The receptive surface of the angiosperm stigma · 1234 Heslop-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma A major comparative study of the stigma surface

Ann. Bot. 41, 1233-1258, 1977

The Receptive Surface of the Angiosperm Stigma

YOLANDE HESLOP-HARRISON*Department of Botany, University of Massachusetts, Amherst, Mass. 01003, U.S.A.

and

K. R. SHIVANNADepartment of Botany, University of Delhi, Delhi 110007, India

Received: 14 January 1977

ABSTRACT

This paper reports upon a study of the characteristics of the receptive surfaces of angiosperm stigmas,covering almost 1000 species of about 900 genera of some 250 families. In both monocotyledons anddicotyledons the major subdivision is into those stigmas which are 'dry' at maturity, having a hydrated,proteinaceous extracuticular layer or pellicle but no free-flowing secretion, and those which are 'wet'bearing such a fluid secretion when in the receptive state. Further subdivision may be made talcing intoaccount the nature of the surface cells—whether or not the receptive surface is papillate or smooth, and ifpapillate, whether the papillae are unicellular or multicellular. When the genera are classified according tothese criteria, various taxonotnic regularities emerge. Many families are homogeneous in stigma type, butsome prove to be diverse. Among these are families such as the Liliaceae, a fact that may have phylogeneticsignificance.

The physiological importance of stigma type is shown by the correlations that exist between the charac-teristics of the receptive surface and self-incompatibility system. Sporophytic self-incompatibility systemsare associated with dry, papillate stigmas; most gametophytic systems with wet stigmas. Further relation-ships exist with pollen type and physiology. Trinucleate pollen, not readily germinated in vitro, tends to beassociated with dry stigmas, while wet-stigma forms tend to have binucleate pollen, easily germinated inliquid or semi-solid media; binucleate pollen, however, occurs with both wet and dry stigmas.

INTRODUCTION

The detailed structure and functions of the receptive surface of the angiosperm stigma—that part specialized for the receipt and early nurture of the male gametophyte—have beenrelatively neglected through much of the present century, notwithstanding the intense in-terest of many earlier investigators. In 1824 Amici made his pioneer observation of pollengrains germinating on the stigma of Portulaca oleracea, and in the same year Raspail (1824)used stigma features in a classification of the genera of the Gramineae, taking into accountboth the form of the stigma lobes and the presence or absence of papillae. Hartig (1842)noted that some stigmas carried 'absorbent hairs' or papillae, as in Matthiola, Glaucium,Capsella and Clarkia, whereas other stigmas appeared naked or destitute of hairs butsecreted a 'mucous' covering {Petunia, Nicotiana, Atropd). Capus (1878) made a carefulstudy of the anatomy of the style and stigma in relation to the path taken by the pollentubes, and noted many important features of the stigmatic surface, observing such differ-ences as the presence or absence of simple (unicellular) or compound (multicellular)papillae. Capus also distinguished between species with a dry stigma surface and those witha wet surface, where the papillae were often necrotic at maturity, a distinction later empha-sized by Burck (1902), according to Konar and Linskens (1966). The transmitting tracts ofthe style were included in Capus's studies, and he noted a further distinction here.betweenthose species with a distinct stylar canal and those with a solid style.

• Present address: Welsh Plant Breeding Station, Plas Gogerddan, Aberystwyth.

1234 Heslop-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma

A major comparative study of the stigma surface and stylar transmitting tract was pub-lished by another French botanist, Gueguen (1900-1902) who examined species of over onehundred genera of apetalous and gamopetalous dicotyledons, as well as some mono-cotyledons, belonging to some fifty families. Following Gueguen interest declined, and formuch of the present century botanists have been preoccupied with the gross features of thestyle and stigma in relation to taxonomy and pollination biology, largely ignoring theearner detailed anatomical work. In consequence, general botanical texts of the last seventyyears have had little to say about the pollen-stigma interaction or the life of the malegametophyte after its capture, while often devoting many pages to flower morphology andpollination mechanisms.

The current revival of work on the stigma has resulted from interest in its function andthat of the transmitting tracts of the style in relation to the control of breeding systems,notably in connection with self-incompatibility. Vasil and John (1964) published a valuablecomparative study of the surface features of stigmas and the subsequent path of the pollentube in seven species belonging to six families. Kroh (1964) gave the first ultrastructuralaccount of the stigma surface and pollen-tube penetration for Brassica oleracea, confirmingand extending many of the light-microscopic observations made earlier on another cruci-ferous genus, Cardamine, by Christ (1959). The stigma surface and transmitting tracts ofLilium have been investigated by Rosen (1964), Welk, Millington and Rosen (1965), Rosenand Thomas (1970) and Dashek, Thomas and Rosen (1971), and other recent studiesinclude those of Konar and Linskens (1966) on Petunia; Dickinson and Lewis (1973a, b) onRaphanus; Dulberger (1974) onLinum and Dulberger (1975) onPlumbaginaceae; Dickin-son and Lawson (1975) on Oenothera; Mattsson, Knox, Heslop-Harrison and Heslop-Harrison (1974) on Raphanus; Heslop-Harrison, Knox, Heslop-Harrison and Mattsson(1975) on various Cruciferae and Caryophyllaceae; Heslop-Harrison, Heslop-Harrisonand Barber (1975) on various families; Pettitt (1976) on Thalassia and Thalassodendron;J. Heslop-Harrison (1976) on Malus and Prunus and Y. Heslop-Harrison (1977) on Crocus.

The recent work has shown that the pollen-stigma interaction is a complex one, and hasindicated that the stigma surface may play a vital part in controlling interspecific hybridi-zation and regulating compatibility relationships within species. The structural and physio-logical features of the pollen-capturing surfaces vary considerably between families andsometimes even within families, and these characteristics often prove to be related to theoperation of the breeding system. Accordingly the comparative morphology and physi-ology of stigmas merit investigation in their own right for the light they can throw onimportant aspects of reproductive biology. In this paper we present a general analysis ofangiosperm stigma surfaces and a classification based on that proposed by J. Heslop-Harrison (1975a, b, 1976; see also Heslop-Harrison, Heslop-Harrison and Barber, 1975).In the course of the work the features of the receptive surfaces of the stigma have beenstudied in nearly 1000 species of about 900 genera of some 250 families, so that it is likelythat the spectrum of variation has been covered reasonably well. The survey is thereforesufficiently comprehensive to permit certain general conclusions to be drawn. In particularit has been possible to assess the significance of features that relate to the capture, recog-nition, selection and control of germination of pollen at the stigma surface. Such adapta-tions have obviously been of great importance in the evolution of the angiosperms, andsome of the evolutionary and phylogenetic implications are briefly discussed.

MATERIALS AND METHODSFlowers at anthesis and in various stages of development were collected from plants held bythe Living Collections Division of the Royal Botanic Gardens, Kew. In protandrousspecies it was usually necessary to remove the anthers before they dehisced, and the cleanstigmas uncontaminated by captured grains were then allowed to mature in the laboratoryuntil they were in a fully receptive state.

Heslop-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma 1235

The preliminary survey of the fresh stigmas was made with a binocular dissecting micro-scope, and more detailed features were examined after mounting whole or part of thetissues in phosphate-buffered sucrose (005 M, pH 7-2) of an appropriate tonicity to main-tain the form of the stigma papillae.

Earlier indications that the receptive surfaces in all types of stigmas almost invariablyshow cytochemically-detectable esterase activity (Mattsson, et ah, 1974; Heslop-Harrison,et al., 1975) were confirmed during the present study, and indeed it ultimately becameapparent that the pollen-capturing sites could actually be identified by such activity instyles of complex form with non-receptive trapping or brush hairs and other elaborations,or where, as for example in Castanea, only a very few cells are receptive. For the localizationof esterase activity, the method of Pearse (1972) was used, with a-naphthyl acetate as a sub-strate in a coupling reaction with Fast Blue B salt. Controls were run without substrate.

Characteristics of the cuticle of the cells of the receptive surfaces were observed afterstaining in the fluorescent dye, auramine O (Y. Heslop-Harrison, 1977), made up at 0-01per cent in phosphate-buffered sucrose of appropriate tonicity. Surface lipids were foundsometimes to obscure certain features of cuticular patterning, and comparisons were there-fore made of stained fresh stigmas with those previously rinsed with ether: methanol (1/1,V/V). Observations were made with the Vickers Photoplan system with incident illumina-tion, using Vickers exciter filter No. 1 and barrier filter No. 3. With this combination theclear yellow fluorescence of the cuticle can readily be distinguished from the greenish fluor-escence of cytoplasm and the lipidic components of the surface secretions of wet stigmas.

Stigmas for scanning electron microscopy were mounted in the fresh state in a slow-drying glue and observed without coating (Y. Heslop-Harrison, 1970).

The families in Table 3 are numbered according to the Kew List, used in the Herbariumof the Royal Botanic Gardens, Kew, and also by the British Museum, Natural History. Thenomenclature of the families follows the Kew List, with the principal synonyms fromRouleau (1970).

The full list of species studied has been deposited in the Library of the Royal BotanicGardens, where it is available for consultation.

CLASSIFICATION OF STIGMA TYPES

Classificatory categories

Taxonomically speaking, the stigma surface is as variable as other morphological featuresof the flowering plant, and even closely related species rarely possess identical characteris-tics. However, the survey has shown that the types encountered can be classified relativelyeasily into the broad groupings set out in Table 1.

The principal subdivision is into stigmas of the 'dry' type, with little or no surface secre-tion at maturity, and the 'wet', where a distinct surface secretion is present, with a free fluidsurface. In the latter group, the secretion may be copious enough to appear as a distinctglobule. As a simple rapid test, a stigma may be characterized as 'wet' if when in the recep-tive state the secretion can be printed clearly onto a dry, non-absorbent surface.

Within the 'dry' and 'wet' categories, the taxa can be classified according to the form ordisposition of the surface cells, which morphologically speaking belong to the epidermis.Where the stigma surface is relatively smooth, the bounding cells are referred to as 'surfacereceptive cells'. This then reserves the term 'papilla' for use in its proper botanical sense torefer to those single or grouped stigmatic receptive cells which stand significantly free fromeach other for some of their length above the general level of the stigma surface.

