethylene,ratherthanACC, is translocatedbetweenfloral organs,thereis a largebody of researchimplicating theethyl-eneprecursor,ACC, asanimportantsecondarypollinationsignalthatcoordi-natesinterorganpollination-regulatedresponses.Translocationof ACC wasfirst demonstrated in waterlogged tomato plants(15).This result illustrated thepotential for transportof this water-solublehormoneprecursorto effect in-

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terorganregulationof growth responses ratherthantransportof ethyleneitself,which is lessamenableto targetedtranslocationprocessesbecauseof its gase-ousstate.Similarly, ACC translocation in pollinated flowersprovidesa poten-tial mechanismfor thetargetedtranslocation of a secondary pollinationsignal.Following pollination of carnationflowers,ACC levelsincreasedin all flowerparts,which was proposedto result from ACC translocation(111). It wassubsequentlyshownthat 14C-ACC appliedto thestigma of carnationflowersresultedin theproductionof 14C-labeledethylenein thegynoeciumandperi-anth,whichprovidedcompellingevidencethatACC wastranslocatedfrom thestigma to the gynoecium andperianth,where it servedas a substrateforethylenebiosynthesis(127).Emasculation-inducedsenescenceof Cymbidiumflowers demonstratedthat changesin lip coloration,an early morphologicalmarkerof ethylene-regulatedsenescence,weretriggeredby ACC translocatedfrom thecentralcolumn(166). In Phalaenopsis orchid flowers,ethylenepro-ductionby the intact flower significantly exceededthe sumof ethylenepro-ductionby excisedfloral organs,which wasinterpretedto indicatethatethyl-eneproductionby somefloral organsis dependenton ACC import from otherfloral parts (117). Collectively, thereis strongexperimental supportfromseveralflower systemsthatACC is translocatedbetweenfloral organs,whereit servesasa substratefor ethylenebiosynthesis. This translocation of ACCalsoimplicatesit asa secondarypollinationsignalin the interorgancoordina-tion of pollination-regulateddevelopmentalresponses.

A very earlyresponseof floral tissuesto pollinationis increasedsensitivityto ethylene(125). Substantialresearchhas focusedon the identification oftransmissible“sensitivity factors”that renderthefloral tissuemoresensitive tosenescence-inducingeffectsof ethylene.Following pollination of Phalaenop-sis flowers, there was a significant increasein the endogenouscontentofshort-chainsaturatedfreefatty acidsin thecolumnandperianth.Furthermore,exogenousapplication ofthesefreefatty acidsto thestigmaincreasedsensitiv-ity of the flower to ethylene,leadingto the suggestion that theseshort-chainfatty acidsmaybeethylenesensitivity factors(52). It is likely thatelucidationof themolecularcomponentsinvolvedin ethyleneperceptionandsignaltrans-ductionwill contribute to betterunderstandingthis phenomenon.

REGULATION OF ETHYLENE BIOSYNTHESISINPOLLINATED FLOWERS

Ethyleneis centralto thecontrolof pollination-regulatedflower development,and the regulationof its endogenoussynthesis appearsto be an importantcomponent oftheinterorgancoordinationof discretedevelopmentalprocesses.


Examination of the regulationof expressionof genesencodingthe majorbiosynthetic stepsin ethylenebiosynthesishasprovidedthe basisfor analyz-ing thetemporalandspatialregulationof ethylenebiosynthesisin flowersandin responseto bothprimaryandsecondarypollination signals.In addition, thecloning of ethylenebiosynthetic geneshasprovidedthe meansto geneticallyengineer flowers for enhancedlongevity(91).

The penultimateenzymein the ethylenebiosynthetic pathway,ACC syn-thase,is widely regarded as therate-controllingstep. This step is highlyregulatedat the level of enzymeactivity andat the level of geneexpression(69, 70). In addition,while consideredto be constitutive in manytissues,thefinal enzymein ethylenebiosynthesis,ACC oxidase,is alsoregulatedat thelevel of enzymeactivity and at the level of geneexpression(69, 70). Thespatialand temporalexpressionof both ACC synthaseand ACC oxidaseinresponseto pollination haveprovidedsignificant insight into the interorgancoordinationof pollination-regulated flowerdevelopment.

PollinationRegulationof ACC Synthase

In all speciesexaminedto date,ACC synthaseis encodedby multiple genesthat exhibit differential tissuespecificity and/or differentialregulation byenvi-ronmentalor hormonalstimuli (70). Many cDNA clonesencodingACC syn-thasehavebeenisolatedfrom a numberof flowers including tomato,carna-tion, Petunia,geranium,andorchid(24,57,91,117,119,129).Becauseof itspotentialrole in the regulationof ethyleneproductionin responseto pollina-tion, ACC synthasehasbeenthesubjectof intenseinterestregardingpollina-tion-regulatedflower development. ACC synthasecDNA cloneshavebeenisolatedfrom senescingcarnationflowers andfrom pollinatedorchid flowersandtheir expression at thelevel of mRNA abundancecharacterizedin detail inrelationto pollination andperianthsenescence(57, 117,119,171). In carna-tion flowers, ACC synthasemRNA was undetectablein all floral organsimmediately after harvestbut increaseddramaticallyafter 5–6 daysin petalsandstylescoincidentwith the increasein ethyleneproduction.ACC synthaseactivity was approximately sixfold higher in senescingstylesthan in petals,whereasACC synthasemRNA accumulatedto similar levels in both tissues(171).Subsequently,a seconddivergentACC synthasemRNA wasidentifiedthat waspredominantly expressedin stylesandmay accountfor theapparentdiscrepancybetweenstylar ACC synthasemRNA and activity levels (57).Expressionof both carnationACC synthasecDNAs (termedCARACC3 andCARAS1)werethemselvesethylene regulated, suggesting that they contributeto autocatalytic ethyleneproduction. Relatively low levelsof both ACC syn-

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thasemRNAs were detectedin ovaries,in spite of high levels of ethyleneproductionin this organ,suggesting the existenceof a third ACC synthasegenepredominantly expressedin theovary.Thediscrepanciesnotedin attrib-uting ACC synthaseenzymelevels to the expressionof particularACC syn-thase illustrate thecomplexity in understanding the detailed regulationofethyleneproductionby multiple ethylenebiosynthetic genesin floral tissues(57).

Expressionof ACC synthasegeneshasalso beencharacterizedin polli-natedorchidflowers(117).In this flower system,threeACC synthasecDNAshavebeencharacterizedthat collectively accountfor the observedACC syn-thaseenzymeactivity thathasbeencharacterizedin thevariousorgansof theflower. mRNAs corresponding to two highly homologous ACC synthasecDNAs (OAS1 and OAS2)accumulated to highlevels in the gynoeciumapproximately18 h afterpollination,accumulatedalsoin labellumtissueoverthesameperiod,butwereundetectablein theperianth(excludingthelabellum)evenat 72 h after pollination (117). Theseresultswere consistentwith theabsenceof ACC synthaseenzymeactivity in theperianthtissues,eventhoughthe perianthis the siteof substantial ethyleneevolution (19, 117).

