Endress, P K (2008). Perianth biology in the basal grade of extant angiosperms. International Journal of Sciences, 169(7):844-862. Postprint available at: http://www.zora.uzh.ch University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich. Zurich Open Repository and Archive http://www.zora.uzh.ch Originally published at: International Journal of Plant Sciences 2008, 169(7):844-862.

Winterthurerstr. 190 CH-8057 Zurich http://www.zora.uzh.ch

Year: 2008

Perianth biology in the basal grade of extant angiosperms

Endress, P K

Endress, P K (2008). Perianth biology in the basal grade of extant angiosperms. International Journal of Plant Sciences, 169(7):844-862. Postprint available at: http://www.zora.uzh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch

Originally published at: International Journal of Plant Sciences 2008, 169(7):844-862. Perianth biology in the basal grade of extant angiosperms

Abstract

Perianth structure and behavior were studied comparatively in representatives of all families of the basalmost extant angiosperms (ANITA grade plus Chloranthaceae). In addition, data from the literature were reviewed. Tepal aestivation is spiral imbricate in Amborella and , with broadly overlapping flanks; aestivation is mainly contort within each of the two tepal whorls in Cabomba (but open within each whorl and imbricate only between whorls in Brasenia) and is whorled imbricate in Nymphaeaceae. Tepals are absent in Hydatellaceae, Chloranthaceae (other than Hedyosmum), and Ceratophyllaceae. In two genera of Nymphaeales (Cabomba and Nuphar), nectaries are present on inner tepals. Tepals are caducous during or at the end of anthesis in Austrobaileyales. Preformations of the tepal abscission zone in flowers with caducous tepals include a narrow tepal base, constriction as seen in median longitudinal sections, and small‐celled tissue. In contrast, the perianth organs of Amborella, Nymphaeales, and Chloranthaceae are not caducous and are associated with a broad tepal base without indentation and often without small‐celled tissue. Only in the latter groups are there genera with basally united tepals (Amborella, Cabomba, and Hedyosmum). Int. J. Plant Sci. 169(7):844–862. 2008. Ó 2008 by The University of Chicago. All rights reserved. 1058-5893/2008/16907-0003$15.00 DOI: 10.1086/589691

PERIANTH BIOLOGY IN THE BASAL GRADE OF EXTANT ANGIOSPERMS

Peter K. Endress1

Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland

Perianth structure and behavior were studied comparatively in representatives of all families of the basalmost extant angiosperms (ANITA grade plus Chloranthaceae). In addition, data from the literature were reviewed. Tepal aestivation is spiral imbricate in Amborella and Austrobaileyales, with broadly overlapping flanks; aestivation is mainly contort within each of the two tepal whorls in Cabomba (but open within each whorl and imbricate only between whorls in Brasenia) and is whorled imbricate in Nymphaeaceae. Tepals are absent in Hydatellaceae, Chloranthaceae (other than Hedyosmum), and Ceratophyllaceae. In two genera of Nymphaeales (Cabomba and Nuphar), nectaries are present on inner tepals. Tepals are caducous during or at the end of anthesis in Austrobaileyales. Preformations of the tepal abscission zone in flowers with caducous tepals include a narrow tepal base, constriction as seen in median longitudinal sections, and small-celled tissue. In contrast, the perianth organs of Amborella, Nymphaeales, and Chloranthaceae are not caducous and are associated with a broad tepal base without indentation and often without small-celled tissue. Only in the latter groups are there genera with basally united tepals (Amborella, Cabomba, and Hedyosmum).

Keywords: Amborellaceae, Austrobaileyales, basal angiosperms, Chloranthaceae, Nymphaeales, perianth.

Introduction female flowers of Hedyosmum have a perianth. In Ceratophyl- laceae, a perianth is lacking if the whorl of phyllomes around The basal grade of extant angiosperms, the ANITA grade a female or male flower is not regarded as a perianth (discus- (Qiu et al. 1999), consists of Amborella, Nymphaeales, and sion in Endress 1994b); furthermore, it is not clear whether Austrobaileyales. In some phylogenetic analyses, Chlorantha- the male flowers are real flowers or rather inflorescences with ceae and Ceratophyllum immediately follow the ANITA grade unistaminate flowers (Endress 2004)—in the latter case, a as the next step, still below the remainder of the angiosperms perianth would be missing anyway. (Doyle and Endress 2000; Qiu et al. 2005, 2006; Duvall et al. Perianth phyllotaxis is diverse (Endress and Doyle 2007): 2006; Mathews 2006; Endress and Doyle 2008). Although the spiral in Amborella (Endress and Igersheim 2000) and Austro- position of Chloranthaceae and Ceratophyllum is not yet set- baileyales (Endress 1980b, 1983, 2001; Endress and Sampson tled (for other positions, see Jansen et al. 2007; Moore et al. 1983; Tucker and Bourland 1994) and largely whorled in 2007), I also include them in this study. Nymphaeales (Endress 2001; Schneider et al. 2003). Diverse The perianth is a basic part of the flowers of the crown phyllotaxis patterns commonly appear to be functionally linked group of angiosperms (for which the name Angiospermae was with different aestivation patterns in angiosperms. However, proposed; Cantino et al. 2007) and may even be much older aestivation has been little studied in basalmost angiosperms. (Doyle 2008). The perianth in the basalmost extant angio- Therefore, aestivation and potential correlations with phyllo- sperms has diverse functions. It plays a role in the protection taxis are addressed here. of flower buds and, in some cases, also of fruits, often in opti- Perianth abscission, although a topic of much interest in cal attraction of anthetic flowers, exceptionally in nectar pro- horticulture with regard to the longevity of flowers (e.g., van duction. To what extent perianth organs, together with other Doorn 1997, 2001), has been little studied by plant systema- floral organs, are specifically involved in scent production and tists and morphologists interested in the diversity of angio- thermogenicity is largely unexplored (Thien et al. 2000; Yuan sperms. The perianth of flowers may fall off during or after et al. 2008). anthesis, it may stay and even grow further (especially green The flowers of all families of the ANITA grade have a peri- organs), or it may simply dry out or rot after anthesis without anth, except Hydatellaceae, a long-neglected family that has abscising. Interest in the process of abscission or dehiscence of been moved from the monocots to Nymphaeales as sister to organs in general in has also grown, especially with re- the remainder of the order (Saarela et al. 2007). The flowers gard to crop plants in agriculture (Addicott 1982; Roberts of Hydatellaceae are minute and extremely simple (Hamann et al. 2000, 2002; Leslie et al. 2007), with a focus on fruit 1975, 1976; Rudall et al. 2007), and anthesis is, at least in dehiscence in the model plant Arabidopsis (Gu et al. 1998; part, underwater (Edgar 1966). In Chloranthaceae, only the Liljegren et al. 2000; Rajani and Sundaresan 2001; Child et al. 2003; Dinneny and Yanofsky 2005; Dinneny et al. 2005). 1 E-mail: [email protected]. However, in these works, floral organ abscission has been Manuscript received November 2007; revised manuscript received February tackled less extensively than fruit abscission (Li et al. 2006) or 2008. dehiscence (Stenvik et al. 2006). Some of the basalmost angio-