The dry stigma types are further subdivided. Group I accommodates the plumose formcharacteristic of most Gramineae, where there are discontinuities along the receptive sur-face {Dactylis glomerata, Plate 1A, B). Group II includes those stigmas where the receptivesurface is concentrated into distinct ridges, zones or heads. The receptive surfaces of Group


T A B L E 1. General classification of angiosperm stigma types based on the morphology of thereceptive surface and the amount of secretion present during the receptive period {after J.

Heslop-Harrison, 1976)

Dry stigmas (without copious fluid secretions)Group I. Plumose, with receptive cells dispersed on multiseriate branchesGroup II. Receptive cells concentrated in distinct ridges, zones or heads

A. Surface non-papillateB. Surface distinctly papillate

(/.) Papillae unicellular(//.) Papillae multicellular

(a) Papillae uniseriate(b) Papillae multiseriate

Wet stigmas (surface secretions present during receptive period)Group HI. Receptive surface with low to medium papillae; secretion fluid flooding intersticesGroup IV. Receptive surface non-papillate; cells often necrotic at maturity; usually with more surface

fluid than Group HI

II are broadly divisible into A, non-papillate, and B, papillate categories. 'Non-papillate'means having a smooth surface, or one with no more than slight bullations (Euphorbiasanguinea Plate lc, D). By far the largest numbers of taxa in the dry category have papillatestigmas (Table 2), and these can be further grouped according to whether the papillae are, i,unicellular (Iberis semperfiorens, Plate 2A, Matthiola incana, Plate 2B; Hibiscus rosa-sinensis, Plate 2c; Schizostylis coccineus, Plate ID), or, ii, multicellular. The multicellularcategory can be conveniently divided into those stigmas where the cells are arranged in (a)uniseriate, or (b) multiseriate order. An example of the uniseriate type is provided byLopezia cornuta (Plate 3A, B) and of the multiseriate by Rosa pendulina (Plate 3c, D).

Further subdivisions of the dry, multicellular category would be possible, but such re-finement is unnecessary for the present purposes. One type of variation may be noted, how-ever : namely the potential for branching. Both uniseriate and multiseriate papillae may bebranched or unbranched, and where branching occurs the form may be quite complex.Examples are found in Epilobium (Onagraceae), where the papillae are uniseriate withoccasional branches, and Aechmea (Bromeliaceae), where the multiseriate papillae areregularly branched.

Among the wet stigma types two main categories may be distinguished, Group HIbearing a receptive surface consisting of low to medium-length papillae or with a marginalfringe of long papillae, and Group IV where the receptive surface is essentially non-papil-late, the secretory cells being flat or only slightly bullate. Wet-stigma types of Groups HIand IV commonly occur in markedly protandrous flowers, and in these the stigma surfaceat anthesis may appear dry. This is the situation in many Liliaceae and Bromeliaceae, wherethe stigmas in freshly opened flowers could be misclassified as dry papillate, Group EEB. At alater stage, however, the stigmatic lobes may open out further and then a copious secretionappears and the papillae become partially inundated. A developmental sequence showingthis change is seen in Plate 4A, B and c, of the progressive accumulation of secretion productmLonicerapericlymenum. In this case the secretion is released near the base of the papillaemore or less simultaneously over the stigma head. The behaviour is characteristic of severalgenera of the Liliaceae (e.g. Hosta) and Saxifragaceae, and it has been described in Petunia(Solanaceae) by Konar and Linskens (1966). In the Prunoideae and Pomoideae of theRosaceae the stigmas may be wet at anthesis, but the main secretion follows later, and herethe walls at the base of the papillae show the internal ramifications of the transfer-cell typecommonly found in secretory tissues (J. Heslop-Harrison, 1976). It is noteworthy that in allof these examples the surface cells are disrupted during the emission of the secretion, andare therefore moribund or dead when the stigma surface is fully receptive. In stigmas of


T A B L E 2. Genera of the families of monocotyledons and dicotyledons examined, grouped inthe categories of Table 1. Families, and genera within families, listed alphabetically

A. MONOCOTYLEDONS

DRY STIGMAS

Group I (Plumose, with receptive cells dispersed in multiseriate branches)Gramineae: Alopecurus; Andropogon; Anthoxanthum; Arrhenatherum; Bothriochloa; Briza;

Bromus; Cynodon; Dactylis; Elymus; Festuca; Gaudinia; Helictotrichon; Holcus; Hordeum;Lollum; Melica; Molinia; Oryzopus; Phalaris; Phleum; Poa; Triticum; Secale; Setaria; Sorghum;Spartina; Stlpa; Zea

Group II (Receptive cells concentrated in distinct ridges, zones or beads)A. Surface non-papillate

Cyperaceae: CyperusLiliaceae: Aspkodeline, Bowiea, Disporum, Ophiopogon, VeratrumPalmae: PtychospermaPotamogetonaceae: PotamogetonTyphaceae: TyphaZannichelliaceae: Amphibolis; Thalassodendron1

B. Surface papillate(0 Papillae unicellular

Agavaceae: Agave;2 Cordyline; Furcraea; YuccaAlismataceae: EcfdnodorusAmaryllidaceae: Cryptostephanus; Cyrtanthus; Eucharis; Eucrosia; Galanthus; Hippeastrum;

Hymenocallis; Ixiolirion; Leucojum; Narcissus; Nerine; Sternbergia; Urceolina; Zephyran-thus

Aponogetonaceae: AponogetonAraceae: Arisarum; Ptstia; SpathiphyllumButomaceae: ButomusCommelinaceae: Anelima; CaUisia; Camptlia; Commelina; TradescantiaCyperaceae: Btysmus; Carex; Eleocharis; SctrpusEriocaulaceae: ErlocaulonGramineae: MiboraHaemodoraceae: XiphidiumHydrocharitaccae: Thalassia1

Hypoxidaceae: Hypoxts; RhodohypoxisIridaceae: Alophia; Anomalheca; Arlstea; Babiana; Belamcanda; Chcamanthe; Crocosmia;

Crocus; Curtonis; Dierama; Dieles; Diplarrhena; Freesia; Gladiolus; Hesperantha; Iris;Ixia; Lapeyrousia; Montbretia; Morea; Neomarica; Orthosanthus; Rigidella; Romulea;Schizostylis; Sisyrinchium; Sparaxis; TigriaHa; Tritonia; Watsonia

Juncaceae: Juncus; LuzulaJuncaginaceae: TriglochlnLiliaceae s.l.: Agapanthus; Albuca; Allium; Anthericum; Aphyllanthes; Asparagus; Asphodelus;

Astelia; Astroloba; Bulbinella; Calochortus; Chamaealoe; Chionodoxa; Chlorophyton;Clintonia; Colchicum; Dasystachys; Dianella; Dichopogon; Dipcadi; Drimiopsis; Echean-dia; Endymion; Erythronium; Eucomis; Fortunata; Geitonoplesium; Haworthia; Hyacinthus;Ipheion; Kniphofia; Lachenalia;Leopoldia; Liriope; Maianthemum; Massonia; Notholirton;Northoscordum; Paradisea; Pasithaea; Poellnitzia; Pofygonatum; Puschkirda; Reineckia;Sandersonia; SciUa; Scollopus; Smilax; Speirantha; Thysanotus; Trillium; Tullpa; Vel-theimia; Whiteheadia

Palmae: ChamaedoraPhilydraceae: OrthotkylaxPontederiaceae: Eichomia; PontederiaScheuzeriaceae: ScheuzeriaSparganiaceae: SpargardumTaccaceae: Tacca

(ii) Papillae multicellular(a) Papillae uniseriate

Arnaryllidaceae: CaliphruriaHypoxidaceae: CwculigoLiliaceae: Philesia


TABLE 2—continued

(b) Papillae multiseriateBromeliaceae: Abromeitella; Dyckia; NeoregeliaFlagellariaceae: FlagellariaHydrocharitaceae: LLmnobium

WET STIOMAS

Group IH (Receptive surface with low to medium papillae)Agavaceae: Agave1; BeschorneriaAlstroemeriaceae: AlstroemeriaAmaryllidaccae: Habranthus; Rhodophiala; SprekeliaBromeliaceae: Aechmea; Bilbergia; Bromelia; Canistrum; Fosterelia; Nidularia;Pitcairnia;Portea;

Quesnelia; Streptocalyx; VrieslaCannaceae: CannaCommelinaceao: Gibasis; Thyrsanthemum; WeldeniaCostaceae; Cost usCyclanthaceae: CarludoviciaHaemodoraceae: Anigozanthos; WachendorfiaLiliaceae: Aloe; Arthopodium; Bloomeria; Drimia; Eremwus; Frttillaria; Galtonia; Gasteria;

HemerocaUis; Hosta; Hyadnthelia; Lapageria; Leucocoryne; IMium; Merendera; Muscaria;Omithogalum; Ruscus; Tricyrtis

Musaceae: Heliconia; Musa; StrelltziaOrchidaceae: Anacamptis; Bletilla; Cattleya; Coebglossum; Dactylorhiza; Dactylorhynchus;

Dendrobium; Epipactis; Goodyera; Gymndenia; Miitonia; Neottia; Odontoglossum; Ophrys;Orchis; Paphiopedilum; Platanthera; Spiranthes

Xanthorrhoeaceae: Lomandra

Group IV (Receptive surface non-papillate; cells often necrotic at maturity)Agavaceae: Dracaena; PleomeleAraceae: AlocasiaCommelinaceae: CyanotisDioscoreaceae: TamusLiliaceae: Camassia; Iphigenia; UrgiidaLowiaceae: OrchidanthaMarantaceae: Calathea; Maranta; Marantachloa; Stromanthe; TrachyphryniumZingiberaceae: Alpinia; Cautleya; Curcuma; Globba; HedycMum; Kaempfera; Roscoea; Zingiber

B. DICOTYLEDONSDRY STIOMAS

Group I (Plumose, with receptive cells dispersed on multiseriate branches)No families

Group II (Receptive cells concentrated in distinct ridges, zones or heads)A. Surface non-papillate

Acanthaceae: Acanthus; Asytasia; Eranthemum; Hypoestes; Justicia; Schaueria; RuelllaAccraceae: AcerAsclepiadaceae:/tsc/epto; VincetoxicumBerberidaceae: Nandina; PlagiorhegmaBetulaceae: Abuts; BetulaBrexiaceae: BrexiaCalycanthaceae: Catycanthus; ChimonanthusCapparidaceae: Capparis; Euadenia; IsomerisCelastraceae: Euonymus; Cassine; MaytenusChloranthaceae: ChloranthusCornaceae: Aucuba; CornusCorylaceae: CorylusCucurbitaceac: SicyosDavidiaceae: DavidiaDioncophyllaceae: HabropetalumDipsacaceae: Knautia; Scabiosa; Succisa; SucclsellaEbenaceae: DiosporosElaeagnaceae: ElaeagnusEucryphiaceae: Eucryphia