Becauseauxinhasbeenimplicatedasa primarysignalin pollination-regu-lated responsesin orchid flowers and becauseauxin has beenreportedtoinduceexpressionof certainACC synthasegenefamily membersin severalplantspecies (105,122,153), the regulationof the orchidACC synthase genesby auxin was carefully evaluated(117). Although exogenousapplication ofNAA to thestigma stronglypromotedaccumulationof ACC synthasemRNA,this inductionwascompletelyreversedby pretreatmentwith AVG, an inhibi-tor of ethylene biosynthesis. This result indicated that OAS1 and OAS2mRNAs were regulatedby ethyleneand,as with carnationACC synthases,participatedin autocatalytic ethyleneproduction. A third ACC synthasecDNAwasclonedfrom pollinatedorchidflowersthatwasdivergentfrom OAS1andOAS2 andshownto be pollinationregulatedin the stigmaandto be directlyregulatedby auxin (19). Taken together,in pollinatedorchid flowers thereappearto be at least two distinct types of ACC synthasegenesthat differmarkedlyin their spatialandhormonalregulation.Thefirst typeis responsiveto a primary pollination signal,auxin; the secondtype is ethyleneregulatedandmayserveto amplify or sustaintheprimarypollination signalby regulat-ing autocatalyticethyleneproduction.None of the ACC synthasegenesinpollinatedorchid flowers areexpressedin the perianthdespitehigh levelsofethylenebiosynthesis in thosetissues(117). This implies that a sourceofACC, otherthanendogenousproduction, existsfor conversionto ethyleneinperianthtissue.


PollinationRegulationof ACC Oxidase

ACC oxidaseis the final enzymein ethylenebiosynthesisthat convertsACCto ethyleneandin most instancesis consideredto be constitutive (70). How-ever, increasesin ACC oxidasehave beenreportedin senescingcarnationflower petals(87), andACC oxidasemRNA levelsarepollination inducedinPhalaenopsis and carnationflowers (101, 155). In carnation,ACC oxidasemRNA wasundetectablein presenescentpetals,ovaries,andreceptaclesbutwaspresentat significantlevelsin presenescentstylesandincreaseddramati-cally in abundancefollowing pollination (171). TheseresultssuggestthatACC oxidasemay be presentin carnationstigmas beforepollination.Simi-larly, it wasreportedthat ACC oxidaselevelsin Petuniaflowers weremaxi-mal shortly after flower openingandthat ACC oxidaseenzymeactivity wasmostabundantin thePetuniaflower stigmabeforepollination (121).Recently,a family of PetuniaACC oxidasegeneshavebeencloned andtheir expressionin Petuniaflowers studiedin detail (147,148). In agreementwith Pechet al(121), eachof the threeexpressedACC oxidasemRNAs accumulatedin thegynoeciumduringearly flower development,reachingtheir maximallevelsatthetime of flower opening(147).In addition,ethylenetreatmentenhancedtheaccumulationof all three ACCoxidase mRNAsin thepistil, and ACCoxidasemRNA accumulation was also inducedin the floral transmitting tissuebypollination(149).Collectively, theseresultssuggestthatACC oxidaseis likelyto be presentin the stigmaof both carnationandPetunia,andthesestigmascan likely convert pollen-borneACC to ethyleneas a part of the primaryperceptionof pollen by the stigma.In addition, it appearsthat ACC oxidasegenesexpressedin flowers are ethyleneregulatedand so are likely to alsoparticipate,with ACC synthase,in autocatalyticethyleneproduction in polli-nated flowers.

ACC oxidaseactivity and ACC oxidasemRNA accumulationhavealsobeencharacterized inorchidflowers(101,117).Unlike Petunia,ACC oxidaseactivity wasnot detectedin matureflowersbefore pollinationbutwasinducedrapidly following pollination (101). Following pollination,orchid ACC oxi-dase(OAO1) mRNA accumulatedto high levels within 48 h in all floralorgans,including the perianth(101). This resultdemonstrateda striking dis-parity betweenthe accumulation of ACC synthasemRNA, which failed toaccumulatein theperianth,andsuggestedthatthesepalsandpetalsdevelopedthecapacityto convertACC to ethylenebut couldnot synthesizeACC endo-genously(101, 117). In light of the high level of ethyleneevolution fromperianthtissuesandtheabsenceof ACC synthaseenzymeactivity or a corre-spondingmRNA, it hasbeensuggestedthat ACC mustbe translocatedfrom

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other floral organsto the perianthwhere it is convertedto ethyleneby theactivity of residentACC oxidase(117).

MODEL FOR INTERORGANCOORDINATION OFPOLLINATION-REGULATED FLOWERDEVELOPMENT

Ethylenewith auxin plays important roles in pollination-regulateddevelop-mentalresponsesand,in conjunctionwith ACC, participatesin theinterorgancoordinationof diversecomponentsof pollination-regulatedflower develop-ment.Themodeloutlinedin Figure2 attemptsto summarizedatathataddressthe initiationof ethylenebiosynthesis bypollination and the interorgan regula-tion of ethylenebiosynthesisin pollinated flowersbecausethesetwo processesappearto becentralto thecoordinationof pollination-regulatedflower devel-opment.Much of themodelrelieson the recentelucidationof thepatternsofexpressionof genesencodingethylenebiosynthetic enzymesin pollinatedflowers. In this model,a pollen-associatedfactor is prominentastheprimarystimulus in initiating ethylenebiosynthesis as well as the overall processofpollination-regulatedflower development. In orchid flowers, an importantcomponentof the primary pollen signal is auxin, whereasin other flowers,ACC or otheras-yet-unidentifiedpollen-borne substancesmayalso participatein primary pollen signaling. The earliestresponseto pollination is the induc-tion of ethyleneproductionin the stigmaand style, which may usepollen-borneACC directlyassubstrateor,morelikely, reliesontherapidinductionofACC synthasein the stigma.In orchid flowers,expressionof an auxin-regu-latedACC synthaseis rapidly inducedin thestigmaby pollination, andthis islikely to accountfor the rapid transductionof the putative primary pollensignal,auxin,to the initial burstof ethyleneproduction.In otherflowerssuchasPetunia,a traceamountof pollen-borneACC maybeconverteddirectly toethylene,which leadsto localized autocatalyticethyleneproduction in thestigma.Thepresenceof ACC oxidasemRNA in presenescentPetuniastigmasandits rapidethylene-dependentinduction following pollinationis consistentwith this mechanismof initial pollination-inducedethyleneproduction.