844 ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 845 sperm families are characterized by caducous perianth organs Austrobaileyaceae (Endress 2004). The genus Piptocalyx (Trimeniaceae) even owes Austrobaileya scandens C.T. White; PKE 4218, Boonjee, its name to this behavior (‘‘falling calyx’’). In other groups, Northern Queensland, Australia (fig. 4A); PKE 4265, Boon- tepals are persistent even in fruit. Thus, presence or absence of jee, Northern Queensland, Australia (figs. 1F,2D; fig. 8A, early or late perianth organ abscission will be explored, studying 8B); raised from seed of PKE 9083, Mt. Lewis, Northern morphology and histology of the tepal base, especially the site Queensland, Australia, BGZ (fig. 5F–5K). where the tepal abscises from the floral base. In basal angiosperms, nectaries, if present, are on perianth organs (Nymphaeales and Magnoliales) or on stamens and Trimeniaceae staminodes (Laurales). In the basalmost extant angiosperms, Piptocalyx moorei Oliv.; PKE 4005, New South Wales, floral nectaries are known from only two genera of Nym- Australia (figs. 4C,8F–8H); PKE 4367, New South Wales, phaeales (Cabomba and Nuphar; Bernardello 2007). They are Australia (fig. 5L–5N). located on perianth organs. However, they were found to be Trimenia neocaledonica Baker f.; PKE 6316, New Caledo- different histologically and were therefore interpreted as non- nia (fig. 5O). homologous (Vogel 1998). More comparative studies are nec- Trimenia papuana Ridl.; PKE 4066, Papua New Guinea essary. (figs. 2E,8C–8E); John S. Womersley s.n., September 1970 A long-standing question is whether outer sepaloid organs (received by F. Bruce Sampson; fig. 4B). and inner petaloid organs in basalmost (and also in other basal) angiosperms are homologous with sepals and petals in eudicots. This question will not be addressed here in any detail. The neu- tral term ‘‘tepals’’ will be used for all perianth organs. This japonica Benth.; PKE s.n., BGZ (figs. 1G,4E); article integrates new results and current knowledge on the PKE 4530, BGZ (fig. 2F). perianth structure and behavior of basalmost angiosperms. chinensis Baill.; PKE 99-29, BGZ (fig. 8I–8K); PKE 99-32, BGZ (fig. 4D). Schisandra grandiflora Hook.f. & Thomson; male flowers, PKE 7331, BGZ (not figured). Material and Methods Illiciaceae The following species and collections were studied (abbre- viations: BGZ ¼ cultivated, Botanical Garden of the Univer- Illicium anisatum L.; PKE, s.n., cultivated, Isole di Brissago, sity of Zurich; PKE ¼ collected by Peter K. Endress). Switzerland (fig. 1H); PKE 930, cultivated, Isole di Brissago, Switzerland (figs. 2G,4F,8L–8N). Amborellaceae Chloranthaceae Amborella trichopoda Baill.; male flowers, Hugh S. McKee 38907, New Caledonia (figs. 1A,2A,3A,5C; fig. 7A,7B); Hedyosmum bonplandianum Humb., Bonpl. & Kunth; PKE female flowers, Hugh S. McKee 38909, New Caledonia (figs. 97-103, Costa Rica (fig. 6A,6B). 3B,5D; fig. 7C,7D); male flowers, raised from seeds re- Hedyosmum costaricense W.C. Burger; PKE 97-106, Costa ceived from Hugh S. McKee, BGZ (fig. 5A,5B); female flow- Rica (fig. 6C). ers, cultivated, Santa Cruz Botanical Garden (received by Hedyosmum cf. racemosum (Ruı´z & Pav.) G. Don; female Hiroshi Tobe; fig. 5E). flowers, Ju¨ rg Scho¨ nenberger 482, Bolivia (fig. 4G).

Cabombaceae Flowering material, fixed in 70% ethanol or FAA, was used for LM and SEM studies. For serial microtome section- Brasenia schreberi J.F. Gmel.; Rolf Rutishauser, s.n., July ing, the material was embedded in Kulzer’s Technovit 7100 2001, Ontario, Canada (fig. 3D; fig. 7G,7H). (2-hydroxyethyl methacrylate) and sectioned at 5–10 mmwith Cabomba caroliniana A. Gray; PKE 9841, BGZ (fig. 7E, a Microm HM 355 rotary microtome and a standard micro- 7F; fig. 9B,9C); PKE s.n., cultivated, Botanic Garden, Uni- tome knife D. The sections were stained with ruthenium red versity of Basel (figs. 1C,9A); PKE 07-02, cultivated, Botanic and toluidine blue (both from Fluka) and mounted in Histo- Garden, University of Basel (fig. 2B); PKE 06-05, cultivated, mount. For SEM studies, specimens were treated with 2% os- Botanic Garden, University of Basel (figs. 3C,9D). mium tetroxide (Fluka), dehydrated in ethanol and acetone, Cabomba furcata Schult. & Schult. f.; PKE 00-58, culti- critical-point dried, sputter-coated with gold, and studied at vated, Zurich (commercial plants; fig. 1B). 20 kV with a Hitachi S-4000 scanning electron microscope.

Nymphaeaceae Euryale ferox Salisb.; PKE, s.n., BGZ (fig. 1D). Results and Comparative Analysis Nuphar advena Aiton; PKE 07-07, BGZ (fig. 9B,9C). Nuphar pumila (Timm) DC.; PKE 07-14, BGZ (figs. 3E,9D). Tepal Aestivation and Differential Size in Bud (Figs. 1–5) Nymphaea tetragona Georgi; PKE 96-45, BGZ (fig. 2C); Amborella. Tepal aestivation in bud is imbricate, following PKE 01-16, BGZ (fig. 7I,7J); PKE 07-31, BGZ (fig. 3F). a Fibonacci spiral phyllotaxis pattern. The overlapping parts Victoria cruziana A.D. Orb.; PKE, s.n., BGZ (fig. 1E). of the tepals are broad. The margins are two cell layers thick 846 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 1 Buds and flowers from the side or from below. A, Amborella trichopoda, male flower bud, from the side. B, Cabomba furcata, young floral bud from above, inner whorl of sepals delayed in development. C, Cabomba caroliniana, open flower, submerged floral bud and closed postanthetic flowers. D, Euryale ferox, opening flower from the side. E, Victoria cruziana, closed flower cut in half longitudinally. F, Austrobaileya scandens, open flower from below, showing gradual change in properties of tepals from outside to inside. G, Kadsura japonica, open flowers from the side, with outer tepals smaller than inner tepals. H, Illicium anisatum, open flowers from the side, with outer tepals smaller than inner tepals. Scale bars: A ¼ 0.5 mm, B ¼ 0.25 mm. for a short distance. The size of the tepals increases from the the outer whorl and the three tepals of the inner whorl have an outer to the inner ones. Thus, only the inner tepals are effi- open aestivation, but the tepals of the outer whorl partly cover cient protective organs in advanced buds (figs. 1A,2A,5B). those of the inner whorl; only the median parts of the tepals Nymphaeales. Tepal aestivation is imbricate based on a of the inner whorl remain uncovered (fig. 3D). All uncovered whorled phyllotaxis. The outermost organs are the largest in areas of the six tepals have a dense carpet of mucilage- bud and cover all the subsequent ones (fig. 1B–1E; fig. 2B, producing hairs, so the bud is completely surrounded by 2C). Among Cabombaceae, in Brasenia, the three tepals of mucilage (fig. 3D). In Cabomba, both whorls of tepals are ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 847