Heslop- Harrison and Shivama—The Receptive Surface of the Angiosperm Stigma 1239

TABLE 2—continued

Euphorbiaceae: Breynia; Dalechampia; Euphorbia; Homalanthus; Poinsettia; SeccuringaFagaccae: Costarica; Fagus; Uthocarpus; Notkofagus; QuercusFlacourtiaceae: AzaraFrancoaccac: FrancoaGarryaceae: GarryaHamamelidaceae: Corylopsis; Distylium; Hamamelis; Parrot ia; TrichocladusHelwingiaceac: HelwingiaHemandiaceae: HemancUaDliciaceae: IlliciumJuglandaceae: Juglans; PterocaryaLabiatae: Mentha; Rosmarinus; Salvia; SatureiaMalvaceae: AnodaMarcgraviaceae: MarcgraviaMenispermaceae: StephaniaMoraceae: DorsteniaMyricaccae: MyricaOchnaceae: OchnaOleaccae: ChionanthuasPassifloraccae: AdeniaPiperaceae: PeperomiaPlumbaginaceae*: Acantkolimon; Armeria; LAmoniumPodoaceae: CampylopetatumPolygalaceae: PotygalaPolygonaceae: Fagopyrum; RheumPrimulaceae: CyclamenRanunculaccae: Aconitum; Aquilegia; DelphiniumResedaceae: Astrocarpus; ResedaRosaceac: PotentillaRubiaceae: PsychotriaRutaceae: Correa; Chotsya; Pilocarpus; SkimmiaSabiaceae: MeliosmaSchrophulariaceae: VeronicastrumSelaginaceae: HebenstretiaSimaroubaceae: Brucea; PicrasmaStyracaceae: HalesiaTheophrastaceae: ClavijaTropaeolaccae: TropaeolumTumeraceae: TurneraVitidaceae: Cissus; Cyphostemma;Parthenocissus

B. Surface papillate(0 Papillae unicellular

Acanthaceae: Barleria; Carpanthe; Hemigraphis; StrobilanthesAceraceae: DipteroniaAdoxaceae: AdoxaAizoaceae: CarpantheaAltingiaceae: LiquidambarApocynaceae: StrophanthusAraliaceae: Delarbrea; HederaAristolcxjhiaceae: AristolochlaBaueraceae: BaueraBegoniaceae: BegoniaBombacaceae: BombaxBoraginaceae: Alkanna; Anchusa; Borago; Cerinthe; Cynoglossum; Echium; Ehretia; LJn-

delofia; Uthodora; Mertensia; Myosotis; Nonea; Omphalodes; Paracaryum; Pentagbttis;Symphytum

Buxaceae: Pachysandra; SarcococcaCampanulaceae: Asyneuma; Campanula; Codonopsis; Jasione; Musschia; PhyteumaCannabaceae: Cannabis; HumulusCapparidaceae: CleomeCaricaceae: CaricaCarpinaceae: Carpinus; Ostrya


TABLE 2—continued

CaryophyUaceae: Agrostemma; Alsinodendron; Dianthus; Gypsophila; Lychnis; Melandrium;Saponwia; Silene

Chenopodiaceae: Beta; Chenopodium; Hablitzia; RhagodiaClethraceae: ClethraCobaeaceae: CobaeaCompositae: Achillea; Anthemis; Aster; Centaurea; Chrysanthemum; Cosmos; Crepis;Eupa-

torium; Gazania; Helenium; HcUanthus; Hleraclum; Santolina; Senedo; Serratula; Vernona;WedeUa

Convolvulaceae: Argyreia; Cafystegia; Convohulus; Cuscuta; Ipomoea; Stictocardia; TurbinaCoriariaccae: CoriariaCruciferae: Atyssum; Arabis; Aubretia; Berteroa; Brassica; Capsella; Cwdamine; Chetranthus;

Dlplotaxis; Erophila; Eruca; Erucastrum; Draba; Hesperis; Iberis; Lunularia; Malcohnia;Matthiola; Moricanda; Rapkanus; Sinapis; Sisymbrlum

Cucurbitaceae: CucumisCunoniaceae: CunoniaDaphniphyllaceae: DaphnlphylhmDatiscaceae: DatiscaElaeocarpaceae: Aristotelia; Crinodendron; ElaeocarpusErythroxylaccae: ErythroxylonFrankeniaccae: FrankeniaGesneriaceae: Aeschynanthus; Columnea; Fieldia; SaintpauliaGoodeniaccae: ScaevolaGunneraccae: Gunner aHaloragaceae: MyriophyllumHippocastanaceac: AesculusHippuridaceae: HippwisHydrangeaceae: Carpentaria; Detiumthe; Hydrangea; Jamesia; Kirengeshoma; Philadelphus;

Pileostegia; SchizophragmaHydrophyllaceae: PhaceliaHypericaceae: HypericumIllecebraceae: HerniariaLabiatae: Leonurus; Phiomis; Scutellaria; ThymusLauraceae: Cinnamomum; Laurus; UmbeUulartaLimnanthaccae: LlmnanthesLinaccae:* JJnum; ReinwardiaLoasaccae: Blumenbachia; Cajophora; Loasa; MentzeliaLythraceae:* Cuphea; LythrumMagnoliaceae: Liriodendron; Magnolia*Malpighiaceae: TrichomariaMalvaceae: Abutilon; Althaea; Afyogyne; Goethea; Gossypium; Hibiscus; Hoheria; Kitaibelia;

Lagunaria; Lavatera; Malope; Malva; Malvastrum; Malvaviscus; Modiola; Pavonia;Robinsonella; Slda; Sidalcea; Sphaeralcea; Urena; Urcarpidium

Moraccae: Brosimum; Ficus; Morus; PseudomorusMyoporaccac: EremophilaMyrsinaceae: Edgeworthia; MaesaMyrtaceae: Calothamnus; Eugenia; Feijoa; Leptospermum; SyzygiumNcpenthaceae: NepenthesNyctaginaccae: Mirabilis; OxybaphusNymphaeaceae: NupharOleaceae: Abeltophyllum; Fraxinus; Ligustrum; Osmanthus; PhilfyreaOnagraccae: ClarkiaOrobanchaceae: OrobanchePapaveraceae: Chelldonium; Dendromecon; Dicranostigma; Eomecon; Eschscholtzla; Glau-

cium; Hypecoum; Macleya; Meconopsis;Papaver; RomneyaParnassiaceae: ParnassiaPassifloraceae: PassifloraPhytolaccaceae: Ercilla; PhytolaccaPiperaceae: PiperPlantaginaceae: PlantagoPlatanaccac: PlatanusPlumbaginnorae:* Acantholimon; Armeria; LimoniumPolcmoniaceae: Coliomia; Gilia; Phlox; Polemonium

Heslop- Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma 1241

T A B L E 2—continued

Polygonaceae: Potygonum; OxyriaPortulacaceae: Claytonia; Portulaca; TalinumPrimulaccae :• Ardisiandra; PrimulaProteaceae: Embothrium; GrevilleaRanunculaceae: Actaea; Adonis; Anemone; Anemopsis; Cimi/uga; Clematis; Helleborus;

Laccopetalum; Myosurus; Nigella; Ranunculus; Thaltctrum; Trautvetteria; TrolltusRhamnaccae: Ceanothus; Noltea; Paliurus; Pomadenis; SpyrUtiumRosaceae: Filipendula; GeumRubiaceae: Bouvwdla; Burchellia; Coprosma; Crucianella; Dlctamnus; Galium; Hamelia;

Ixora; Pentas; Pseudomussaenda; RondeleliaRutaceac: Crowea; Eriostemon; EuodiaRnHrnpi-a^- SalixSambucaceae: SambucusSapotaccae: LucumaSarraceniaceac: SarraceniaSaururaceac: Houttuynia; SaururusSaxifragaceae: Astilbe; Uthophragma; Rodgersia; Saxifrage?Scrophulariaccae: Antirrhinum; Chelone; Digitalis; Gratiola; Hebe; Lathraea; Linaria;

Pentstemon; Scrophularia; Torenla; Verbascum; VeronicaSelaginaceae: GlobulariaSolanaceac: SolandraSterculiaceae: TheobromaStylidiaceae: StylidiumStyracaccae: StyraxThymelaeaceae: Daphne; PimelaeaUlmaceae: Celtts; Ulmus; ZelkovaUrticaccac: Helxine; Laportea; ParietariaValerianaceae: Cent ranthus; ValerianaZygophyllaccae: Peganum; Zygophyllum

{if) Papillae multicdlular(a) Papillae uniseriate

Amaranthaceae: AmaranthusGeraniaceae: Erodium; Geranium; PelargoniumLee&ceae: Leea

Nymphaeaceae: NymphaeaOleaceae: Forsythta; JasminumOnagraceae: EpilobiumScrophulariaceae: AlonsoaUrticaceae: Urtica

(b) Papillae multiseriatcActinidiaceae: ActinldiaAizoaceae: TetragoniaBerberidaceae: Bongardia; EpimediumCistaceae: Cistus; HelianthemumCucurbitaceae: EcballiumDroseraceae: Dionaea; DroseraEuphorbiaceae: Acatypha; Mercurialls; RidnusMagnoliaceae: MagnoliaMonimiaceae: DoryphoraNyctaginaceae: BougainvilleaNymphaeaceae: VictoriaOxalidaceae: OxalisPlumbaginaceae: Ceratostlgma; PlumbagoPolygonaceae: Muehlenbeckta, RumexRosaceae: Dry as; Potent tUa; Prtnsepta; Rosa; Rubus; SanguisorbaSalicaceae: PopulusTiliaceae: Grewta; Sparmannia; TUia

WET STIGMAS

Group HI (Receptive surface with low to medium papillae)Aizoaceae: ApteniaAnnonaceae: Annona; Friesodielsia