The interorgantransmissionandamplificationof theprimarypollensignalrequiressecondarysignalsthat emanatefrom the stigma, and an importantcomponentof this signalappearsto beACC andits subsequentconversiontoethylene in distal floral organs. Inorchidflowers,theroleof translocatedACCwas implicated by the failureof petals andsepals to accumulate ACC synthasemRNA or enzymeactivity, in spiteof high levelsof ethyleneproductionbythesefloral organs,suggestingthat ethyleneproduction in theseorgansisentirely dependenton translocatedACC. This situation is lesspronouncedin


ACC

AdoMet

AUX-ACS

ETHYLENESTIGMA

ACC

TTRR

AANN

SSLLOO

CCAA

TTIIOO

NN ??

AdoMet

AUX-ACS (ACS3)

ETH-ACS (ACS1)

ETHYLENEOVARY

ETH-ACO(ACO1)

PERIANTHLABELLUM

ACC ETHYLENEAdoMet

(+)

ETH-ACO(ACO1, ACO2)

EMASCULATIONAUXIN

&

(ACS2)

ETH-ACS (ACS1)

ETH-ACS(ACS1)

?

(+)

(+) (+)

(+)(+)

(+) (+) (+) (–)

ETH-ACO(ACO1)

POLLINATION

POLLEN FACTOR(S)

Figure 2 Modelfor the interorganregulation of ethylenebiosynthetic genesin poll inatedflowers,basedprimarily ondata from thePhalaenopsisorchid flower,with otherflowersystemsviewedasvariationsonthis basic theme(19, 101,117). Theprimarysignaling event for poll ination-regulateddevelopment occurswith thetransferof pollen-bornefactors,includingauxin, to thestigmasurface,thesiteof initial perception. An auxin-regulatedACC synthasegene(AUX-ACS)is inducedby theprimary poll ination signal(s). ACC synthesizedin the stigma is converted to ethyleneby ACCoxidase,initially presentat a low level but inducedto high levelssoon afterpoll ination to initiateautocatalytic ethylene production in the stigma. Expression of other ethylene-regulated ACCsynthasegene(s)(ETH-ACS)arealsoinducedby ethyleneto furtheramplify autocatalytic ethyleneproduction. ACC translocatedfrom the stigmato the perianth supports the production of ethylenein thatorgan,initiating itssenescence.This mechanismof interorganregulation reliesontransloca-tionof ACCtodistalorganstosupport ethyleneproduction. In additionto itsroleasagaseoussignalcoordinating ethylene production at the molecular level, ethyleneitself may alsobe translocatedwithin theflowerasatranslocatedsignal.Abbreviations:ACC, 1-aminocyclopropane-1-carboxylicacid; ACO,ACCoxidase;ACS,ACCsynthase;AdoMet,S-adenosylmethionine;AUX, auxin-regu-lated;ETH, ethylene-regulated.

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flowers such as Petunia where ACC synthaseis induced in petal tissues.However,thePetuniapetalACC synthaseis ethyleneinduced,andthe initialproductionof ethylenein petalsrequiredto stimulate autocatalyticethyleneproduction may bederived from translocated ACC.The model shown inFigure 2 is idealizedin that it reflects the situation in Phalaenopsis orchidflowers, one of the most extremeexamplesof pollination-regulatedflowerdevelopment.Datafrom otherspeciessuggestthat therearevariationson thethemespresented inFigure 2.

CONCLUSIONSAND FUTUREDIRECTIONS

Pollination regulatesa suite of developmentalresponsesthat transformtheflower from a structurededicatedto pollendispersalandreceptionto onethatis dedicatedto fertilization, embryogenesis,seeddevelopment,andultimatelyseeddispersal.Oneimportant aspectof this processis the sheddingof floralorgans,such as the petalsand sepalsthat have completedtheir service inpollinator attraction.In addition,pollination demandsthatcertain reproductivestructuresrapidly maturein anticipationof fertilization. Thus,thesignalsthatregulatepollination responsesare involved in simultaneouslycoordinatingprocessesof programmedcell deathwhile initiating thedifferentiation and/ormaturationof importantreproductivestructures.

Researchdirectedat understanding thenatureof thepollinationsignalshasa rich history dating to the beginningsof this century,and it has revealedimportantelementsof the interorgansignaling neededto coordinatethe fullsyndromeof pollination-regulateddevelopmentalprocesses.Although it isclear that auxin, ethylene,and ACC are important actorsin this regulatoryprocess,it is likely that this is not thecompletecast.More researchis neededto morefully elucidateprimarypollinationsignalsandhow they interactwitheachotherandwith thestigma andstyleto propagatethesignalto distal floralorgans.

This review focuseson the early eventsin pollen signaling. However,thegrowing pollen tube continuesto exchangeinformation with the style andovary, and the natureof thesesignalsalso representsa rich areaof furtherresearch.Much researchhascharacterizeda numberof modelflower systemsthatarephysiologically suitedto studying pollination-regulatedflower devel-opment,but thesemodelsystemsdo not generallyoverlapwith modelgeneticsystems,such as Arabidopsis thaliana. Despite the recognizeddifferencesbetweenplantsin termsof theirpollinationresponses,futureprogressrequiresthat information frompowerfulphysiologicalsystems betransferredto species


that are well suited to geneticdissection and transgenicmanipulation andanalysis.

ACKNOWLEDGMENTS

I thankDrs. Anhthu Bui, JeanetteNadeau,Ron Porat,andXianshengZhangfor discussionsandresearch contributionsdescribedin this review andProfes-sor AbrahamH Halevy (TheHebrewUniversity of Jerusalem)for his friend-ship and inspiration. I also thank the USDA-NRICGP (Plant Growth andDevelopmentProgram), the National ScienceFoundation(DevelopmentalMechanismsProgram),andthe Binational Agricultural ResearchandDevel-opmentFund for providing supportfor my laboratoryto study many of theissuesdiscussedhere.