Fig. 2 Tepals from advanced floral buds, an outer and an inner one, from ventral side. A, Amborella trichopoda, male flower. B, Cabomba caroliniana. C, Nymphaea tetragona. D, Austrobaileya scandens. E, Trimenia papuana. F, Kadsura japonica. G, Illicium anisatum.Scalebar¼ 1cm. imbricate. They are either contort or with one organ inside other four. The outer four tepals can be interpreted as form- and one outside. A cover of hairs is present in young buds ing one whorl of four or two whorls of two tepals each but (fig. 1B) but later is no longer obvious (fig. 3C). However, with a unidirectional development. In the following, they this may also be different from species to species (Warner will be described as forming one whorl. et al. 2008). The tepals of the inner whorl are conspicuously Austrobaileyales. Tepal aestivation is imbricate, following delayed in bud (fig. 1B). Although the tepals are thin in both a Fibonacci spiral phyllotaxis pattern. The tepals have very genera, the flanks do not flare out into two-cell-layered mar- wide overlapping areas (figs. 1F,4A). They are not stuck to- gins. Among Nymphaeaceae, in Nymphaea, the outer four gether by their surfaces. The size of the tepals increases from tepals are imbricate, and in the region where they overlap, the outer to the inner ones. In Austrobaileya, the outermost they are postgenitally connected so that they provide a firmly ones are very small and bractlike (fig. 1F). The broad flanks closed envelope for the inner floral organs (fig. 3F). The of the inner ones are only two cell layers thick. In Trimenia, mechanism of coherence of the contiguous surfaces of neigh- the outermost tepals are bractlike (fig. 5L,5O) and are formed boring tepals is not by cellular or cuticular interdentation, pronouncedly earlier than the inner organs; they are smaller but they appear to be glued together by secretion. Also, the than the inner ones (fig. 4C). In Schisandraceae and Illiciaceae, surfaces of the subsequent four tepals are stuck to the outer the outer tepals are also smaller than the inner ones. In both four to some degree. In Nuphar, the flanks of the outer tepals families, the inner tepals may have thin margins (two cell layers are at least appressed to each other (fig. 3E). In Victoria (and thick). Thus, in Austrobaileyales, only the middle or the inner Nymphaea), at the time the perianth organs are initiated, the tepals are efficient protective organs in later floral bud stages. flower is more developed on the abaxial side than on the ad- Chloranthaceae.InHedyosmum female flowers, the three te- axial side and thus is somewhat incurved. Thus, the outer pals are small, and aestivation is more or less valvate (figs. 4G, (abaxial) tepal appears first and, as a result, later covers the 6A–6C). At the flanks, they are more than two cell layers thick. 848 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 3 Transverse sections of perianth in bud (Amborella, Nymphaeales). A, Amborella trichopoda, male flower. B, Amborella trichopoda, female flower. C, Cabomba caroliniana. D, Brasenia schreberi. E, Nuphar pumila. F, Nymphaea tetragona. Scale bars ¼ 0.5 mm.

Tepal Display at Anthesis (Figs. 1, 3, 5–7) the upper surface of the thin tepals is papillate (but not the lower). In Brasenia, instead of having a simple papillate epi- Amborella. The perianth is inconspicuous (whitish-cream). In male flowers, the nine to 11 tepals soon become reflexed dermis, the upper surface is covered with spherical (roundish) and are more or less covered by the spreading stamens so tricellular hairs. In Nymphaeaceae, the tepals are in several that they are not easily visible from above (fig. 5A–5C). In commonly tetramerous whorls (rarely trimerous or pentamer- female flowers, the seven or eight tepals are more exposed ous whorls; Conard 1905; Schneider et al. 2003); tepal num- because the carpels are more upright (and there are fewer ber of the inner whorls is increased by double positions carpels than there are stamens in the male flowers; fig. 5D, (Endress 2001) and is from four to eight in forms of Ondinea, 5E); the inner five tepals appear in series (Endress 2001). The up to more than 50 in Nymphaea, and more than 70 in Victo- upper surface of the inner tepals is irregularly papillate, and ria (Schneider and Williamson 1993). They are spreading (up- this layer is full of tannins in bud (fig. 7B,7D). right in Nuphar). The tepals of the outermost whorl are Nymphaeales. In Cabombaceae, there are two trimerous commonly green, and all other ones are white, yellow, pink, whorls (rarely dimerous in Cabomba) of spreading white, yel- red, blue, or purple. In bud, the outermost tepals cover all the low, or purple tepals, all six of similar size (fig. 1C). Histology inner ones. In Nuphar, the tepal areas exposed in bud are of the outer and inner tepals is similar (except for the nectarif- green, and the covered areas are yellow (Warner et al. 2008). erous area of the inner ones in Cabomba;fig.3C). In Cabomba, In some Hydatellaceae, at first sight, the reproductive organs ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 849