TABLE 2—continued

Apocynaceae: Carissa; MandeoiUa; VincaAraliaceae: Oreopanax; TrevisiaBcrberidaceae: Berber is; Mahonia; RomaniaBignoniaceae: Bignonia; Catalpa; Clytosioma; TecomantheBoraginaceae: HeliotropiumCaprifoliaceae: Abelia; Diervilla; Dipelta; Kolkwitzia; Lonicera; Symphoricarpos; ViburnumCrassulaceae: Altamiranda; Crassula; Echeveria; Kalanchoe; StdumCucurbitaceae: Bryonia; Cyclanthera; EchinocystisEricaceae: Agapetes; Andromeda; Arbutus; Arctostaphylos; Calluna; Cassandra; Daboecia; Enki-

anthus; Erica; Kalmiopsis; Ledum; Menziesia; Pernettya; Pieris; VacciniumGentianaceae: Exacum; Gentiana; OrphiumGesneriaceae: Sinningia; StreptocarpusGrossulariaceae: RibesLeguminosae: Astragalus; Brownea; Cassia; Crotalaria; Galega; Hedysarum; Lathyrus; Lespedeuza;

Leucaeba; Lotus; Lupinus; Medicago; Melilotus; Negretia; Onobrychis; Ononis; Psoralea;Sophora; Strongylodon; Trifolium; Vicia

Lentibulariaceae: Genlisea; Pinguicula; UtriculariaLoganiaceae: BuddleiaMelastomataceae: Amphiblemma; Hypanthe; TibouchinaMeliaceae: Dysoxybn; TurraeaMenyanthaccae: JJmnanthemum; MenyanthesMyrsinaceae: ArdisiaMytraceae: CaUistemon; MelaleucaNolanaceae: NolanaOnagraceae: Camissonia; Circaea; Fuchsia;' LopeziaPaeoniaceae: PaeoniaPedal iaceae: UncarinaPunicaceae: PunicaRosaceae: Malus; Mespilus; Neillia; Osmaronia; Prunus; Pyrus; RhaphiolepisRubiaccae: MussaendaSaxifragaceae: AceriphyUum; Bergenia; Heuchera; Peltiphyllum; Saxifraga;* Teliima; TiarellaSchisandraccae: Kadsura; SchisandraScrophulariaceae: Calceolaria; NemesiaSolanaceae: Atropa; Cestrum; Fabiana; Hyoscyamus;Lycopersicon; Nicandra; Nicotiana;Petunia;

Physalts; Salpiglossis; SolariumStachyuraceae: StachyurusTernstroemiaceae: Eurya; TernstroendaTheaceae: Camellia; Franktinia; StuartiaTheophrastaceae: Dehairainea; JacquiniaThunbergiaceae: ThunbergiaVerbenaceae: Caryopteris; dtharexylum; Gmelina;Lantana; Peirea; VerbenaViolaccae: Hymanthera; ViolaWinteraceae: DrimysZygophyllaccae: Porlieria

Group IV (Receptive surface non-papillate; cells often necrotic at maturity)Anacardiaceae: CotinusApocynaceae: Apocynum; OncinotusAquifoliaceae: IlexAristolochiaceae: Aristohchta6

Asclepiadaceae: Asclepias;'' StephanotisBalsaminaceae: ImpatiensBerberidaceae: Diphyleia; PodophyllumCactaceae: Opuntia; SchlumbergeriaCampanulaceae: Lobelia; PratiaCombretaceae: Languncularia; QuisqualtsCyrillaceae: CyrtitaDiapensiaceae: GalaxDilleniaceae: HibbertiaEpacridaceae: Epacris; RicheaEricaceae: Azalea; Comarostaphylis; Gaultheria; Kalmia; Macleania; RhododendronEscalloniaceae: Corokia; Escallonla; I tea


TABLE 2—continued

Fumariaceae: Adlumia; Corydalis; Dicentra; Fumaria; RupicapnosGreyiaceae: GreyiaGuttlferae: GarciniaLardizabalaceae: Akebia; Decaisnea; Holboettia; SinofranchetiaLecythidaceae: Grias; NapoleonaLeguminosae: MimosaOnagraccae: Cafybphus; Fuchsia;' Gaura; Hauya; Ludwigia; OenotheraPittosporaccae: Citriobatus; Pittosporum; SoltyaPyrolaceae: Chimaphila; PyrolaRosaceae: Alchemilla; PkotirdaRubiaceae: Gardenia; Hamellia; MitriostigmaRutaccae: Citrus; RaveniaSapindaceae: DodonaeaSolanaceae: Datura; SchizanthiuStaphyleaceae: StaphyleaSterculiaceac: Fremontodendron; Herrania; ThomasisTamaricaceae: TamarixUmbelliferae: Astrantia; Bupleurum; Chaerophylhtm; Cruciella; Daucus; Eryngium; Hacquetia;

Heracleum; Laserpitium; Orlaya; Pimpinella; SelinumVerbenaceae: Oxera

* Heterostylous species occur in some genera.1 Thalassodendron and Thallassia have submerged flowers, but the receptive surface of the stigma has the

characteristic features of Group n .1 Agave: possibly heterogeneous.3 Magnolia: see text and Table 3.* Saxifraga has at least one anomalous species; see text.5 Fuchsia is heterogeneous; see text.4 Receptive surface is not readily located in Aristobchia, and the genus requires further study.7 Asclepias: possibly heterogeneous.

Group IV with non-papillate or only slightly raised cells the secretion is released simul-taneously over the whole surface, often forming a large globule (Heracleum mantegazzia-num, Plate 4F,G). Again the surface receptive cells may be moribund at maturity, as inOenothera organensis (Dickinson and Lawson, 1975).

In certain species with wet stigmas a stylar canal lined with glandular hairs is present, asin some Liliaceae and Bromeliaceae. These cells secrete as the stigma reaches maturity, andmay produce a copious outflow which wells up to join the surface secretions. A stylar canalis found in dicotyledonous families such as the Ericaceae, but here the cells lining the canaldo not seem to make a major contribution to the stigma surface secretion, which is derivedmainly from the surface papillae, as in Calluna vulgaris (Plate 4D, E). Cells of the trans-mitting tract of species with solid styles secrete into the intercellular spaces, but there is noindication that the secretion can ever reach the stigma surface.

Interestingly, detailed study of the wet-stigma species of Group III showed that here, asin the dry-stigma category Group IIB, the papillae may be unicellular or multicellular, andthe multicellular types may be uniseriate or multiseriate. A further subdivision could besought on this basis, but it was deemed unnecessary in the present survey.

In considering the validity of the classification adopted here one must of course be awarethat, as in most biological classifications, the subdivisions are to some extent arbitrary sinceit is a continuum that is being treated. The recognition of 'dry' and 'wet' classes is con-venient and undoubtedly acknowledges a very important functional distinction, but thetwo categories do intergrade. The secretion of the wet-stigma type is often conspicuouslyapparent to the naked eye, or, when present in smaller quantities, is readily seen with thejnicroscope, without preparation. But sometimes it may be restricted to the intersticesbetween the papillae, to be detected, often as a viscous emulsion, only after staining; and


T A B L E 3. Families of the flowering plants, in alphabetical order, showing the distribution ofthe genera examined in the stigma-type classes of Table 1. The first figure in each entry indi-cates the number of genera, and the bracketedfigure the number of species. The code numbers

are those of the Kew List, which has been taken as a standard for family nomenclature

Kewlist no.

Family Group Group nI A B

Group Group

m iv11

(a) (b)

A. MONOCOTYLEDONS

174/4194/1174/3174/1195/5191171194/2170/6183/1170/2189199176/1196185200

172/1167174/2173/1186/1195/2178/1

170/5170/3170/4

169187180179196/5195/3190/2175190/1178/2195/9170/1

122

51/3

AgavaceaeAlismataceaeAlstroemeriaceaeAmaryllidaceaeAponogetonaceaeAraceaeBromeliaceaeButomaceaeCannaceacCommelinaceaeCostaceaeCyclanthaccaeCyperaccaeDioscoreaceaeEriocaulaccaeFlagellariaceaeGramineae 29(39)

(Poaceae)HaemodoraceaeHydrocharitaccaeHypoxidaceaeIridaceacJuncaccaeJuncaginaceacLiliaceae

(inc. Aphyllanthaccae,Asparagaccae, Alliaceae,Philcsiaceae, Smilacaceac,Trilliaceac)

LowiaccacMarantaceaeMusaceae

(inc. Heliconiaccae,Strelitziaceac)

OrchidaccaePalmacPhilydraceaePontcderiaceaePotamogetonaceaeScheuzcriaceaeSparganiaceaeTaccaceaeTyphaceacXanthorrhoeaceaeeZannichclliaceaeZingiberaceae

1

1

5

1

1(2)

1

2(3)

41

14(16)13

1

5

4

1

112

30(54)21(2)

55(58)

1(2)12

111

B. DICOTYLEDONSAcanthaceae

(see also Thunbergiaccae)Aceraceae

7

1(2)

4

1

2(3)

1(2)3

3(4) 11(12)

131(4)1

19

3(6)

18

8(9)

Heslop-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma

TABLE 3—continued

1245

Kcwlist no.

28/583/47962/213053/15/110646/181138107

38/859/13767/1

159/1

120/131/2112/159/8151/278/1391/1

153/412/1

83/174/4159/222/147/1131/11401493/3120/26688

113/1

5482/1159/260/1

Family

ActinidiaceaeAdoxaceaeAizoaceaeAltingiaceaeAmaranthaceaeAnacardiaceaeAnnonaceaeApocynaceaeAquifoliaccaeAraliaceaeAristolochiaceaeAsclepiadaceae

(inc. Periplocaceae)BalsaminaccaeBaueraceaeBegoniaceaeBerberidaceae

(inc. Leonticaceae,Nandinaceae, Podo-phyllaceae)

Betulaceae(see also Carpinaceae,Corylaceae)

BignoniaceaeBombacaceaeBoraginaceaeBrexiaceaeBuxaceaeCactaceaeCalycanthaceaeCampanulaceae

(inc. Lobeliaceae)CannabaceaeCapparidaccae

(inc. Qeomaceae)CaprifoliaceaeCaricaceaeCarpinaceaeCaryophyllaceaeCelastraceaeChenopodiaceaeChloranthaceaeCistaceaeClethraceacCobaeaceaeCombretaceaeCompositae

(Asteraceae)Convolvulaceae

(inc. Cuscutaceae; seealso Nolanaceae)

CoriariaceaeCornaceaeCorylaceaeCrassulaceae

Group Group III

A

2(3)

2

2(3)

1

2

3

3(4)

1

2<3)1(2)

Bi ii

(a)

111

1(5)

1

21(5)

11(2)

116(17)

2(3)

6(8)

21

12(3)8

4(6)

11

171

7

1

(b)

1

1

2

2(4)

GroupIII

1

23

2

3

4

1

7

5

GroupIV

1

21(2)

1?2?