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LiteratureCited

1. AdamsDO, YangSF. 1979. Ethylenebio-synthesis:Identifi cation of 1-aminocyclo-propane-1-carboxylic acidasanintermedi-atein the conversion of methionineto eth-ylene. Proc. Natl. Acad. Sci. USA 83:7755–59

2. AkamineEK. 1963.Ethyleneproductioninfading Vanda orchid blossoms.Science140:1217–18

3. AndersonJD, Mattoo AK, LiebermanM.1982. Inductionof ethylenebiosynthesisintomatoleafdisksby cell wall-digesting en-zymes. Biochem. Res.Commun. 107:588–96

4. Arditti J. 1971. Orchids andthe discoveryof auxin. Am.Orchid Soc. Bull. 40:211–14

5. Arditti J. 1979. Aspectsof the physiologyof orchids.Adv. Bot. Res.7:421–655

6. Arditti J, Flick BH. 1976. Post-pollinationphenomenain orchid flowers.VI. Excisedfloral segments ofCymbidium. Am.J. Bot.63:201–11

7. Arditti J,HoganNM, ChadwickAV. 1973.Post-poll ination phenomena in orchidflowers.IV. Effectsof ethylene.Am.J.Bot.60:883–88

8. Arditti J,JeffreyDC,Flick BH. 1971. Post-poll ination phenomenain orchid flowers.III. Effects and interactions of auxin, ki-netin or gibberellin. New Phytol. 70:1125–41

9. Arditti J, Knauft RL. 1969. The effectsofauxin, actinomycin D, ethionine and

puromycin on post-pollination behavior inCymbidium (Orchidaceae)flowers.Am.J.Bot. 56:620–28

10. Asen S, StewartRN, Norris KH. 1977.Anthocyanin andpH involvedin the colorof ‘Heavenly Blue’ morning glory. Phyto-chemistry 16:1118–19

11. Barendse GWM, Rodrigues-Pereira AS,Berkers PA, DriessenFM, Eyden-Emonsvan A, Linskens HF. 1970. Growth hor-monesin pollen,stylesandovariesof Pe-tunia hybrida andof Lil ium species.ActaBot. Neerl.19:175–86

12. BashawEC,HannaWW. 1990. Apomicticreproduction. In ReproductiveVersatili ty intheGrasses,ed.GPChapman,pp. 100–30.Cambridge:CambridgeUniv. Press

13. Borochov A, WoodsonWR. 1989. Physiol-ogy andbiochemistryof flowerpetalsenes-cence.Hortic. Rev. 11:15–43

14. BoumanF. 1984. Theovule. See Ref.66a,pp. 123–57

15. BradfordKJ, YangSF. 1980. Xylemtrans-port of 1-aminocyclopropane-1-carboxylicacid,anethyleneprecursor, in waterloggedtomatoplants.Plant Physiol. 65:322–26

16. BradyCJ.1987. Fruit ripening. Annu. Rev.Plant Physiol. 38:155–78

17. Brown SM, Crouch ML 1990. Charac-terization of a gene family abundantly ex-pressedin Oenothera organensis pollenthat shows sequence similarity to poly-galacturonase.Plant Cell 2:263–74

568 O'NEILL

18. Bufler G,Mor Y, Reid MS,YangSF. 1980.Changes in 1-aminocyclopropane-1-car-boxylic acidcontent of cutcarnation flow-ers in relation to their senescence.Planta150:439–42

19. Bui A. 1996. Temporal and spatial regula-tion of ACC synthase genes in poll inatedorchid flowers.PhD thesis.Univ. Calif.,Davis

20. Burg SP, DijkmanMJ. 1967. Ethyleneandauxin participationin polleninducedfadingof Vanda orchid blossoms.Plant Physiol.42:1648–50

21. ChadwickAV, HoganNM, Arditti J.1980.Postpoll inationphenomenain orchid flow-ers.IX. Inductionandinhibitionof ethyleneevolution, anthocyanin synthesis,andperi-anth senescence.Bot. Gaz.141:422–27

22. ChaubalR,RegerBJ.1990.Relativelyhighcalcium is localized in synergid cells ofwheat ovaries. Sex. Plant Reprod. 3:98–102

23. ChaubalR, RegerBJ.1992. Thedynamicsof calciumdistributionin thesynergidcellsof wheatafter poll ination. Sex.Plant Re-prod. 206–13

24. ClarkD,Lind-IversenS,RichardsC,Even-senK. 1994. Ethylene-regulatedgene ex-pression in geranium flowers. See Ref.140a,pp. 291–95

25. CurtisJT. 1943. An unusualpollenreactionin Phalaenopsis.Am.OrchidSoc.Bull. 21:98–100

26. DavidsonOW. 1949. Effectsof ethyleneonorchid flowers.Am. Soc. Hortic. Sci. 53:440–46

27. Dijkman MJ, Burg SP. 1970. Auxin-in-duced spoiling of Vanda blossoms.Am.Orchid Soc. Bull. 39:799–804

28. DobsonHEM. 1989. Pollenkitt in plantre-production. In TheEvolutionaryEcologyofPlants, ed.JH Bock, YB Linhart, pp.227–46. Boulder, CO:Westview

29. DuncanRE, Curtis JT. 1942. Intermittentgrowth of fruits of Cypripedium andPaphiopedilum.A correlationof thegrowthof orchid fruitswith their internal develop-ment. Bull. Torrey Club69:353–59

30. Duncan RE, Curtis JT. 1943. Growth offruits in Cattleyaandallied genera in theOrchidaceae.Bull . Torrey Club70:104–19

31. EatonGW.1959.A studyof themegagame-tophyte in Prunusaviumandits relation tofruit setting. Can. J. Plant Sci. 39:466–76

32. Eaton GW, JamontAM . 1964. Embryo sacdevelopment in the Apricot, Prunus ar-meniacaL. CV constant. Am.Soc. Hortic.Sci. 86:95–101

33. Felix G, Grosskopf DG, RegenassM,BasseCW, BollerT. 1991. Elicitor-induced

ethylenebiosynthesisin tomatocells.PlantPhysiol. 97:19–25

34. FittingH. 1909. Die Beeinflussung derOr-chideenblüten durch die Bestäubung unddurchandereUmstände.Z. Bot. 1:1–86

35. Fitting H. 1910. Weitere entwicklung-sphysiologishe Untersuchungen an Or-chideenblüten. Z. Bot. 2:225–67

36. Fredrikson M. 1991. An embryologicalstudy of Platantherabifolia (Orchidaceae).Plant Syst.Evol. 714:213–20

37. Fredrikson M. 1992. The developmentofthe female gametophyte of Epipactis (Or-chidaceae)andits inference for reproduc-tiveecology. Am.J. Bot. 79:61–8

38. Fredrikson M, Carlsson K, FrankssonO.1988. Confocalscanninglasermicroscopy,a newtechniqueusedin anembryologicalstudy of Dactylorhiza maculata (Orchi-daceae).Nord. J. Bot. 8:369–74

39. GardDL. 1994.γ-tubulin isasymmetricallydistributed in the cortex of Xenopus oo-cytes.Dev. Biol. 161:131–40

40. GilissenLJW. 1976. Theroleof thestyleasa sense-organin relation to wil ting of theflower. Planta 131:201–2

41. GilissenLJW. 1977. Style-controlledwil t-ing of the flower. Planta 133:275–80

42. GilissenLJW, HoekstraFA. 1984. Pollina-tion-inducedcorollawil ting in Petunia hy-brida. Rapid transferthroughthestyle of awil ting-inducing substance.Plant Physiol.5:496–98