Fig. 4 Transverse sections of perianth in bud (Austrobaileyales, Chloranthaceae). A, Austrobaileya scandens. B, Trimenia papuana. C, Piptocalyx moorei. D, Schisandra chinensis, female flower. E, Kadsura japonica, male flower. F, Illicium anisatum. G, Hedyosmum cf. racemosum. Scale bars: A–F ¼ 0.5 mm, G ¼ 0.1 mm. look like flowers with a dimerous perianth in two whorls. inner ones (Endress and Sampson 1983). The inner tepals are However, these are inflorescences with four bracts; in some slightly papillate on the upper surface. Illiciaceae flowers have species, there is only one pair, or there are more than two pairs relatively large tepals of various shape, number (seven to 33), of bracts (Cooke 1987). A perianth is missing. The bracts and color (white, cream, pink, red, or purplish; Saunders cover the flowers in bud, although they grow to their full 1995; fig. 1H). The outer tepals are smaller than the inner length relatively late (Rudall et al. 2007). ones. In the inner tepals, the epidermis of the upper surface is Austrobaileyales. Austrobaileyaceae have the largest flow- papillate. In Schisandraceae, tepal number and shape vary ers of all families in the order (fig. 5F–5K). The 19–24 tepals somewhat less than in Illiciaceae. The five to 20 tepals are are greenish-yellowish, sometimes with brown spots. The out- commonly white, cream, or red (Saunders 1998, 2000, 2001; ermost organs are green, small, and decussate. They gradually fig. 1G). The outer tepals are smaller than the inner ones. change to colored and larger and spiral toward the inside The inner tepals have shallow papillae on both surfaces and (Endress 1980b; fig. 1F). The inner tepals have a papillate epi- the outer tepals slightly on the upper surface (Schisandra gran- dermis on both sides, with the papillae unexpectedly more diflora), or the inner tepals have papillae only on the upper developed on the lower surface; the outer tepals are not pa- surface (Kadsura japonica). In some species of Schisandraceae pillate. Trimeniaceae have very small flowers with an incon- and Illiciaceae, the small, outermost tepals are permanently spicuous perianth of two to 38 brownish tepals (Endress and green. Sampson 1983; fig. 5L,5O); the optically attractive organs Chloranthaceae. In the wind-pollinated Hedyosmum, the are mainly the stamens. The outer tepals are smaller than the minute tepals are green and inconspicuous (fig. 6A). Fig. 5 Process of anthesis (Amborella, Nymphaeales, Austrobaileyales). A–E, Amborella trichopoda. A, Male inflorescence. B, Male flower, early anthesis. C, Male flower, late anthesis. D, Female flower, from above. E, Female flower, from the side (one of the tepals removed). F–K, Austrobaileya scandens, flower at different stages through anthesis. F, Day 1: flower opening, female phase. G, Day 2: female phase. H, Day 5: male phase. I, Day 8: flower beginning to shatter. J, Day 10: perianth (except for outermost, bractlike tepals) and androecium fallen, view from above. K, Same stage, view from the side. L–O, Trimeniaceae. L–N, Piptocalyx moorei. L, Inflorescence at anthesis. M, Bisexual flower in female phase, tepals still present. N, Bisexual flower in beginning male phase, tepals fallen. O, Trimenia neocaledonica, open flower and floral buds. Scale bars ¼ 0.5 mm. ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 851

Fig. 6 Female structures of Hedyosmum (Chloranthaceae). A, Hedyosmum bonplandianum, female inflorescence. B, Hedyosmum bonplandianum, young fruit with persistent tepals. C, Hedyosmum costaricense, young fruit with persistent tepals. Scale bars ¼ 0.5 mm.