1(3)

2

2

2(5)

2

1246 Heshp-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma

TABLE 3—continued

Kcwlist no.

11

7559/946/2151/477/182/5962/161/48661/110214733/29593/134/259/759/11151/1159/317/359/5211082/3109/138/111990/159/1059/1264/327/164/162/181143/251/264/259/6

1112622/24/3156/1126

7/2143/167/250/2

Family

Cruciferac(Brass tcaceac)

CucurbitaceaeCunoniaceaeCyrillaceaeDaphniphyllaceaeDatiscaceaeDavidiaceaeDiapensiaccaeDilleniaceacDioncophyllaceacDipsacaceaeDroseraceaeEbenaceaeElaeagnaceaeElaeocarpaceaeEpacridaceaeEricaceaeErythroxylaceaeEscalloniaceaeEucryphiaceaeEuphorbiaceaeFagaceaeFlacourtiaceaeFrancoaceaeFrankeniaceaeFumariaceaeGarryaceaeGentianaceaeGeraniaceaeGesneriaceaeGoodeniaceaeGreyiaceaeGrossulariaceaeGunneraceaeGutttferaeHaloragaceaeHamamelidaceaeHelwingiaceaeHernandiaceaeHippocastanaceaeHippuridaceaeHydrangeaceae

(inc. Philadelphaceae)HydrophyllaceaeHypericaceaeUlecebraceaeIlliciaceaoJuglandaceaeLabiatae

(Lamiaceae)Lard izabalaceaeLauraceaeLecythidaceaeLeeaceae

Group Group III

A

1

1

14

1(2)1

15511

1

511

1(3)24(6)

Bi ii

(a)

22(24)

11

11

3

1

1

3(6)41

1(2)

1

118

11(3)1

4

3

1

(b)

1

2(4)

3

Group Groupm rv

3

1

11

2(3)15(16) 6

3

5(10)

3(4)

2

11(5)

1

4

2

Heslop-Harrison and Shivanna —TheReceptive Surface of the Angiosperm Stigma

TABLE 3—continued

1247

Kewlist no.

57

11738/334/17210869/14/13631/128/36843/16109/2142/1153/5123157100/167/1136113/21288/141/110470/111638/61/310

59/474/1121132/1139/1

181271549811020/113423/19914469/493/21/11349

Family

Leguminosae(Fabaceae)

LentibulariaceacLimnanthaccaeLinaccae*LoasaceaeLoganiaceaeLythraceae*MagnoliaceaeMalpighiaceaeMalvaceaeMarcgraviaccaeMelastomataceaeMeliaceaeMenispermaceaeMenyanthaceaeMonimiaccacMoraceaeMyoporaceaeMyricaceaeMyrsinaceaeMyrtaccaeNepeathaceaeNolanaceaeNyctaginaceaeNymphaeaceacOchnaceaeOleaceaeOnagraceaeOrobanchaceaeOxalidaceaePaeoniaceaePapaveraceae

(inc. Hypecoaceac)ParnassiaceaePassifloraceaePedaliaceaePhytolaccaceaePiperaceae

(inc. Peperomiaceae)PittosporaceaePlantaginaceaePlata naceacPlumbaginaceae*PolemoniaceaePolygalaceaePolygonaceaePortulacaceaePrimulaceae*ProteaccacPunicaceaePyrolaccaeRanunculaceaeResedaceacRhamnaceae

Group Group III

A

11

1(2)

1(2)

1

11

1

1

12(3)

1

52(3)

Bi ii

(a)

124

2V-1

22(23)

41

251

21 1

5 21 11

11(14)

11(2)

21

1(2)134

2322

14(15)

5

(b)

H5)

1

11

1(2)

2

2(5)

Group GroupIII IV

21 1

3(6)

1(2)

32

2

1

43 6

1(3)

1

3

12

1248 Heslop- Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma

TABLE 3—continued

Kewlist no.

58/184/1395216083/251/1101/19139/359/14/6115124

40/111428/751/53289/1103/12824/128/1100/2122145/133/14/738/273153/280

153/185125/11550/14/237

Family

RosaceaeRubiaceaeRutaceaeSabiaceaeSalicaceaeSambucaceaeSapindaceaeSapotaceaeSarraceniaceaeSaururaceaeSaxifragaceaeSchisandraceaeScrophulariaceaeSelaginaceae

(inc. Globulariaceae)SimaroubaceaeSolanaceaeStachyuraceaeStaphyleaceaeSterculiaccaeStylidiaceaeStyracaceaeTernstroemiaceaeTamaricaceaeTheaceaeTheophrastaceaeThunbergiaceaeThymelaeaceaeTiliaceaeTrochodendraceaeTropaeolaceaeTurneraceaeUlmaceaeUmbelliferae

(Apiaceae)UrticaceaeValerianaceaeVerbenaceaeViolaceaeVitidaceaeWinteraceaeZygophyllaceae

Group Group III

A

14(5)1(2)

1

2

1

1

11

3

B

2(3)113

11

1124(18)5

121(2)

1

11(3)1

2

1

3

31(2)

2

ii(a)

1

1

(b)

6

1

3

Group

m

71

722

11(14)1

2

3(4)21(4)

62(5)

11

GroupIV

232(3)

1

2

13

1

12

1

* Linaceae, Lythraceae, Plumbaginaceae and Primulaceae include some heterostyled species in whichthe morphs differ in stigma characteristics. Only in the Plumbaginaceae would the difference be such as towarrant classification in different categories.

1 Most species of the Compositae have papillate stigmas; but in some the papillae are reduced so thatclassification in Group HA would be warranted.

2 In one species, Magnolia grandiflora, the upper part of the stigmatic carpel margin bears unicellularpapillae.

3 Intcrgrades between wet and dry stigma types occur in the Onagraccae. In some instances, dry stigmasoccur in genera which otherwise have wet stigmas; these flowers are probably female sterile.

? Indicates some uncertainty in the classification.


then again it may form no more than a thin, generally dispersed layer, doubtfully dis-tinguishable from the thin hydrated proteinaceous secretions forming the pellicle invari-ably present on stigmas of the dry type (Mattsson et al., 1974). In the latter case, reference toother species or genera of the same family will, nevertheless, often indicate which categoryis appropriate.

Classification of genera and families of monocotyledons and dicotyledons according tostigma type

Tables 2A and B list the genera in each family of the monocotyledons and dicotyledonsinvestigated, classified according to the criteria of Table 1. Tables 3A and 3B provide abreakdown of the families, listed alphabetically, showing the numbers of genera and speciesstudied and their allocation to each stigma-type category.

INTERPRETATION AND DISCUSSION

Consistency of stigma type within taxa

In both monocotyledons and dicotyledons stigma type proves to be remarkably consistentat specific and generic levels, and even at family level there can be a high degree of unifor-mity. With experience, it is often possible to recognize and place any particular specieswithin its genus or family by reference exclusively to stigma features, a surprising outcomenot anticipated at the outset of the study.

Thus in the monocotyledons 30 genera of Iridaceae examined all possessed dry stigmaswith papillae of a disposition and shape quite characteristic of the family, and the same wastrue in the dicotyledons for 22 genera of Cruciferae. Families, e.g. the Gramineae andMalvaceae uniformly possessed dry papillate stigmas, although in these instances there wasgreater variation in papilla form. Among the wet-stigma types, all of the Orchidaceae andall of the Leguminosae examined showed common family characteristics. Such consistencyoften extended to Englerian orders, so that all 19 genera of the Zingiberales studied, be-longing to some 6 families, were wet, as were 3 three families of the Ericales, comprising 21genera of Ericaceae, 2 of Epacridaceae and 2 of Pyrolaceae.

Apparent inconsistencies

Notwithstanding the good correlations often found between stigma type and taxonomicposition, many noteworthy inconsistencies were also encountered. Thus several familiesproved to be heterogeneous, having some genera with wet stigmas and some with dry.Striking examples of this were the Liliaceae, Amaryllidaceae, Onagraceae and Rosaceae.

Examples of inconsistency within genera were also met, notable instances being Mag-nolia, Fuchsia, Viburnum, Viola and Saxifraga. In the case of Magnolia, usually accepted asa relatively primitive genus, the receptive surface consists of the infolded margins of thecarpel wall, there being no clear distinction between 'style' and 'stigma'. The receptivesurface is roughened by small proliferations, forming in effect multicellular, multiseriatepapillae [Group HB «(b) in the classification of Table 1]. The papillae bear a true pelliclewith dispersed esterase activity, but there is no fluid secretion. Five of the species examinedbore papillae of this type, but in one, M. g/-a/u#/?ora, unicellular [Group HBO)] papillae werepresent towards the summit of the carpel, suggesting the beginning of specialization andindicating how a trend towards the simpler type of papilla might be initiated.

In the genus Fuchsia it was found that five species had 'wet' stigmas, and all early indi-cations were that this type would characterize the genus. However, a later sample of F.thymifolia HBK subsp. minimiflora (Hemsley) Breedlove appeared to have dry stigmas.According to Dr P. R. Raven the species is gynodioecious, but the apparently bisexualflowers of some individuals are functionally staminate and never bear fruit. It seems that in

44


the plants examined the stigma was non-functional, and that female sterility was probablydue to the lack of secretion. In another gynodioecious Fuchsia species, F. encliandra Steudelsubsp. encliandra, the functional female flowers were indeed found to have wet stigmasconforming to the usual type found in the genus. It seems possible that female sterility mayarise in a somewhat similar way in Viola and Viburnum. Most of the species of these generaexamined had wet stigmas, but some of the clonally propagated and probably female-sterile cultivars had dry stigma surfaces.

In another example of intergeneric heterogeneity, no such explanation is readily to hand.Fourteen species of Saxifraga were found to have dry papillate (Group IIB) stigmas, butS. pennsylvanicvm proved to have wet papillate (Group III) stigmas. However, the familySaxifragaceae as a whole is of a mixed stigma type; three genera studied had unequivocaldry papillate stigmas and six wet papillate.