43. Goh CJ, Halevy AH, Engel R, KofranekAM. 1985. Ethylene evolution andsensi-tivity in cutorchid flowers.Sci. Hortic. 26:57–67

44. Gori DF. 1983. Post-pollination phenom-ena and adaptive floral color change. InHandbook ofExperimental PollinationBi-ology, ed.CE Jones,RJLit tle, pp. 31–49.NewYork: VanNostrandReinhold

45. Gustafson FG. 1936. Inducement of fruitdevelopmentby growth-promoting chemi-cals.Proc.Natl. Acad.Sci.USA22:628–36

46. Gustafson FG. 1937. Parthenocarpy in-duced by pollen extracts.Am. J. Bot. 24:102–7

47. Gustafson FG. 1939. Auxin distribution infruits andits significance in fruit develop-ment. Am.J. Bot. 26:189–94

48. Gustafsson A. 1946. Apomixis in higherplants.Part1.Themechanismof apomixis.LundsUniv. Årsskrift, 2:1–66.

49. Hagerup O. 1944. On fertilisation, polyploidyandhaploidy in OrchismaculatusL.sens.lat. Dansk Bot. Arkiv. 11:1–25

50. Halevy AH, Mayak S. 1979. Senescenceandpostharvestphysiology of cut flowers.Hortic. Rev. 1:204–36


51. Halevy AH, Mayak S. 1981. Senescenceandpostharvestphysiology of cut flowers.Hortic. Rev. 3:59–143

52. Halevy AH, PoratR,SpiegelsteinH, Boro-chov A, Botha L, WhiteheadCS. 1996.Short-chain saturated fatty acids in theregulation of poll ination-inducedethylenesensitivity of Phalaenopsis flowers.Physiol. Plant. 97:469–74

53. Halevy AH, WhiteheadCS,KofranekAM.1984. Doespoll ination induce corolla ab-scission of cyclamenflowersbypromotingethylene production? Plant Physiol. 75:1090–93

54. Hall IV, Forsyth FR. 1967. Production ofethyleneby flowersfollowing poll inationandtreatments with water and auxin. Can.J. Bot. 45:1163–66

55. HanSS,HalevyAH, Reid MS. 1991. Therole of ethylene and poll ination in petalsenescenceandovarygrowth of Brodiaea.J. Am.Soc. Hortic. Sci. 116:68–72

56. He C-P, Yang H-Y. 1992. Ultrastructurallocalization of calcium in the embryo sacof sunflower. Chin. J. Bot. 4:99–106

57. Henskens JAM, Rouwendal GJA, HaveAT, WolteringEJ.1994. Molecularcloningof two different ACC synthasePCRfrag-ments in carnation flowersandorgan-spe-cific expression of the correspondinggenes.Plant Mol. Biol. 26:453–58

58. HewCS,TanSC,Chin TY, OngTK. 1989.Influenceof ethyleneonenzymeactivitiesandmobilization of materials inpoll inatedArachnis orchid flowers.J. Plant GrowthRegul. 8:121–30

59. Hil l SE,SteadAD, NicholsR. 1987. Polli -nation-inducedethylene andproduction of1-aminocyclopropane-1-carboxylic acidby pollen of Nicotiana tabacumcv WhiteBurley. J. Plant Growth Regul. 6:1–13

60. HoekstraFA, vanRoekelT. 1988. Effectsof previous poll ination and stylar ethyleneon pollen tube growth in Petunia hybridastyles.Plant Physiol. 86:4–6

61. HoekstraFA, WegesR.1986. Lackof con-trol by earlypistillateethyleneof theaccel-eratedwil ting of Petunia hybrida flowers.Plant Physiol. 80:403–8

62. Huang B-Q, Russell SD. 1992. Femalegerm unit: organization, isolation, andfunction. Int. Rev. Cytol. 140:233–93

63. Huang BQ, Russell SD. 1992. Synergiddegeneration in Nicotiana: a quantitative,fluorochromatic and chlorotetracyclinestudy. Sex.Plant Reprod. 5:151–55

64. HubertB, MatonJ.1939. The influenceofsynthetic growth-controlling substancesandotherchemicalsonpost-floral in tropi-calorchids.Biol. Jarrb. 6:244–85

65. IsraelHW, SagawaY. 1965. Post-poll ina-tionovuledevelopment in Dendrobiumor-chidsIII. Finestructureof meioticprophaseI. Caryologia 18:15–33

66. JensenWA, Ashton ME, Beasley CA.1983.Pollentube-embryosacinteractionincotton. In Pollen:BiologyAndImplicationsfor Plant Breeding, ed. DL Mulcahy, EOttaviano, pp. 67–72. NewYork: Elsevier

66a.Johri BM, ed.1984. Embryologyof Angio-sperms.Berlin: Springer-Verlag

67. KandasamyMK, Dwyer KG, Paoli llo DJ.1990.Brassicas-proteinsaccumulatein theintercellularmatrix alongthepathof pollentubes in transgenic tobaccopistils. PlantCell 2:39–49

68. KapilRN,BhatnagarAK. 1981.Ultrastruc-ture andbiology of femalegametophyte inflowering plants. Int. Rev. Cytol. 70:291–341

69. KendeH. 1989. Enzymesof ethylenebio-synthesis.Plant Physiol. 91:1–4

70. Kende H. 1993. Ethylene biosynthesis.Annu. Rev. Plant Physiol. Plant Mol. Biol.44:283–307

71. Knox RB, Heslop-HarrisonJ.1970. Pollenwall proteins: localization and enzymaticactivity. J. Cell Sci.6:1–27

72. Laibach F. 1932. Pollenhormon undwuchsstoff. Ber. Deutsch. Bot. Ges. 50:383–92

73. LaibachF. 1933. Versuche mit wuchsstof-fpaste.Ber. Deutsch.Bot. Ges.51:386–92

74. LaibachF. 1933. Wuchsstoffversuchemitlebendenorchideenpollinien. Ber. Deutsch.Bot. Ges.51:336–40

75. LarsenPB, Woltering EJ, Woodson WR.1993. Ethyleneandinterorgansignaling inflowersfollowingpoll ination. In Plant Sig-nals in Interactionswith Other Organisms,ed. J Schultz, I Raskin, pp. 171–81.Rockville,MD: Am. Soc.PlantPhysiol.