Behavior of the Tepals through Anthesis: Persistence Warner et al. [2008]). In Nuphar lutea, the flowers close at and Caducousness of Tepals (Figs. 5, 6) night (Heslop-Harrison 1955a); the tepals are persistent. In Nymphaea, there are day-flowering species, in which flow- Amborella. The tepals are basally united and tear apart ers close at night and during unfavorable weather (Heslop- when the flower opens. Anthesis takes 4–5 d in male flowers (Thien et al. 2003). Tepals do not abscise during anthesis or Harrison 1955b; Meeuse and Schneider 1980; P. K. Endress, at the end of anthesis. Male flowers fall off as a whole after personal observation). Some tropical Nymphaea species are anthesis (see also Thien et al. 2003). In female specimens, the night flowering, and they are open at night and closed during tepals may persist up to the fruiting stage, as found in herbar- the day during two to four consecutive days (Schmucker 1932; ium specimens (although Thien et al. [2003] state that they Prance and Anderson 1977). Tepals are more or less persis- abscise 1–2.8 d after anthesis). The perianth is inconspicu- tent and enclose the developing fruit (Heslop-Harrison 1955b; ous, and it simply dries out after anthesis. The tepals have a P. K. Endress, personal observation). Fruit ripening takes place broad base, and during anthesis, they successively recurve, so below water (Wood 1959), where tepals become entirely or they cannot be seen in their full extent when the flowers are partially putrescent, leaving transverse scars of attachment viewed from above (fig. 5A–5E). on the fruit walls when shed (Heslop-Harrison 1955b). The Nymphaeales. The perianth parts have a broad base. In same pattern of diversity, day flowering and night flowering, many species, they make movements during anthesis. They is also exhibited by the closely related Euryale and Victoria. open, close again, and reopen in a diurnal rhythm. At the Euryale flowers are open during the day and closed at night end of anthesis, they finally close (fig. 1C). Among Cabomba- over 2 d or, more often, are cleistogamous (Kadono and Schneider ceae, in Brasenia, the flowers last 2 d. They withdraw under- 1987). In Victoria, a flower emerges and opens in the evening water after the female phase to reappear the following and closes later on the same night during two consecutive morning when the pollen is shed, and finally, they are with- nights, and after anthesis, it becomes submerged again (Gessner drawn again (Tokura 1937; Osborn and Schneider 1988). In 1960; Valla and Cirino 1972; Prance and Arias 1975). In gen- Cabomba, all tepals are united at the base. The same imbri- eral, the fruits of most Nymphaeaceae appear to develop cation pattern they had in bud is attained again when the underwater, covered by the persistent perianth. There, the flower closes. In Cabomba caroliniana, the flowers last 2 d. perianth parts and stamens slowly rot. Exceptions are at least They close in the afternoon on both days (Schneider and some of the species of Nuphar, in which the fruits develop Jeter 1982). Closed flowers lie close beneath the surface of the above water and the perianth parts slowly become dry (Heslop- water, the bud being elevated 1–4 cm above the surface just Harrison 1955a). However, in Nuphar pumila, the flowers go before anthesis. Among Nymphaeaceae, Nuphar has mostly back underwater after anthesis (P. K. Endress, personal obser- five or six thick tepals (Nuphar polysepala nine to 12; Padg- vation). ett 2007). The area that was exposed in bud is green; the Austrobaileyales. In Austrobaileyaceae, the perianth or- area that was covered in bud is yellow (studied in detail by gans, stamens, and staminodes remain for the duration of 852 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 7 Longitudinal sections of floral buds of taxa with persistent tepals (Amborella, Nymphaeales). Yellow ellipses indicate basal area of tepals in close-up figures. A–D, Amborella trichopoda. A, Male bud. B, Close-up. C, Female bud. D, Close-up. E, F, Cabomba caroliniana. E, Bud. F, Close-up. G, H, Brasenia schreberi. G, Part of bud. H, Close-up. I, J, Nymphaea tetragona. I, Part of bud. J, Close-up. Scale bars: A, C, E, G, I ¼ 1 mm; B, D, F, H, J ¼ 0.2 mm. anthesis and then fall off. On days 1 and 2, the flower is in subsequent male phase (Bernhardt et al. 2003). Because the the female phase: the yellow gynoecium in the center is pre- tepals are present only in the floral buds and the female phase sented. Later, in the male phase, the gynoecium is covered by of anthesis and are absent in the male phase, their role in flo- the brown inner staminodes, and pollen is presented. On day ral attraction is lacking or minor. Tepals and stamens in SEM 10 (or earlier), perianth and androecium have fallen. However, micrographs of early anthetic flowers of Trimeniaceae typi- the smallest, outermost green tepals are persistent (fig. 5F–5K). cally appear overexposed because of charging as the abscis- The base of the tepals is very narrow, except for the persis- sion process has already started and the organs are only tent outermost tepals. Among Trimeniaceae, in Trimenia, the loosely attached at this stage (fig. 5M,5N). In contrast to perianth organs fall off when the flower opens or during an- Austrobaileya, the outermost organs also have a very narrow thesis (fig. 5L–5O). The stamens fall off right after anthesis. attachment region, and they fall off. In Illiciaceae and in the The attachment area of the tepals is narrow and thin. Thus, female flowers of Schisandraceae, the tepals fall off after an- anthetic flowers commonly do not retain their tepals (or at thesis, whereas male flowers of Schisandraceae fall off in their least not all of them). In Piptocalyx moorei, in bisexual flow- entirety. If the outermost tepals are very small (this is the case ers, the female phase lasts 3–5 d, and the tepals fall off in the in certain species of both families), they may also persist longer, ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 853 as in Austrobaileyaceae. The tepal base in both Schisandraceae appears to be released (fig. 9C,9D).Thehairsaremulticel- and Illiciaceae is also narrow. lular but have extremely short basal cells that look like a Chloranthaceae. Tepals are present only in female flowers stack of coins. This type of hair is common in Nymphaeales of Hedyosmum. They cover the large developing stigma in (Chifflot 1902) and other members of the ANITA grade (En- bud. They are basally united and form a short tube, which at dress 2001) and is very versatile in its position and function. anthesis surrounds the style or base of the stigma. After an- Such hairs are also present and prominently developed in the thesis, the stigma breaks off. The three tepals are persistent family Hydatellaceae (Hamann 1975; Rudall et al. 2007), (fig. 6B,6C; Endress 1971; Todzia 1988). The persistent flo- both in the vegetative region, where they can produce muci- ral bracts become fleshy and attractive for animal dispersal lage, and on carpels, where they function as stigmatic hairs (Todzia 1988). It is uncertain whether parts derived from the (Hamann 1975; Rudall et al. 2007). tepals may also have a similar function in some species (Endress In Nuphar, the nectaries are situated on inner tepals that 1973). In some fossil Early Cretaceous fruits of Hedyosmum, have sometimes been called ‘‘petals’’ (Hiepko 1965). These the three tepals are still present (Friis et al. 1994, 2000, 2006). organs are small, about the size of stamens, and spathulate. The nectaries form a dark yellow round area in the middle of Morphology and Histology of Tepal Base in Relation each organ on the dorsal side (fig. 9E,9F; Heslop-Harrison to Caducousness or Persistence (Figs. 7, 8) 1953). The organs are thick, and the mesophyll and epider- mis are rich in cytoplasm. The epidermis of the nectary con- Amborella. In Amborella, outer and inner tepals of both sists of tall cells, as in an epithelium. In contrast to that of male and female flowers do not have a specially differenti- Cabomba, the nectary is devoid of hairs but has conspicuous ated base. There is no basal indentation and no small-celled nectar pores (fig. 9G–9I). It would be interesting to know abscission tissue (fig. 7A–7D). whether nectar is produced only by the mesophyll and re- Nymphaeales. Cabombaceae and Nymphaeaceae studied leased through the nectar pores or whether it is also secreted here do not have any special morphological or histological by the epithelial epidermis. differentiation at the base of the tepals (fig. 7E–7J). There is no indentation and no especially small-celled tissue. Austrobaileyales. In Austrobaileyales, which all have ab- Discussion scising tepals, the situation is different. In Austrobaileya, the tepals have morphologically a medianly constricted base and Tepal Phyllotaxis histologically smaller-celled tissue. In the outermost tepals, Floral phyllotaxis in basalmost angiosperms was compara- which do not abscise after anthesis, this differentiation is not tively studied and discussed by Endress (2001) and Endress present (fig. 8A,8B). In Trimeniaceae, with their early cadu- and Doyle (2007). Here some additional aspects on tepal cous tepals, the differentiation of the tepal base is most con- phyllotaxis will be brought into the discussion. spicuous. The tepals have a long dorsal projection (‘‘spur’’), Tepal phyllotaxis in Amborella is spiral (Endress and Iger- and the abscission tissue is very small-celled. This dorsal spur sheim 2000; Endress 2001). Buzgo et al. (2004, p. 943) con- may expedite the abscission process, when the flower opens sider ‘‘the difference between spiral and whorled phyllotaxy and the tepals spread. The spur is more developed on the in Amborella to be gradual.’’ In all angiosperms, the spiral outer tepals than on the inner tepals (fig. 8C–8H). In Illicia- and whorled patterns are two distinct, clear-cut patterns. ceae, there is also a constriction of the tepal base, and the What is flexible, however, is that the two patterns can switch abscission tissue is also small-celled (fig. 8L–8N). In Schisan- between each other relatively easily in some clades (but not draceae, with its unisexual flowers, a constriction is present in Amborella, where floral phyllotaxis is always clearly spi- in female flowers (fig. 8I–8K). However, in male flowers of ral; Endress and Igersheim 2000). In Amborella, in a lateral K. japonica, a constriction is lacking. This is not surprising flower of an inflorescence (which is a botryoid or double bot- because the male flowers fall off as a whole after anthesis. ryoid, often with accessory flowers; Endress and Igersheim Chloranthaceae. In Chloranthaceae, in which only the fe- 2000; Posluszny and Tomlinson 2003), the first two organs male flowers of Hedyosmum have a perianth and the three are transverse and in normal prophyll position, and the fol- tepals are persistent in extant species, there is no articulation lowing organs adjust into a Fibonacci spiral. This is the most at the base of the tepals. A false impression of articulation common pattern in spiral angiosperm flowers and also in the may occur in paramedian sections, in which the area of the calyx of lateral pentamerous core eudicot flowers; in core eu- peculiar windows on the inferior ovary is sectioned (for an dicots flowers have a spiral onset in the calyx, but otherwise, analysis of the windows, see Endress 1971). they are whorled (e.g., Breindl 1934; Endress 1987b). Thus, Amborella behaves in no way differently from less ‘‘basal an- Presence of Nectaries on Tepals (Fig. 9) giosperms’’ in the phyllotaxis of the outermost floral organs. Among the ANITA grade, floral nectaries are known from In a terminal flower of a botryoid of Amborella, tepal phyllo- only two genera in Nymphaleales, Cabomba (Cabombaceae) taxis is spiral, beginning with the outermost perianth organs, and Nuphar (Nymphaeaceae). In Cabomba, the tepals of the which continue the spiral of the bracts on the inflorescence inner whorl differ from the outer ones in having nectaries on axis. a curved appendage on both sides of the base of the blade Phyllotaxis of perianth organs in Nymphaeales is basically (fig. 9A,9B). The nectariferous area is further conspicuous whorled (Endress 2001; Schneider et al. 2003). In Nuphar, the by its yellow coloration. The nectaries are formed by cytoplasm- onset of tepal initiation may be in a spiral sequence. However, rich mesophyll and special short hairs through which nectar if there are six tepals, the final position of the tepals, i.e., their Fig. 8 Longitudinal sections of floral buds with caducous tepals (Austrobaileyales). Yellow ellipses indicate basal area of tepals in close-up figures. A, B, Austrobaileya scandens. A, Part of bud. B, Close-up. C–E, Trimenia papuana. C, Bud. D, Close-up of outer tepal. E, Close-up of inner tepal. F–H, Piptocalyx moorei. F, Bud. G, Close-up of outer tepal. H, Close-up of inner tepal. I–K, Schisandra chinensis. I, Female bud. J, Close-up of outer tepal. K, Close-up of inner tepal. L–N, Illicium anisatum. L, Bud. M, Close-up of outer tepal. N, Close-up of inner tepal. Scale bars: A, C, F, I, L ¼ 1 mm; B, D, J, K, M, N ¼ 0.5 mm; E, G, H ¼ 0.2 mm. ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 855 divergence angles, follows a whorled pattern (Endress 2001). cium is spiral in the fossil, which is not the case in extant Initiation of the tepals in Nuphar and Nymphaea was de- Nymphaeales (it is whorled, as in the perianth, or may be- scribed in several studies (Cutter 1957, 1961, 1966; Chassat come irregular in the inner whorls when there is a large num- 1962; Grob et al. 2006). ber of stamens, which is not the case in the fossil; Endress Floral phyllotaxis in Austrobaileyales is spiral throughout 2001; Schneider et al. 2003), and (2) the position of the te- (Endress 2001). In contrast to Amborella, in Austrobaileya- pals is staggered, as in those ANITA-grade plants with spiral ceae and Trimeniaceae, the vegetative phyllotaxis is not spiral phyllotaxis and not as in Nymphaeales. In some Nymphaea- but decussate (i.e., forming dimerous whorls). At the onset of ceae (Nymphaea), the attachment areas of the rotten tepals a terminal flower, the outermost, smallest organs (bracts) are may become staggered in fruit by the growth of the inferior decussate, with a short transition zone to spiral (Austrobai- ovary, but they are closer together in flower (see figures in leya [fig. 3; Endress 1980b], Trimenia [fig. 7; Endress and Conard 1905). However, the described fossil of Microvictoria Sampson 1983]). However, this does not mean that there is a does not represent a fruit but a flower bud because there are gradual difference between whorled and spiral phyllotaxis. It no developing seeds apparent. In Nymphaeales (Cabomba- means only that there is a short transitional zone where they ceae and Nymphaeaceae), even if not all perianth organs are in- switch between each other and that the two patterns are serted at the same level, the outermost organs are always the completely distinct. A similar switch was shown in detail in longest and enclose all upper ones in bud. This is the case even flowers of Calycanthaceae (eumagnoliids, Laurales; Staedler in Barclaya, in which the outermost tepals are inserted at the et al. 2007). The distribution of perianth organ phyllotaxis base of the flower (Winter 1993; Williamson and Schneider 1994). patterns in the component clades of basal extant angiosperms Further, the nature of the less well-preserved center of the makes the basal state for the crown group equivocal (Endress flower as a gynoecium or a sterile structure not homologous and Doyle 2007). with a gynoecium (the latter favored by Gandolfo et al. [2004]) is unclear but would be important for an interpreta- Tepal Aestivation and Floral Bud Protection tion of the flower. According to the interpretation of Gandolfo with Regard to Phyllotaxis et al. (2004), the ovary is inferior. However, an inferior ovary is not visible, and from the shape of the flower bud, which is Protection of the young floral organs in bud is different in tapering downward in the attachment zone of the floral or- flowers with spiral and whorled perianth phyllotaxis among gans (in contrast to extant Nymphaeaceae; fig. 1E), the pres- basalmost extant angiosperms. In Amborella and all Austro- ence of an inferior ovary is unlikely. baileyales with spiral perianth phyllotaxis, the outer tepals These features indicate that the position of Microvictoria is are smaller than the inner ones and become gradually larger most likely not with Nymphaea and related genera (Victoria, (Endress 2004; fig. 3). This results in a staggered disposition together with Euryale, appears to be nested in Nymphaea or of the tepals in bud, and the periphery of the advanced floral at least sister to Nymphaea; Borsch et al. 2007; Lo¨hne et al. budisformedbyalargernumberoftepals.Thesmallertheouter 2007) and not even with Nymphaeales. Another argument ones, the higher their number. In early development, the outer- for a different position of Microvictoria is that the split be- most tepals cover the floral apex, but because they do not grow tween Victoria/Euryale and Nymphaea was calculated at much, this function gradually is taken over by larger inner tepals. 19.6–11.5 million years ago (Yoo et al. 2005), which is much In contrast, in Nymphaeales, which have whorled perianth more recent than the Turonian (90 million years old) Micro- phyllotaxis, the outer tepals are the largest ones, and they victoria. Thus, a structural reevaluation of Microvictoria will completely cover all inner ones in bud. Thus, the periphery be necessary for a new cladistic analysis. of the bud is made up by only the tepals of the outermost In general, the perianth is sometimes the most difficult part whorl (fig. 1D,1E; Meusel and 1965; Endress 2001, 2004). to reconstruct in fossil flowers because it often is the least In Nymphaeales, the floral buds develop underwater, emerg- well-preserved part (Scho¨ nenberger 2005) or is not preserved ing from the water only shortly before anthesis. In the female at all. If scars of outer organs are still present, then at least flowers of Hedyosmum (Chloranthaceae), the short perianth the phyllotaxis can be reconstructed, such as in the Early covers the stigma in bud, and the young flowers are protected Cretaceous Nymphaeales flower described by Friis et al. (2001). by the subtending bract. In the other three genera of Chlo- Certainly, interpretations of fossils based on extant plants ranthaceae, the youngest stages of the perianthless flowers should be made with caution. However, comparisons between are completely covered by their subtending bract, which forms extant plants and fossil plants are necessary and should be a kind of sheath around each flower (Endress 1987a;von carried out in as much detail as possible (see also Friis and Balthazar and Endress 1999). Male flowers of Hedyosmum Endress 1990; Friis et al. 2006). lack not only a perianth but also a subtending bract. The na- ked stamens protect each other in bud with their shieldlike, sterile apical portion (Endress 2008). Movements of Tepals (and Other Floral Organs) during Anthesis Interpretation of Floral Fossils Whereas in Cabombaceae and Nymphaeaceae the tepals The results of this study have implications for the interpre- commonly open and close, sometimes more than once, in Am- tation of floral fossils. An example is Microvictoria from the borella and Austrobaileyales, the perianth does not close again Upper Cretaceous, which was placed in a clade with Victoria, after anthesis, and thus the only conspicuous movement is Euryale, and Nymphaea (Gandolfo et al. 2004; reconstruc- opening when anthesis begins. This closure and reopening in tion in Crepet et al. 2004). (1) The phyllotaxis of the androe- Nymphaeales is associated with its aquatic habitat and Fig. 9 Tepals with nectaries (Nymphaeales). A–D, Cabomba caroliniana. A, Flower in female phase of anthesis, with paired nectaries on innertepals(arrow).B, Close-up of nectariferous appendage, nectary (arrow). C, Nectariferous hairs. D, Transverse section of tepal, showing ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 857