Heterostyly presents a special case because of the variation in stigma character withinspecies associated with the specialized breeding system. Heterostylic species in the familiesLythraceae, Linaceae, Plumbaginaceae and Primulaceae were found to show distinctionsof stigma surface with the different morphs sometimes sufficiently unlike as to be classifi-able in adjacent subcategories. Thus in Armeria andLimonium both types of stigma are dry,but one has no more than a bullate surface (Group IIA), while the other bears distinct uni-cellular papillae [Group IIB (/)]. Instances of families with heterostylous species have beenmarked in Tables 2 and 3 by asterisks.

No doubt further inconsistencies within genera could be found were the study to beextended, but in actuality those encountered in the survey so far serve mainly to emphasizethe remarkable consistency of stigma surface type as a generic characteristic since mostexceptions are so obviously related to special situations.

Some taxonomic andphylogenetic implications

Among the monocotyledons, the Zingiberales form a relatively unified group in respectto stigma type, as also do the families Iridaceae, Typhaceae, Juncaceae and Cyperaceae. Incontrast, certain families, notably the Liliaceae and Amaryllidaceae, are heterogeneous,with genera of each type. Further subdivision of the Liliaceae does not clarify the situation,for the genera within the Alliaceae are mixed, as is also true for those retained in theLiliaceae. Perhaps the diversity is related to the primitive status usually accorded to thisimportant nexus.

Among the dicotyledons various interesting regularities emerge. A few examples are asfollows.

(1) The genus Paeonia, at one time placed in the Ranunculaceae, is distinguished from allother 19 genera of the family examined in having species with a wet stigma surface. Paeoniais now accepted as being distinctive enough in several floral and vegetative features to meritsegregation in a separate family, Paeoniaceae, as originally suggested by Worsdell (1908).The Paeoniaceae are regarded by several authorities as having closer affinities with theDilleniaceae than with the Ranunculaceae (Corner, 1946; Nakai, 1949; Takhtajan, 1966;Cronquist, 1968), and strikingly enough the Dilleniaceae also have wet stigmas.

(2) The genus Nolana, at one time associated with the Convolvulaceae, is now usuallyplaced in the Nolanaceae, accepted as having affinities with the Solanaceae. It shares thewet stigma character with the latter family, whereas all species of the seven other genera ofConvolvulaceae examined have dry stigmas.

(3) A further example is that of the Acanthaceae. Here 11 genera possess dry stigmas,many being non-papillate. However, four of the species of Thunbergia examined have wet,papillate (Group HI) stigmas. Thunbergia has been separated in a subfamily (Thome, 1968).or placed in a distinct family, Thunbergiaceae (Rouleau, 1970). The family may have some i


links with the Bignoniaceae (Willis, 1968), which is also characterized by having generawith wet stigmas.

(4) The ten genera of Papaveraceae (including Hypecoaceae) examined all possessed drystigmas, whereas the five genera of Fumariaceae were all wet, a correlation supporting theseparation of the latter family.

(5) Similarly the Lobeliaceae examined had wet stigmas whereas the Campanulaceaehave, characteristically, dry stigmas, again a correlation supporting a taxonomic sub-division.

(6) The genus Heliotropium stands rather apart from others placed in the Boraginaceae,and has been placed in a subfamily, Heliotropideae, by Thome (1968). The distinction isseen in stigma character; Heliotropium is wet, papillate (Group III), while the other generaare dry, papillate (Group II).

(7) Within the Umbellales, Hegnauer (1971) reported chemical affinities between theUmbello-Aralian group and the Pittosporaceae, and it is interesting to note that theUmbelliferae, the Pittosporaceae and some genera of the Araliaceae also share the charac-teristic of having wet stigmas. Rodriguez (1971), in discussing the relationships of theUmbellales, describes them as a 'flabellate cluster of advanced taxa originating from acommon area near Escallonia, encompassing the Rhizophoraceae and relating in somedegree with the Rutaceae, Sapindaceae, Caprifoliaceae, Pittosporaceae and Compositae.'In respect to the link with Escallonia, there is agreement in the possession of wet, non-papillate (Group IV) stigmas, and the character is found in Sapindaceae and Pitto-sporaceae. Caprifoliaceae are wet, papillate (Group TV); Rutaceae diverse, with both 'wet'and 'dry' genera, and Compositae all dry, mostly distinctly papillate. Rhizophoraceae havenot been examined.

Characteristics of the stigma have scarcely been accorded any significance in taxonomicandphylogenetic studies hitherto, but consideration of the regularities which haveemergedin the present work strongly suggests that they could well be added to the list of criteria tobe taken into account, much in the way that features of the pollen have in recent years.

Stigma type in relation to incompatibility system

In recent work on the physiology of self-incompatibility (SI) systems in flowering plantsrelationships between stigma characteristics and the type of mechanism involved have beennoted (J. Heslop-Harrison, 1975a; Heslop-Harrison, Heslop-Harrison and Barber, 1975)Thus the families known to have sporophytic self-incompatibility (SSI) systems belong tostigma Group IIB (i), dry papillate, the principal examples being the Cruciferae and Compo-sitae. Here the behaviour of the pollen is determined by the genotype of the pollen parent,and not by the genotype of each individual grain. On the other hand, in genera with game-tophytic self-incompatibility (GSI) systems, where pollen behaviour is determined by thegametophytic (haploid) genotype, the stigmas are usually of the wet type. Typical GSIgenera occur in the Solanaceae, Leguminosae, Liliaceae, Rosaceae and Onagraceae. Thecorrelation is broken in the Gramineae, where a GSI system functions with a dry (Group I)stigma.

Brewbaker (1957, 1967), in surveys of pollen cytology and self-incompatibility systems,pointed out certain correlations between characteristics of the pollen and pollen tube andthe prevailing SI system. In general, the pollen is binucleate in GSI plants, with the inhi-bition of the tube occurring in the style or even ovary in incompatible pollinations, whereasthe pollen of SSI plants is trinucleate, with the inhibition at or near the stigma surface inincompatible combinations. It is therefore of some interest to relate stigma type to pollencytology, and this is done in Tables 4A and B, where the families of the monocotyledonsand dicotyledons are grouped according to wetness or dryness of stigma and the bi- ortrinucleate condition of the mature pollen grain.


T A B L E 4. Relationship between pollen type, whether binucleate or trinucleate, and stigmatype, whether 'dry' or 'wet', for some families of the monocotyledons and dicotyledons.

Pollen data mainly from Brewbaker (1967)

A. MONOCOTYLEDONS

Pollen type

Binucleate

Bi- andtrinucleate

Trinucleate

Pollen type Stigma typeDry

Stigma typeDry

FlagellariaceacHypoxidaceaeIridaceaePalmaePontederiaceaeSparganiaceaeTaccaceaeTyphaceae

(8 families)

Cyperaceae

(1 family)

AlismataceaeAponogetonaceaeButomaceaeEriocaulaceaeGramineaeHydrocharitaceaeJuncaceaeNaiadaceae s.l.PotamogetonaceaeScheuzeriaceae

(10 families)

Wet and dry

AgavaceaeAmaryllidaceaeCommelinaceaeLiliaceae

(4 families)

AraceaeBromeliaceae

(2 families)

B. DICOTYLEDONS

Wet

CannaceaeCyclanthaceaeDioscoreaceaeMarantaceaeMusaccaeOrchidaceaeZingiberaceae

(7 families)

Wet and dry Wet

Binucleate AceraceaeActinidiaceaeBegoniaceaeBctulaceacBombacaceaeBuxaceaeCalycanthaceaeCapparidaceaeCistaceaeCornaceaeCunoniaceaeDatiscaceaeEbenaceaeElaeagnaccaeElaeocarpaceaeEucryphiaceaeFagaceaeFlacourtiaceaeGarryaceaeGoodeniaceaeHamamel idaceaeHernandiaceaeHippocastanaceae

MenispermaceaeMonimiaceaeMoraceaeMyoporaceaeMyricaceaeMyrsinaceaeMyrtaceaeNepenthaceaeNymphaeaceaeOchnaceaeOrobanchaceaeOxalidaceaePapaveraceaePassifloraceaePiperaceaePlatanaceaePolemoniaceaePrimulaceaeProteaceaeRanunculaceaeResedaceaeRhamnaceaeSabiaceae

AristolochiaceaeBerberidaceaeCucurbitaceaeGesneriaceaeOnagraceaeRosaceaeSaxifragaceaeScrophulariaceaeSterculiaceae

AnacardiaceaeAnnonaceaeAquifoliaceaeBalsaminaceaeBignoniaceaeCombretaceaeCrassulaceaeCyrillaceaeDiapensiaceaeDilleniaceaeEpacridaceaeEricaceae1

FumariaceaeGuttiferaeLardizabalaceaeLeguminosaeNolanaceaePedaliaceaePunicaceaePyrolaceaeSapindaceaeSchisandraceaeSolanaceae2

Heslop-Harrison andShivanna—The Receptive Surface of the Angiosperm Stigma

TABLE A—continued

1253

Pollen type

Bi- andtrinucleate

Trinucleate

Stigma typeDry

Hydrophyllaceae SalicaceaeHypericaceae SarraceniaceaeUliciaceae SaururaceaeJuglandaceae SimaroubaceaeLauraceae StylidiaceaeLimnanthaceae StyracaceaeLoasaceae TiliaceaeLythraceae TrochodendraceaeMagnoliaceae TropaeolaceaeMalpighiaceae TurneraceaeMalvaceae UrticaceaeMarcgraviaceae Vitaceae

(70 families)

AcanthaceaeCelastraceaeConvolvulaceaeDroseraceaeEuphorbiaceaeHaloragaceaeLabiataeOleaceaePlantaginaceaePolygalaceaeSapotaceacUlmaceae

(12 families)

Adoxaceae GeraniaceaeAmaranthaceae LinaceaeBoraginaceae3 NyctaginaceaeCaryophyllaceae PhytolaccaceaeChenopodiaceae PlumbaginaceaeCompositae PolygonaceaeCruciferae PortulacaceaeDipsacaceae ThymeleaceaeErythroxylaceae ValerianaceaeFrankeniaceae

(19 families)

Wet and dry

(9 families)

ApocynaccaeAsclepiadaceaeCampanulaceaeMeliaceaeRubiaceaeRutaceaeZygophyllaceae

(7 families)

AizoaceaeAraliaceae

(2 families)