76. Law SK, YeungEC.1989. Embryology ofCalypso bulbosa. I. Ovule development.Am.J. Bot. 76:1668–74

77. Lawton KA, Huang B, Goldsbough PB,Woodson WR. 1989. Molecular cloningandcharacterization of senescence-relatedgenesfrom carnation flower petals.PlantPhysiol. 90:690–96

78. Lawton KA, Raghothama KG,Goldsbrough PB, Woodson WR. 1990.Regulation of senescence-relatedgene ex-pression in carnation flower petalsby eth-ylene.Plant Physiol. 93:1370–75

79. Lay-Yee M, SteadAD, Reid MS. 1992.Flower senescencein dayli ly (Hemerocal-lis). Physiol. Plant. 86:308–14

80. Lingle SE,Dunlap JR.1991. Sucroseme-tabolism andIAA andethyleneproduction

570 O'NEILL

in muskmelon ovaries. J. Plant GrowthRegul. 10:167–71

81. LinskensHF. 1974. Translocationphenom-enain the petunia flower after cross-andself-pollination. In Fertilization in HigherPlants,ed.HF Linskens, pp. 285–92. Am-sterdam:North-Holland

82. Lipe JA, Morgan PW. 1973. Location ofethyleneproduction in cotton flowersanddehiscing fruits.Planta 115:93–96

83. Lovell PJ,Lovell PH,NicholsR.1987. Thecontrol of flower senescence inpetunia(Petunia hybrida). Ann. Bot. 60:49–59

84. Lovell PJ,Lovell PH,NicholsR.1987. Theimportanceof the stigmain flower senes-cencein petunia (Petunia hybrida). Ann.Bot. 60:41–47

85. LukaszewskiTA, Reid MS. 1989. Bulb-type flowersenescence.ActaHortic. 261:59–62

86. MaheshwariP.1950.An IntroductiontotheEmbryology of Angiosperms.New York:McGraw-Hill

87. Manning K. 1985. The ethyleneformingenzyme systemin carnation flowers. InEthylene and Plant Development, JARoberts, GA Tucker, pp. 83–92. London:Butterworths

88. MascarenhasJP. 1993. Molecular mecha-nismsof pollen tubegrowth anddifferen-tiation. Plant Cell 5:1303–14

89. MascarenhasJP, Canary D. 1985. Pollen.Symbionts and symbiont-induced struc-tures.In EncyclopediaofPlantPhysiology,ed. RP Pharis, DM Reid, 2:579–98. Ber-lin/Heidelberg/NewYork/Tokyo: Springer-Verlag

90. Meyer RC, Goldsbrough PB, WoodsonWR. 1991. An ethylene-responsive flowersenescence-relatedgenefromcarnationen-codesa proteinhomologous toglutathiones-transferases.Plant Mol. Biol. 17:277–81

91. MichaelMZ, Savin KW, Baudinette SC,GrahamMW, Chandler SF, et al. 1993.Cloning of ethylene biosynthetic genesin-volvedin petalsenescenceof carnationandpetunia, and their antisense expression intransgenic plants. InCellular and Molecu-lar Aspectsof thePlant HormoneEthylene,ed. JC Pech,A Latché, C Balogué, pp.298–303. TheNetherlands:Kluwer

92. Mo Y,NagelC,TaylorLP.1992.Biochemi-cal complementation of chalcone synthasemutantsdefinesarolefor flavonolsin func-tional pollen. Proc. Natl. Acad. Sci. USA89:7213–17

93. MogensenHL. 1984.Quantitativeobserva-tions on the patternof synergid degenera-tion in barley. Am.J. Bot. 71:1448–51

94. Mogensen HL.1992. The malegerm unit:

concept, compositionandsignificance.Int.Rev. Cytol. 140:129–47

95. MohanRamHY, Mathur G. 1984. Flowercolour changesin Lantana camara. J.Exp.Bot. 35:1656–62

96. Mòl R, Matthys-Rochon E, Dumas C.1994. The kinetics of cytological eventsduring double fertil ization in ZeamaysL.Plant J. 5:197–206

97. Mor Y, Halevy AH, Spiegelstein H, MayakS.1985. Thesiteof 1-aminocyclopropane-1-carboxylic acid synthesis in senescingcarnation petals. Physiol. Plant. 65:196–202

98. Muir RM. 1947. Therelationshipof growthhormones and fruit development. Proc.Natl. Acad. Sci. USA33:303–12

99. Müller R. 1953. Zur quantitativenbestim-mungvon indolylessigsäuremittelspapier-chromatographie und papierelektropho-rese.Beitr.zur Biol. Pflanz.30:1–32

100.NadeauJA, ZhangXS, Li J, O’Neil l SD.1996. Ovuledevelopment: identifi cationofstage-and tissue-specific cDNAs. PlantCell 8:213–39

101.NadeauJA,ZhangXS,NairH,O’Neil l SD.1993. Temporal and spatial regulation of1-aminocyclopropanecarboxylate oxidasein the poll ination induced senescenceoforchid flowers.Plant Physiol. 103:31–39

102.Nair H. 1990. Postharvestphysiology andhandling of orchids. MalayanOrchid Rev.18:62–68

103.Nair H, Fong TH. 1987. Ethylene produc-tion and 1-aminocyclopropane-1-carbox-ylic acidlevelsin detachedorchid flowersof Dendrobium ‘Pampadour’. Sci.Hortic.32:145–51

104.NairH, IdrisZM, Arditti J.1991. Effectsof1-aminocyclopropane-1-carboxylic acidon ethyleneevolution and senescenceofDendrobium (Orchidaceae)flowers. Lin-dleyana6:49–58

105.NakajimaN, Mori H, YamazakiK, ImasekiH. 1990. Molecular cloning andsequenceof acomplementaryDNA encoding1-ami-nocyclopropane-1-carboxylate synthaseinduced by tissuewounding. Plant CellPhysiol. 31:1021–29

106.Nichols R. 1966. Ethyleneproductiondur-ing senescenceof flowers.J. Hortic. Sci.41:279–90

107.Nichols R. 1968. The responseof carna-tions (Dianthus caryophyllus) to ethylene.J. Hortic. Sci. 43:335–49

108.NicholsR.1971. Inductionof flowersenes-cenceandgynoeciumdevelopment in thecarnation (Dianthus caryophyllus) by eth-yleneand2-chloroethylphosphonic acid. J.Hortic. Sci. 46:323–32


109.Nichols R. 1976. Cell enlargement andsugaraccumulationin thegynoeciumof theglasshousecarnation (Dianthuscaryophyl-lus L.) induced by ethylene.Planta 130:47–52

110.Nichols R.1977. Sitesof ethyleneproduc-tion in the poll inatedandunpoll inatedse-nescing carnation (Dianthus caryophyllus)inflorescence.Planta 135:155–59

111.Nichols R, Bufler G, Mor Y, Fujino DW,ReidMS. 1983. Changesin ethylenepro-duction and 1-aminocyclopropane-1-car-boxylicacidcontent of poll inatedcarnationflowers.J. Plant Growth Regul. 2:1–8