flowering above the water surface. In most taxa of Nymphaeales, ceae (tepalless, except for female flowers of Hedyosmum) and the flowers are submerged before and after anthesis and some- Ceratophyllaceae, which were of uncertain position in basal times even rhythmically for certain periods during anthesis. angiosperms for a long time, now also tend to come to the Most publications deal with the behavior of single species at a grade of basalmost angiosperms (Doyle and Endress 2000; specific place. From these studies, overarching patterns emerge. How- Qiu et al. 2005, 2006; Mathews 2006). Also, tepalless fossils ever, a comparative study on a largernumberoftaxaismissing. that may belong to the basalmost angiosperms have recently The only other movements known so far in bisexual flowers been described from the Early Cretaceous (Archaefructus; Sun among Austrobaileyales are in Austrobaileya, in which the et al. 2002; Friis et al. 2003; Ji et al. 2004). staminodes close over the gynoecium at the transition from The flowers of extant tepalless taxa have been studied de- the female to the male phase of anthesis (Endress 1980b, velopmentally, and in all of them, tepals are not even initiated; 2001; this article; fig. 5G,5H), and in Illicium, in which the thus, no cryptic perianth was found (Hydatellaceae [Rudall carpels close together, forming a cone at the transition from et al. 2007], Chloranthaceae [Endress 1987a; Kong et al. 2002], the female to the male stage of anthesis. In Trimeniaceae, in Ceratophyllaceae [Endress 1994b; Iwamoto et al. 2003]). De- contrast to Amborella, the tepals do not reflex during anthesis. velopmental genetic studies in Chloranthus (Chloranthaceae) They just spread and then fall off. showed that although there is no perianth, genes related to class A, B, and E genes, which are generally involved in perianth de- Abscission and Caducousness of Tepals (Sepals) velopment, are present (Li et al. 2005). An equally interesting feature is that some of these perianth- Tepal persistence or caducousness characterizes larger clades less plants are water plants that appear to flower underwater in basalmost angiosperms. Austrobaileyales have caducous te- (Hydatellaceae, Ceratophyllaceae, and Archaefructaceae). An- pals, and Amborella, Nymphaeales, and Chloranthaceae (He- other potentially aquatic fossil from the Early Cretaceous dyosmum) have persistent tepals. Caducous tepals are associated with apparently minute, simple, but poorly preserved flowers, with a narrow and thin attachment zone (indented in median Montsechia, may also be an angiosperm (Gomez et al. 2006). direction) with small-celled tissue. Persistent tepals have a broad To what extent the aquatic habitat, submerged flowering, and and thick attachment zone (streamlined in median direction), tepallessness may be functionally connected and the evolu- often without especially small-celled tissue. In addition, only tionary interpretation of tepallessness (Friis et al. 2003; En- in taxa with persistent tepals does syntepaly occur, as is found dress and Doyle 2008) will not be followed up on here. in Amborella, Cabomba (Nymphaeales), and Hedyosmum (Chlo- Morphological elaborations are not present in tepals of bas- ranthaceae). almost angiosperms, perhaps with the exception of Cabomba, Early abscission or caducousness of tepals (or sepals in eu- in which the inner tepals have curved appendages with nectaries dicots), although conspicuous in Austrobaileyales among the at the base of their blades. This is in contrast to more advanced basalmost angiosperms, is not so common in other groups of clades of angiosperms, in which the inner perianth organs angiosperms. It is also prominent in Papaveraceae and Berberi- (petals) have evolved various elaborations (Endress and Matthews daceae (Ranunculales, basal eudicots). In Berberidaceae, as in 2006). Austrobaileyales, it co-occurs with the presence of a relatively large number of sepals and an increasing size of the sepals from Tepals with Nectaries the periphery toward the center of the flowers. In Papaveraceae, there are only a few sepals, and they may be smaller or larger Distinct floral nectaries are known only from tepals of Ca- than the petals. However, in contrast to Austrobaileyales, Ber- bomba and Nuphar (Nymphaeales) among the ANITA grade beridaceae and Papaveraceae have a whorled, not spiral, sepal (Bernardello 2007). In both genera, these nectaries are associ- phyllotaxis (Eichler 1878; Hiepko 1965; Endress 1995). ated with dark yellow areas (nectar guides; fig. 9A,9E). How- Also in other flowering plants, organ abscission occurs in ever, the nectaries of Cabomba and Nuphar are at different small-celled tissue in the narrow and constricted base of the sites, and even more important, they are histologically differ- tepals. I did not study the process of abscission at the cytological ent. This different structure and position indicate that the nec- level, which was done for other groups (Addicott 1982; Bleeker taries are probably not directly homologous but rather have and Patterson 1997; Leslie et al. 2007). arisen by convergent evolution within Nymphaeales (see also Schneider and Jeter 1982; Vogel 1998). Histologically, Ca- bomba exhibits trichome-type nectaries, and Nuphar appears Presence or Absence and Elaboration of Tepals to conform to a combination of the mesophyll type and the Most of the basalmost extant angiosperms are characterized epithelial type (sensu Vogel 1977). Small quantities of nectar, by flowers with tepals. However, there are several tepalless produced at the base of tepals and stamens, were also reported taxa that have been transferred to the basalmost angiosperms from Illicium of Austrobaileyales (Thien et al. 2000). only recently. Hydatellaceae were transferred from Poales Among other basal angiosperms, nectaries are present on (monocots) to Nymphaeales (Saarela et al. 2007). Chlorantha- inner tepals in Asimina triloba (epithelial type; Endress 1994a)