Wet

StachyuraceaeTamaricaceaeTheaccaeTheophrastaceaeThunbcrgiaceacViolaceaeWinteraceae

(30 families)

GentianaceaeLecythidaceaeLoganiaceaeStaphyleaceaeVerbenaceae

(5 families)

CactaceaeCaprifoliaceaeEscalloniaceaeLentibulariaceaeMelastomataceaePittosporaceaeUmbelliferae

(7 families)

1 Enkiantfws has trinucleate pollen.1 Solandra has a dry stigma.

Within the monocotyledons, three unequivocal conclusions can be drawn:(1) binucleate pollen occurs in association with both wet and dry stigmas;(2) all wet stigma forms have binucleate pollen;(3) all trinucleate forms have dry stigmas.For the dicotyledons, the trend is similar, but not so clear cut:(1) binucleate pollen occurs in association with both wet and dry stigmas, c. 67 per cent

having dry and c. 25 per cent wet, the remaining families having genera with each;(2) most wet stigma forms (61 per cent) have binucleate pollen, although 17 per cent

have trinucleate grains;(3) most trinucleate forms (68 per cent) have dry stigmas, although 27 per cent have wet.The relationship between SI system, where this is known, and pollen type, worked out by

Brewbaker (1957, 1967), is clear cut enough to allow extension to take in stigma charac-teristics using the data of Tables 4A and B. However, in addition one may now take into

1254 Heslop- Harrison and Shivama—The Receptive Surface of the Angiosperm Stigma

account work on the physiology of SI systems. In the Compositae and Cruciferae, theresponse is mediated by sporophytically-derived materials carried in the pollen wall(reviews, J. Heslop-Harrison, 1975i, c), and the interaction is with individual stigmapapillae. A system of this kind, involving cell-by-cell interaction with rejection responses onboth pollen and stigma sides, could obviously not be operated on a wet stigma particularlywhere the surface cells are necrotic, but could only function with a dry stigma where singlestigmatic cells tend to encounter single pollen grains, or at the most very small numbers(Heslop-Harrison, Heslop-Harrison and Barber, 1975). The adaptive significance of thepapillate form of the surface cells may also be surmised. Not only does this increase thecapturing area, a function already suggested for stigma hairs by earlier workers, but itreduces the opportunity for interaction by ensuring that pollen surface materials cannot bedistributed too freely on the stigma surface from individual grains or small clumps. In thecrucifers, a papilla is prevented from further function by encounter with the wall materialsfrom incompatible pollen (Dickinson and Lewis, 1973ft; Heslop-Harrison, Rnox andHeslop-Harrison, 1974), but the fact that the receptive zone of each is at the tip with the tipsheld apart helps to prevent the passage of materials from one to another and so conservesthe functional area of the stigma. Bearing these points in mind, one can pick out fromTable 4 other obvious dry-stigma, trinucleate candidates for families where an SSI systemmight operate.

Correspondingly, the families listed in the wet-stigma, binucleate category and certaingenera from binucleate-pollen families with mixed stigma types would be likely to haveGSI systems, if self-incompatibility exists in them at all. In most investigated GSI genera,the general rule is that both compatible and incompatible pollen germinates in the stigmasurface fluid, the rejection of incompatible gametophytes occurring in the passage throughthe style, and not on the stigma surface. Self-sterility has been reported in various species ofwet-stigma, binucleate-pollen families listed in Table 4 apart from those in which thegenetics of the SI system have been worked out, and it would seem a reasonable surmisethat in all such cases the system will prove to be a gametophytic one.

Notwithstanding the regularities that are apparent, several of the categories of Table 4remain enigmatic in respect to the relationship of pollen type, stigma type and SI system.Clearly the large group of dicotyledonous families with binucleate pollen and dry stigmaswould now well repay further genetical and physiological study. Several are known to havegenera with SI systems, and where these have been investigated genetically, they haveappeared to be of the gametophytic type, as for example in the Ranunculaceae (0sterbye,1975). Physiologically these must differ from the more fully investigated GSI genera withwet stigmas, and it is perhaps significant that the genetical control is of a complex typecomparable with that of the Gramineae, where inhibition of incompatible pollen occurs ator near the stigma surface which is dry (Group I). Similarly, in the Papaveraceae the recentwork of Lawrence (1975) strongly suggests gametophytic control; here there seems nodoubt that the inhibition of incompatible grains occurs on the dry stigma surface as in SSIsystems.

Stigma type and pollen germination and tube growth in vitro

The listings of Tables 3 and 4 reveal a further correlation. It has long been known thatbinucleate pollen is more readily germinated in vitro than trinucleate, a fact commentedupon by Brewbaker in his pioneer study (1957). Generally speaking, liquid or semi-liquidmedia are used in pollen germination trials, and in these the grains of species with tri-nucleate pollen either fail to germinate or burst prematurely, depending on tonicity. Table4 shows that trinucleate species tend to have dry stigmas and binucleate often have wet.Binucleate pollen of wet-stigma types is presumably adapted for germination in a liquidmedium, while trinucleate pollen is commonly adapted for germination on 'dry' stigma


surfaces where hydration is slow and controlled. To promote its germination, the situationencountered on the stigma surface has to be simulated (Bar Shalom and Mattsson, in press).

It seems, then, that the correlation between pollen cytology and capacity for germinationin vitro on liquid or semi-liquid media is a secondary one, the primary factor being the typeof stigma. One might expect all species with dry stigmas to require more specialized con-ditions for pollen germination than those with wet.

Conspectus

Some of the implications of this investigation of stigma types in the angiosperms havebeen brought out in the foregoing paragraphs, but much more remains to be done, both inextending and refining the survey itself and in tracing the significance of the various regu-larities that have emerged. Papilla form, size and distribution constitute topics of interest intheir own right, particularly when considered in relation to pollen size and exine sculp-turing. Fine structural studies of various types of stigma surface cells have shown intriguingspecial adaptations, notably in characteristics of the cuticle (see, for example, Heslop-Harrison and Heslop-Harrison, 1975). Comparative work on stigmatic surfaces as secre-tory systems has only recently begun, and much is yet to be found out about the compo-sition of the surface exudates of wet stigmas (Martin, 1969,1970) and their functions in theregulation of pollen germination.

In respect to the biology of the angiosperms as a whole, the findings so far lend weight tothe view that the development and refinement of the siphonogamous system of fertiliz-ation and the pollen-stigma interactions which it involves have been vitally importantparts of flowering-plant evolution, governing fundamental aspects of the breeding systemand so affecting the capacity for variation and adaptation within the group as a whole.

We propose to take up these topics in further publications.

ACKNOWLEDGEMENTS

It is a pleasure to thank the Curator of the Royal Botanic Gardens, Kew, and his staff forcollaboration in the supply of the very large quantity of living material used in this investi-gation; nowhere else in the world could such a study have been made with so comprehen-sive a cover of well-grown living plants. We are particularly grateful to Mr Dickin Bowling,for his assistance in collecting the material and making many of the preparations.

We wish also to thank many colleagues who have given information and advice relatingto particular groups, including especially Dr P. R. Raven, Dr R. M. Pettitt and ProfessorR. B. Knox.

It was our privilege to discuss some of the phylogenetic implications of the work withAcademician A. Takhtajan, and we thank him for his enthusiastic interest.

KRS wishes to thank the British Council for a fellowship award which made possible hisstay at the Royal Botanic Gardens, Kew, during 1974/75.

LITERATURE CITED

AMIO, M., 1824. Observations microscopiques sur diverses especes de plantes. Article 3, du pollen. Ann.Sd. Nat. 2, 65-70.

BAR SHALOM, D. and MATTSSON, O., 1977. The mode of hydration as an important factor in germination oftrinucleate pollen grains. (In press).

BREWBAKER, J. L., 1957. Pollen cytology and self incompatibility systems in plants. / . Hered. 48, 271-7.1967. The distribution and phylogenetic significance of binucleate and trinucleate pollen grains in the

Angiosperms. Am. J. Bot. 54,1069-83.BURCK.W., 1902. Over de prickelbare stempels van ToreniaenMimulusluteuseaover voorbehoedmiddelen

tegen het kiemen van vreemd stuifmeel op de stempel. Versl. gewone Vergad. wis-en natuurk Afd. K.Akad. Wet. Amst. 10, 209-19.

CAPUS, M. G., 1878. Anatomic du tissu conducteur. Ann. Sd. Nat. 7, 207-91.


CHRIST, B., 1959. EntwickJungsgeschichtliche^und physiologische untersuchungen tiber die sclbs-sterilitatvon Cardamine pratensis L. Z. Bot. 47, 88-112.

CORNER, E. J. H., 1946. Centrifugal stamens. J. Arnold Arboretum 11, 423-37.CRONQUIST, A., 1968. The Evolution and Classification of Flowering Plants, Houghton Mifflin, Boston.DASHEK, W. V., THOMAS, H. R. and ROSEN, W., 1971. Secretory cells of lily pistils n . Electron microscope

cytochemistry of canal cells. Am. J. Bot. 58,909-20.DICKINSON, H. G. and LAWSON, J., 1975. Pollen tube growth on the stigma ofOenotheraorganensisfoUov/ing

compatible and incompatible intraspecific pollinations. Proc. R. Soc. Lond. B 188, 327-44.and LEWIS, D., 1973a. Cytochemical and ultrastructural differences between intraspecific compatibleand incompatible pollinations in Raphanus. Ibid. B 183, 21-38.

19736. The formation of the tryphine coating the pollen grains of Raphanus, and its propertiesrelating to the self incompatibility system. Ibid. 184,149-65.

DULBERGER, R., 1974. Structural dimorphism of stigmatic papillae in distylous Linum spp. Am. J. Bot. 61,238-43.1975. Intermorph structural differences between stigmatic papillae and pollen grains in relation to

incompatibility in Plumbaginaceae. Proc. R. Soc. Lond. B 188, 233-375.GUEOUEN, M. F., 1900. Recherches sur le tissu collecteur ct conducteur des phanerogames, Monocotyle-

dones, Dicotyledones, Apetales et Gamopetales. / . Bot. Paris 14, 140-8; 165-72.1901a. Anatomie comparfe du tissu conducteur du style et du stigmate des phandrogames. Mono-

cotyledones, Apetales et Gamopetales. L Introduction. Ibid. 15, 265-70.19016. n . Tissu conducteur des Monocotyledoncs. Ibid. 15, 271-300.1902a. HI. Tissu conducteur des Apetales. Ibid. 16,15-30.19026. IV. Tissu conducteur des Gamopetales. Ibid. 16,48-65; 138-^4; 167-80; 280-6; 300-13.