112.Nichols R, Ho LC.1975. An effect of eth-ylene on the distribution of 14C-sucrosefrom the petals to other flower parts in thesenescentcut inflorescenceof Dianthuscaryophyllus.Ann. Bot. 39:433–38

113.Nichols R, Ho LC. 1975. Effectsof ethyl-ene and sucrose on translocation of drymatterand14C-sucrosein thecutflowerofthe glasshousecarnation (Dianthus caryo-phyllus) during senescence.Ann. Bot. 39:287–96

114.Noher deHalacI, HarteC. 1985. Cell dif-ferentiation during megasporogenesisandmegagametogenesis. Phytomorphology 35:189–200

115.O’Neil l SD. 1994. Pollen signaling andinterorganregulation of thepostpollinationsyndrome of flowers. SeeRef. 140a, pp.161–77

116.O’Neil l SD,NadeauJA.1997. Postpoll ina-tion flower development. Hortic. Rev. 19:1–58

117.O’Neil l SD, NadeauJA, Zhang XS, BuiAQ, Halevy AH. 1993. Interorganregula-tionof ethylenebiosynthetic genes bypol-lination. Plant Cell 5:419–32

118.Oertli JJ,Kohl JHC.1960.DerEinflussderBestaubungauf dieStoffbewegungin Cym-bidiumbluten. Munchen/Bonn/Wien: BLV

119.Park KY, Drory A, Woodson WR. 1992.Molecular cloning of an 1-aminocyclo-propane-1-carboxylate synthasefrom se-nescingcarnation flowerpetals.Plant Mol.Biol. 18:377–86

120.PearceG,StrydomD,JohnsonS,RyanCA.1991. A polypeptide from tomato leavesinduces wound-inducible proteinase in-hibitor protein. Science253:895–98

121.PechJ-C,LatchéA, LarrigaudièreC, ReidMS. 1987. Control of early ethylene syn-thesisin poll inatedpetunia flowers.PlantPhysiol. Biochem.25:431–37

122.PeckSC,KendeH.1995.Sequential induc-tion of the ethylenebiosynthetic enzymesby indole-3-acetic acid in etiolatedpeas.Plant Mol. Biol. 28:293–301

123.Pimienta E, Polito VS. 1983. Embryo sacdevelopment in almond [Prunus dulcis(Mi ll .) DA Webb] as affected by cross-,self- and nonpollination. Ann. Bot. 51:469–79

124.PoratR, Borochov A, Halevy AH. 1994.Pollination-induced changes in ethyleneproductionandsensitivity toethylenein cutDendrobium orchid flowers.Sci. Hortic.58: 215–21

125.PoratRA, Halevy AH, SerekM, BorochovA. 1995. An increasein ethylenesensitivityfollowing poll ination is the initial eventtriggering an increasein ethyleneproduc-tion and enhanced senescenceof Pha-laenopsis orchid flowers. Physiol. Plant.93: 778–84

126.Proctor JTA, CreasyLL. 1969. An antho-cyanin-decolorizing system in florets ofCichorium intybus. Phytochemistry 8:1401–3

127.ReidMS,FujinoDW, HoffmanNE,White-head CS. 1984. 1-aminocyclopropane-1-carboxylic acid: thetransmittedstimulusinpoll inatedflowers?J. Plant Growth Regul.3:189–96

128.ReiserL, FischerRL. 1993. Theovuleandembryo sac.Plant Cell 5:1291–301

129.RottmannWH,PeterGF,OellerPW,KellerJA, Shen NF et al. 1991. 1-aminocyclo-propane-1-carboxylatesynthasein tomatois encoded by a multigene family whosetranscription is induced during fruit andfloral senscence. J. Mol. Biol. 222:937–61

130.RussellSD. 1993. The eggcell: develop-mentandrole in fertilizationandearlyem-bryogenesis.Plant Cell 5:1349–59

131.RyanCA, FarmerEE.1991. Oligosaccha-ridesignals in plants:acurrent assessment.Annu. Rev. Plant Physiol. 42:651–74

132.SacalisJ,WulsterG,JanesH. 1983. Senes-cencein isolatedcarnation petals:differen-tial response of various petal portions toACC,andeffectsof uptakeof exudatefromexcisedgynoecia. Z. Pflanzenphysiol. 112:7–14

133.SagawaY, IsraelHW. 1964. Post-poll ina-tionovuledevelopment in Dendrobiumor-chids. I. Introduction. Caryologia 17:53–64

134.Sakurai A, Fujioka S. 1993. The currentstatus of physiology and biochemistry ofbrassinosteroids.Plant Growth Regul. 13:147–59

135.Sanders LC, Lord EM. 1989. Directedmovementof latexparticlesin thegynoeciaof three speciesof flowering plants. Sci-ence243:1606–8

136.SimpsonCE, Bashaw EC. 1969. Cytology

572 O'NEILL

and reproductive characteristics of Pen-nisetumciliare.Am.J. Bot. 56:31–36

137.SinghA, EvensenKB, KaoT. 1992. Ethyl-enesynthesisandfloralsenescencefollow-ing compatible and incompatible poll ina-tions in Petunia inflata. Plant Physiol. 99:38–45

138.SoodSK,MohanaRaoPR.1986.Develop-mentof maleandfemalegametophytesinHerminium angustifolium (Orchidaceae).Phytomorphology 36:11–5

139.Stead AD. 1992. Poll ination-inducedflowersenescence:areview. Plant GrowthRegul. 11:13–20

140.SteadAD, Reid MS. 1990. The effect ofpoll ination and ethylene on the colourchange ofthe banner spot of Lupinus albi-frons (Bentham) flowers. Ann. Bot. 66:655–63

140a.StephensonAG, KaoTH, eds.1994. Pol-len-Pistil Interactions and Pollen TubeGrowth. Rockvil le, MD: Am. Soc. PlantPhysiol.