hairs (arrows). E–H, Nuphar advena. E, Flower in female phase of anthesis, with nectary on inner tepals (arrow). F, Inner tepal from dor- sal side; lower border of nectary indicated with arrows. G, H, Close-up of nectary, showing nectar pore. I, Nuphar pumila, transverse sec- tion of inner tepal with nectary; nectar pore indicated with arrow. Scale bars: B ¼ 0.25 mm; C ¼ 0.05 mm; D, I ¼ 0.1 mm; F ¼ 0.5 mm; G, H ¼ 5 mm. 858 INTERNATIONAL JOURNAL OF PLANT SCIENCES and some other Annonaceae (Magnoliales). Laurales are char- tural aspects, makes the situation more complicated. In acteristic for their nectaries on stamens and staminodes Cabomba, apart from developmental delay and nectar pro- (Endress 1980a; Endress and Lorence 2004; Chanderbali duction, there is no obvious difference between the outer te- et al. 2006; Buzgo et al. 2007). It is noteworthy that nectaries pals and the inner tepals. Both have the same size and color, in some basal angiosperms are not single massive tissues, as both are relatively thin, both have intercellular spaces, and usually found in more derived groups, but associations of both have a papillate epidermis. In other groups, the outer many small nectariferous areas, termed ‘‘nectarioles’’ by Vogel and inner tepals are much more different in these features but (1998), such as on the tepals of Chimonanthus (Calycantha- may not have the developmental delay in the inner tepals. ceae, Laurales) and Aristolochia (Aristolochiaceae, Piperales) A concept for the understanding of perianth evolution and and on the floral subtending bracts of the tepalless Peperomia the use of sensible terms for the perianth organs in different (Piperaceae, Piperales; see also Vogel 1998). clades of angiosperms is still to be worked out. How much The diverse structure, rare occurrence, and scattered distri- will the use of the existing terms ‘‘tepals,’’ ‘‘sepals,’’ and bution of nectaries indicate convergent evolution not only in ‘‘petals’’ need to be modified in the future? As an important Cabomba and Nuphar but also in other basal angiosperms. step toward a resolution, it would be useful to know more It may also indicate that in early angiosperms, nectar was about the development, anatomy, histology, and behavior of not a major floral reward (see also Thien et al. 2003). the perianth organs across all groups of basal angiosperms (not only the basalmost clades). Also, the fossil record should Bracts and Tepals, Sepaloid and Petaloid be evaluated. The currently oldest-known fossils with pre- Tepals, and Sepals and Petals served tepals are related to Hedyosmum (Eklund et al. 2004; Friis et al. 2005, 2006). Such a comparative structural study is It has often been reported that in some basal angiosperms still lacking, and it would need a big effort. For eudicots, such there is a gradual transformation from (smaller) bracts to an approach has been attempted (Ronse De Craene 2007, (larger) tepals and from (green) sepaloid tepals to (colored) 2008). As a further step, the evolution of the diversity of these petaloid tepals. This is especially obvious in spiral flowers features should be analyzed on the basis of the currently avail- with a relatively high number of organs and relatively long able phylogenetic studies of angiosperms; there are some ini- and equal plastochrons between the initiation of subsequent tial attempts of such studies (Doyle and Endress 2000; Ronse organs, in which the transformation occurs in equal steps. In De Craene et al. 2003; Zanis et al. 2003; Endress and Doyle Amborella and Austrobaileyales, in which the outermost te- 2007, 2008). Likewise, the genetic program for perianth de- pals are smaller than the inner ones and bractlike, this is espe- velopment and its origin and evolution in angiosperms should cially obvious (Amborella [Endress and Igersheim 2000; also be further elucidated (Jaramillo and Kramer 2004, Posluszny and Tomlinson 2003; Buzgo et al. 2004], Austro- 2007a, 2007b; Stellari et al. 2004; Kim et al. 2005; Baum and baileya [Endress 1980b, 1983], Trimeniaceae [Endress and Hileman 2006; Irish 2006; Kramer and Zimmer 2006; Soltis Sampson 1983]). Among other basal angiosperms, it is present et al. 2006, 2007a,2007b; Litt 2007). Both the structural and in Calycanthaceae of Laurales (Staedler et al. 2007). However, the developmental genetic approach would be important to eval- the phenomenon is not restricted to basal angiosperms. It also uate homologies (Wagner 2007). The evolutionary understanding occurs rarely in eudicots (e.g., Camellia, Tutcheria, Theaceae, Ericales; Eichler 1878; Melchior 1925; Tsou 1998). Developmentally, instead of a one-step change from bracts to tepals (sepals) or from sepals to petals, as is common in whorled flowers with very short plastochrons between the or- gans of a whorl but a very long plastochron between two whorls, the change occurs in several smaller steps. A ‘‘fading border’’ model has been proposed to explain this pattern at the genetic level (Buzgo et al. 2004; Soltis et al. 2007a, 2007b). It appears easier to apply this model to describe the development of flowers with an increased (evolutionarily de- rived) number of perianth organs in spiral arrangement rather than to see it as an expression of a primitively multistep grada- tion from an outer to an inner morph of tepals or from sepals to petals. The multistep gradation per se may not be basal in angiosperms, but it could easily evolve at this level and less easily in more derived groups. This should be further explored.