HARTIG, T., 1842. New Theory of the Fertilisation of Plants. Brunswick.HEGNAUER, R., 1971. Chemical patterns and relationships of Umbelliferae. In The Biology and Chemistry of

the Umbelliferae, ed. V. H. Heywood. Suppl. 1 Bot. J. Linn. Soc. 64, 267-77.HESLOP-HARRISON, J., 1975a. Male gametophyte selection and the pollen-stigma interaction. In Gamete

Competition in Plants andAnimals, ed. D. L. Mulcahy, pp. 177-190. NorthHolland Publ. Co., Amster-dam,19756. Incompatibility and the pollen-stigma interaction. A. Rev. Pi. Physiol. 26,403-25.1975c. The physiology of the incompatibility reaction in the Cruciferae. Report of the Eucarpia

Conference on the Cruciferae, Invergowrie, pp. 14-9.1976. Amos Memorial lecture. A new look at pollination. Rep. E. Mailing Res. Stnfor 1975,141-57.and HESLOP-HARRISON, Y., 1975. Fine structure of the stigmatic papillae of Crocus. Micron 6,45-52.

and BARBER, J., 1975. The stigma surface in incompatibility responses. Proc. R. Soc. Lond. B188, 287-97., KNOX, R. B. and HESLOP-HARRISON, Y., 1974. Pollen-wall proteins: exine-held fractions associatedwith the incompatibility response in Cruciferae. Theoret. appl. Genet. 44,133-7.

and MATTSSON, O., 1975. Pollen-wall proteins: emission and role in the incompatibilityresponse. In The Biology of the Male Gamete, ed. J. G. Duckett and P. A. Racey. Suppl. 1, Biol. J. Linn.Soc. 7,189-202.

HESLOP-HARRISON, Y., 1970. Scanning electron microscopy of fresh leaves ofPinguicula. Science N. Y. 167,

1977. The pollen-stigma interaction: pollen tube penetration in Crocus. Ann. Bot. 4, 913—22.KONAR, R. N. and LJNSKENS, H. F., 1966. The morphology and anatomy of the stigma of Petunia hybrida.

Planta 71, 356-71.KROH, M., 1964. An electron microscopic study of the behaviour of Cruciferous pollen after pollination. In

Pollen Physiology and Fertilisation: Symposium at U. of Nijmegen, Netherlands, ed. H. F. Linskens.pp. 221-4. North Holland Publ. Co., Amsterdam.

LAWRENCE, M. J., 1975. The genetics of self-incompatibility in Papaver rhoeas. Proc. Lond. B 188, 275-85.MARTIN, F. W., 1969. Extracts of the stigma often species. Am. J. Bot. 56,1023-7.

1970. The ultra-violet absorption profile of stigmatic extracts. New Phytol. 69, 425-30.MATTSSON, O., KNOX, R. B., HESLOP-HARRISON, J. and HESLOP-HARRISON, Y., 1974. Protein pellicle of

stigmatic papillae as a probable recognition site in incompatibility reactions. Nature, Lond. 247, 298-300.

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0STERBYE, U., 1975. Self incompatibility in Ranunculus acris L. I. Genetic interpretation and evolutionaryaspects. Hereditas 80, 91-112.

PEARSE, A. G. E., 1972. Histochemistry, Theoretical and Applied, Vol. 2,3rd edn. ChurchilJ, Edinburgh andLondon.

PEITIIT, J. M., 1976. Pollen wall and stigma surface in the marine angiosperms Thalassia and Thalassoden-dron. Micron 7, 21-32.


RASPAIL, M., 1824. Essai d'une classification generate des Graminees, fondee sur l'etude physiologiquedes characteres de cette famille Ann. Sd. Nat. 5,287-311; 433-60.

RODRIGUEZ, R. L., 1971. The relationships of the Umbcllales. In The Biology and Chemistry of the Umbelli-ferae, ed. V. H. Heywood. Suppl. 1, Bot. J. Linn. Soc. 64, 63-91.

ROSEN, W. G., 1964. Chemotropism and fine structure of pollen tubes. In Pollen Physiology and Fertilisa-tion: Symposium at U. of Nijmegen, ed. H. F. Linskens. pp. 159-66. NorthHollandPubl.Co., Amster-dam.and THOMAS, H. R., 1970. Secretory cells of lily pistils I. Fine structure and function. Am. J. Bot. 57,1108-14.

ROULEAU, E., 1970. Guide to Index Kewensisandits Supplements i-xiv. Bibl. Nationale du Quebec, Montreal.TAKHTAJAN, A., 1969. Flowering Plants: Origin and Dispersal. Oliver and Boyd, Edinburgh.THORNE, R. F., 1968. Synopsis of a putatively phylogenetic classification of the flowering plants. Aliso 6,

57-66.VASIL, I. K. and JOHRI, M. M., 1964. The style, stigma and pollen-tube. Phytomorphology 14, 352-69.WELK, M., MILLINGTON, W. F. and ROSEN, W. G., 1965. Chemotropic activity and the pathway of the

pollen tube in lily. Am. J. Bot. 52, 774-81.Wnxis, J. C , 1968. A Dictionary of the Flowering Plants and Ferns. 8th edn., revised by H. K. Airy Shaw.

Cambridge University Press, London.WORSDELL, W. C , 1908. The affinities oiPaeonia. J. Bot. Lend. 46,114-6.

EXPLANATION OF PLATES

Scanning electron micrographs of fresh, uncoated stigmas of characteristic types belonging to the variouscategories of Table 1.

PLATE 1A, B. Group I. Dactylis glomerata L. (Gramineae). A, Portion of one stigma arm, showing the evenly

arranged multicellular, multiseriate branches, any part of which can receive pollen, x c. 250. B, Detail,showing the out-turned cell tips of the stigma branches; in some grasses these are pointed, providinglodging places for the pollen, x c. 1000.

c, D. Group IIA. Euphorbia sanguinea Hort. (Euphorbiaceae). c, One branch viewed from above; openpollinated. Several grains have become hydrated and have produced pollen tubes which can be seenpenetrating the surface. Others have not yet hydrated, and may be incompatible. The stigma surface isdry and non-papillate, x c. 110. D. Detail, showing the smooth, shining stigma surface. Patches oflipidic material are present, but no fluid secretion comparable with that of the Group IV stigma ofPlate 4F and o. x c. 450.

PLATE 2

Examples of dry, unicellular-papillate stigmas of Group HB /.A. Iberis semperflorens L. (Cruciferae). Stigma viewed from above; style towards the lower left. The

papillae are relatively short, x c. 205.B. Matthiola incana R.Br. (Cruciferae). Part of the stigma surface, showing the elongated, clavate

papillae, x c. 315.c. Hibiscus rosa-sinensis L. (Malvaceae). Oblique view of part of one stigmatic head, showing the subu-

late papillae typical of many species in this family, x c. 250.D. Schizostylis coccineus Backh. and Harv. (Iridaceae). Oblique view of surface, showing the digitiform

papillae characteristic of many species in this family. Most of the attached pollen grains have becomehydrated. x c. 540.

PLATE 3

Examples of stigmas with multicellular papillae.A. Lopezia cornuta Wats. (Onagraceae). Oblique view of stigma surface. The multicellular, uniseriate

papillae are 2-4 cells in length. This stigma is classed as Group in , because the bases of the papillae areinundated with a foamy secretion. It is, however, transitional to the Group HB /'(a) stigma of Epilo-bium of the same family, also with multicellular, uniseriate papillae, x c. 450.

B. Lopezia cornuta Wats. Detail showing one papilla. A few lipid droplets are present on the surface,x c. 1250.

c, D. Rosa pendulina L. (Rosaceae). c. Stigmatic head, surrounded by receptacular hairs, viewed fromabove. The cleft in the stigma, continuous with the stylar cleft, may be seen. The papillae are multi-cellular, multiseriate, dry (Group IIB //(b)). x c. 155. D. Detail, showing the stylar cleft, and thenumerous multicellular, multiseriate papillae. Papillae of a closely similar type are found in Magnoliaand various other genera of primitive families, x c. 470.


PLATE 4

Examples of wet stigmas of Groups m and IV.A-C. Lonicerapeiiclymenum L. (Caprifoliaceae). Sequence showing progressive accumulation of secretion

fluid as the stigma matures (Group TB). When the flower first opens, the surface is dry, with the uni-cellular, short papillae clearly visible (A). AS the stigma approaches the receptive state, the secretionfluid begins to accumulate between the papillae (B); eventually, only the tips are visible (c). Partlyinundated pollen grains are seen in c. x c. 250.

D, E. Calluna vulgaris Salisb. (Ericaceae). In this mature stigma (Group III) the thick secretion covers thewhole head. In E, the secretion has withdrawn a little at the margin, revealing some of the shortpapillae, D, X C. 260; E, X C. 650.

F, o. Heracleum mantegazzianum Sommier and Lev. (Umbelliferae). The stigma is non-papillate (GroupTV), but the secretion is very copious and free-running, a characteristic of the Umbelliferae. Capturedpollen grains are rapidly submerged, including those of foreign species. This open-pollinated stigmahas received grains of Compositae growing in the neighbourhood, and some of these are seen in o,almost totally inundated. Compare with the superficially similar Group DA stigma of Euphorbiaillustrated in Plate ID. F, X C. 325; o, x c. 675.

HESLOP-HARRISON and SHIVANNA—The Receptive Surface of the Angiosperm Stigma

PLATE l

Ann. Bot. 41, 1233-1258, 1977 (facing page 1258)

H E S L O P - H A R R I S O N and SHI v ANNA—The Receptive Surface of the Angiosperm Stigma

PLATE 2

Ann. Bot. 41, 1233-1258, 1977

HESLOP-HARRISON and SHI VANNA—The Receptive Surface of the Angiosperm Stigma

PLATE 3

Ann. Bot. 41, 1233-1258, 1977

HESLOP-HARRISON and SHIVANNA—The Receptive Surface of the Angiosperm Stigma

PLATE 4Ann. Boi. 41, 1233-1258, 1977

Documents

The receptive surface of the angiosperm stigma · 1234 Heslop-Harrison and Shivanna—The Receptive Surface of the Angiosperm Stigma A major comparative study of the stigma surface