141.StraussM, Arditti J. 1982. Postpoll inationphenomenain orchid flowers.X. Transportandfateof auxin. Bot. Gaz.143:286–93

142.StraussMS,Arditti J.1984.Postpoll inationphenomenain orchid flowers.XII. Effectsof poll ination, emasculation, and auxintreatment on flowers of Cattleya Porcia‘Cannizaro’ and the rostellum of Pha-laenopsis.Bot. Gaz.145:43–49

143.Suessenguth K. 1923. Über diepseudogamie bei Zygopetalum MackayiHook. Ber. Duetsche.Bot. Ges.41:16–23

144.Swamy BGL. 1943. Embryology of theOrchidaceae.Curr. Sci. 12:13–17

145.SweetGB, Lewis PN. 1969. A diffusibleauxin from Pinus radiata andits possiblerole in stimulating ovule development.Planta 89:380–84

146.Sylvestre I, Droillard M-J, Bureau J-M,Paulin A. 1989. Effectsof theethyleneriseon the peroxidation of membrane lipidsduring the senescenceof cut carnations.Plant Physiol. Biochem.27:407–13

147.TangX, GomesAMTR, Bhatia A, Wood-sonWR. 1994.Pistil -specific andethylene-regulated expression of 1-aminocyclo-propane-1-carboxylate oxidase genes inpetunia flowers.Plant Cell 6:1227–39

148.Tang X, Wang H, Brandt AS, WoodsonWR. 1993. Organization and structure ofthe 1-aminocylopropane-1-carboxylate oxi-dasegenefamily from Petunia hybrida.Plant Mol. Biol. 23:1151–64

149.TangX, WoodsonWR.1996.Temporalandspatial expression of 1-aminocyclo-propane-1-carboxylateoxidasemRNAfol-lowing poll ination of immatureandmature

Petunia hybrida flowers. Plant Physiol.112: 503–11

150.Tong CB, Labavitch JM, Yang SF. 1986.Theinductionof ethyleneproduction frompear cell culture by cell wall fragments.Plant Physiol. 81:929–30

151.UedaJ, Kato J. 1981. Promotive effect ofmethyl jasmonateonoatleafsenescenceinthelight.Z.Pflanz.physiol. Bd. 103:357–59

152.van der Donk JAWM. 1975. Recognitionandgene expressionduring the incompati-bili ty reaction in Petunia hybrida L. Mol.Gen.Genet. 141:305–16

153.Van der Straeten D, Van WiemeerschL,Goodman HM, Van Montagu M. 1990.Cloning and sequencing of two differentcDNAsencoding1-aminocyclopropane-1-carboxylatesynthasein tomato. Proc.Natl.Acad. Sci. USA87:4859–63

154.Vogt T, PollakP, TarlynN, TaylorLP.1994.Pollination- or wound-inducedkaempferolaccumulation in petunia stigmasenhancesseed production. Plant Cell 6:11–23

155.Wang H, Woodson WR. 1991. A flowersenescence-related mRNA from carnationshowssequencesimilarity with fruit ripen-ing-related mRNAs involved in ethylenebiosynthesis.Plant Physiol. 96:1000–1

156.WeidhaseRA, Kramell H-M, Lehmann J,LiebischH-W, LerbsW, Parthier B. 1987.Methyljasmonate-induced changes in thepolypeptidepatternof senescingbarleyleafsegments.Plant Sci. 51:177–86

157.WeissMR. 1991. Floral colour changesascues for poll inators.Nature354:227–29

158.Whitehead CS, Fujino DW, Reid MS.1983.Identificationof theethyleneprecur-sor 1-aminocyclopropane-1-carboxylic acid(ACC) in pollen.Sci. Hortic. 21:291–97

159.WhiteheadCS,FujinoDW,ReidMS.1983.The rolesof pollen ACC andpollen tubegrowth in ethylene production by carna-tions.Acta Hortic. 141:221–27

160.Whitehead CS, Halevy AH, Reid MS.1984. Rolesof ethyleneand1-aminocyclo-propane-1-carboxylic acid in poll inationandwound-inducedsenescenceof Petuniahybridaflowers.Physiol. Plant. 61:643–48

161.Whitehead CS, Halevy AH, Reid MS.1984. Control of ethylenesynthesisduringdevelopmentandsenescenceof carnationpetals.J.Am.Soc.Hortic. Sci. 109:473–75

162.Wiermann R, Vieth K. 1983. Outer pollenwall, an important accumulation site forflavonoids.Protoplasma118:230–33

163.Wil lemseMTM, van Went JL. 1984. Thefemale gametophyte. See Ref. 66a, pp.159–96

164.WingRA,YamaguchiJ,Larabell SK,UrsinVM, McCormick S. 1989. Molecular and


genetic characterization of two pollen-ex-pressedgenesthathavesequencesimilarityto pectatelyasesof the plantpathogenEr-winia. Plant Mol. Biol. 14:17–28

165.WolteringEJ.1989. Lipcoloration in Cym-bidium flowers by emasculation and bylip-produced ethylene.Acta Hortic. 261:145–50

166.Woltering EJ. 1990. Interorgan transloca-tion of 1-aminocyclopropane-1-carboxylicacid andethylenecoordinatessenescencein emasculated Cymbidium flowers.PlantPhysiol. 92:837–45

167.Woltering EJ. 1990. Interrelationship be-tween the different flower parts duringemasculation-inducedsenescencein Cym-bidiumflowers.J. Exp. Bot. 41:1021–29

168.Woltering EJ. 1994. Ethyleneand orchidflower senescence:roles of ethyleneandACC in inter-organ communication inCymbidiumflowers.Proc.NagoyaInt. Or-chid Congr., pp. 64–70. Nagoya, Jpn: Na-ganae Print. Co.

169.Woltering EJ, Ten Have A, Larsen PB,WoodsonWR.1994. Ethylenebiosyntheticgenes and inter-organ signalling duringflower senescence.In Molecular and Cel-lular AspectsofPlantReproduction,ed.RJScott, AD Stead,pp. 285–307.Cambridge:CambridgeUniv. Press

170.WoodsonWR, Lawton KA. 1988. Ethyl-

ene-inducedgene expressionin carnationpetals. Relationship to autocatalytic ethyl-ene production and senescence.PlantPhysiol. 87:498–503

171.Woodson WR, ParkKY, Drory A, LarsenPB,WangH. 1992. Expression of ethylenebiosynthetic pathwaytranscriptsin senesc-ing carnation flowers. Plant Physiol. 99:526–32

172.YamaneH, Abe H, Takahashi N. 1982.Jasmonicacidandmethyl jasmonatein pol-lensandanthersof threecamellia species.Plant Cell Physiol. 23:1125–27

173.Yasugi S. 1983. Ovule andembryo devel-opment in Doritis pulcherrima (Orchi-daceae).Am.J. Bot. 70:555–60

174.Yeung EC,Law SK. 1989. Embryology ofEpidendron ibaguense. I. Ovule develop-ment. Can. J. Bot. 67:2219–26

175.Yip KC, Hew CS.1988. Ethyleneproduc-tion by young Aranda orchid flowersandbuds.Plant Growth Regul. 7:217–22

176.Zhang XS, O’Neill SD. 1993. Ovary andgametophytedevelopmentarecoordinatelyregulated following poll ination by auxinandethylene.Plant Cell 5:403–18

177.ZhangYX, LespinasseY. 1991. Pollinationwithgamma-irradiatedpollenanddevelop-mentof fruits, seedsandparthenogeneticplantsin apple. Euphytica 54:101–9

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