Perianth Organ Origin and Evolutionary Differentiation In earlier publications, the delay in development of the in- ner tepals in Cabomba, which, together with the presence of Fig. 10 Cladogram of basalmost angiosperms (topology combined nectaries on them, resembles the petals of some eudicots (espe- from Qiu et al. 1999, 2005, 2006; Renner 1999; Doyle and Endress cially Ranunculales), was emphasized (Endress 2001, 2002). 2000; Duvall et al. 2006; Mathews 2006; Saarela et al. 2007). Blue, This was similarly discussed for Nuphar (Hiepko 1965). taxa with persistent tepals; red, taxa with caducous tepals; green, taxa However, a more inclusive view, including additional struc- without tepals. ENDRESS—PERIANTH IN BASAL ANGIOSPERMS 859 of sepals and petals is so difficult because specific functional Some of these differential features of the perianth are com- and developmental constraints similar to those of male- and paratively largely unexplored in other basal extant angio- female-producing parts in stamens and carpels are not present, sperms (i.e., magnoliids). It would be of interest to shed light and thus, more evolutionary flexibility may be expected (see on the diversity in behavior of the perianth in a large range also Endress 1994a, 2006; Stuessy 2004). of basal angiosperms, also in comparison with monocots and eudicots, to contribute to the elucidation of perianth evolu- tion in angiosperms. Conclusions Austrobaileyales are distinctive among the basalmost angio- Acknowledgments sperms in having tepals that fall off during or at the end of an- thesis (fig. 10). The site of abscission is preformed structurally I thank Thomas Denk and Ju¨ rg Scho¨nenberger for the invi- by narrowness and constriction of the tepal base, associated tation to participate in the international paleobotanical sym- commonly with small-celled tissue. In contrast, in Amborella, posium ‘‘In Search of the Earliest Flowers’’ in honor of Nymphaeales, and Hedyosmum (Chloranthaceae), tepals are Professor Else Marie Friis, held in Stockholm in June 2007, persistent. Their base is broad, not constricted (streamlined in and to contribute to this special issue of the International median longitudinal section) and commonly not especially Journal of Plant Sciences. In the early 1980s, Else Marie Friis small-celled. Amborella and Austrobaileyales are distinctive pioneered studies of three-dimensionally preserved Cretaceous in their spiral perianth phyllotaxis, combined with the stag- flowers that became important for our understanding of early gered placement of tepals, with the smallest being outside and flower evolution. She is a leader in the field, and her research becoming gradually larger toward the inside of the flower. In has been a model for many colleagues and students. I thank contrast, in Nymphaeales, perianth phyllotaxis is whorled and Bernie Hyland for support in the field in Northern Queens- not staggered, with the largest tepals outside, covering all the land, Alex Floyd in New South Wales, and Gordon McPher- inner ones in bud. In the basal grade of extant angiosperms, son in New Caledonia. Further, I thank F. Bruce Sampson, complete lack of a perianth is more common than in more de- Ju¨ rg Scho¨ nenberger, and Hiroshi Tobe, who provided fixed rived groups because it occurs in Hydatellaceae, Chloranthaceae material. I am grateful to Rosemarie Siegrist for microtome (except for female flowers of Hedyosmum), and Ceratophylla- sections, Urs Jauch for support with the SEM, and Alex Bern- ceae as well as the fossil Archaefructaceae (see also Endress hard for artwork. Three anonymous reviewers are thanked for and Doyle 2008). valuable comments on the manuscript.

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