Developmental Study on the Inflorescence and Flower Of

Botanical Journal of the Linnean Society, 2002, 140, 39–47. With 37 ﬁgures

Developmental study on the inﬂorescence and ﬂower of Caldesia grandis Samuel (Alismataceae)

KE-MING LIU1, LI-GONG LEI1,2*, and GUANG-WAN HU1

1Department of Botany, College of Life Sciences, Hunan Normal University, Changsha, 410081, Downloaded from https://academic.oup.com/botlinnean/article/140/1/39/2433605 by guest on 29 September 2021 Hunan, People’s Republic of China 2Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, Yunnan, People’s Republic of China

Received January 2002; accepted for publication May 2002

The inflorescence and floral development of Caldesia grandis Samuel is reported for the first time in this paper. The basic units of the large cymo-thyrsus inflorescence are short panicles that are arranged in a pseudowhorl. Each panicle gives rise spirally to three bract primordia also arranged in a pseudowhorl. The branch primordia arise at the axils of the bracts. Each panicle produces spirally three bract primordia with triradiate symmetry (or in a pseudowhorl) and three floral primordia in the axils of the bract primordia. The apex of the panicle becomes a terminal floral primordium after the initiations of lateral bract primordia and floral primordia. Three sepal primordia are initiated approximately in a single whorl from the floral primordium. Three petal primordia are initiated alternate to the sepal primordia, but their subsequent development is much delayed. The first six stamen primordia are initiated as three pairs in a single whorl and each pair appears to be antipetalous as in other genera of the Alis- mataceae. The stamen primordia of the second whorl are initiated trimerously and opposite to the petals. Usually, 9–12 stamens are initiated in a flower. There is successive transition between the initiation of stamen and carpel primordia. The six first-initiated carpel primordia rise simultaneously in a whorl and alternate with the trimerous stamens, but the succeeding ones are initiated in irregular spirals, and there are 15–21 carpels developed in a flower. Petals begin to enlarge and expand when anthers of stamens have differentiated microsporangia. Such features do not occur in C. parnassifolia. In the latter, six stamen primordia are initiated in two whorls of three, carpel primordia are initiated in 1–3 whorls, and there is no delay in the development of petals. C. grandis is thus considered more primitive and C. parnassifolia more derived. C. grandis shares more similarities in features of floral development with Alsma, Echinodorus, Luronium and Sagittaria. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 39–47.

ADDITIONAL KEYWORDS: bract primordia – ﬂoral primordia – initiation – organogenesis – sequences – systematic relationships.

INTRODUCTION distribution of C. parnassifolia is more widespread than that of C. grandis (Chen, 1992). Caldesia Parl. is a small genus of Alismataceae. It has Caldesia grandis is an aquatic or swampy herba- four species distributed in the Old World Tropics (one ceous perennial with upright aerial stems 80–120 cm extends to Europe) and is often associated taxonomi- high, small erect rhizomes and basal, simple, oblate cally with Alisma Linn (Mabberley, 1987). Only two leaves, c. 4.5 cm long and c. 6.5 cm wide, concave apex species, C. grandis Samuel and C. parnassifolia (Bassi with an acute tip at the end of the middle vein, and ex L.) Parl., are native to China. Caldesia grandis straight or slightly cordate or rarely decurrent base. differs morphologically from C. parnassifolia in leaf The leaf blade has parallel basal veins and a petiole shape and the numbers of stamens and carpels. The 15–50 cm long with a basal sheath. Branches with turions enveloped by 5–7 scales (bracts) may arise *Corresponding author. E-mail: [email protected]. from the sheath. The turion drops off naturally when

© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 39–47 39 40 K.-M. LIU ET AL. it is mature and will develop into a new plant. The This paper reports the development of the inflores- inflorescence is a cymo-thyrsus with a 30–60 cm high cence and flowers of Caldesia grandis Samuel, com- peduncle. It branches in whorls and each whorl has pares it with that of C. parnassifolia, with the aim of three branches. Each branch is subtended by an providing new information concerning the phylogeny acutely tipped lanceolate bract. The flowers are bisex- of the genus and the family. ual and subtended by a bract. Each flower has a pedicel 1.2–2 cm long, or more; the three sepals are MATERIAL AND METHODS greenish with longitudinal stripes, elliptic or broad ovate and deflexed, 3–4 mm long, and persistent; the The material (Table 1) for floral initiation and devel- three petals are white, 6–8 mm long, spoon-like or opmental observation was collected from Mangshan

nearly obovate, flat or reflexed; stamens 9–12, with Mountain National Natural Reserve, Yizhang County, Downloaded from https://academic.oup.com/botlinnean/article/140/1/39/2433605 by guest on 29 September 2021 basal fixed anthers; carpels are often 15–21, free, and Hunan Province. The inflorescences at different stages irregularly arranged in the centre of the flower, with of development were preserved in FAA 1 : 1 : 3. Vouch- erect or slightly curved styles about 1.5 mm long ers are deposited in the Herbarium of Hunan Normal arising from the ventral tops of carpels. The achene University (HHNU). has 3–5 ridges and a straight, or more or less curved, The fixed material of inflorescences was dehydrated rostrum that is longer than the achene. through a series of alcohol solutions ranging from 50% The carpel arrangements in Alismataceae are in a to 95%. Bracts and perianths were then dissected at single whorl as in Alisma and C. parnassifolia or in a relevant developmental stages. The pretreated mate- head as in Sagittaria, Echinodorus (Salisbury, 1926; rial was further dehydrated with, and temporarily Charlton, 1968, 1973; Singh & Sattler, 1972, 1973, preserved in, 100% alcohol. The material was passed 1977; Sattler & Singh, 1978; Wang & Chen, 1997), through a series of iso-pentanol acetate and ethanol Ranalisma (Charlton, 1991; Charlton & Ahmed, alcohol solutions and the alcohol replaced by iso- 1973a,b), and C. grandis. Observations on the floral pentanol acetate before being dried in a Hitachi HCP- anatomy of the family (Salisbury, 1926; Charlton, 2 CO2 Critical Point Dryer. When dried it was mounted 1968) and floral development of Alisma triviale Pursh on stubs and coated with gold in an RMC Eiko IL-5 (or, A. plantago-aquatica Linn.), Echinodorus ama- Ion Sprayer. The micrographs were taken with a zonicus Rataj, E. tenellus Rataj, Sagittaria cuneata E. Hitachi S-570 and a JEOL JSM-5600 L scanning elec- Sheldon and S. latifolia Willd. (Charlton, 1968; Kaul, tron microscope (SEM) at 25 kV. 1967; Singh & Sattler, 1972, 1973, 1977; Sattler & Singh, 1978), Luronium natans (Linn.) Raf., Ranal- RESULTS isma humile (Kuntze) Hutch. (Charlton, 1991, 1999a; Charlton & Ahmed, 1973a,b), and Ranalisma rostra- The young cymo-thyrsus has many branches that are tum Stapf (Wang et al., 1998) have revealed that the triradiately developed around the main rachis and alismataceous flowers conform to a basic trimerous produce the many triradiately arranged short panicles pattern of initiations of floral parts, and the first six which are the basic units of the ramification system of stamens appear to arise in pairs associated with the the inflorescence (Fig. 1). Each panicle gives rise to petal primordia. Recently, Wang & Chen (1997) reported floral organogenesis in C. parnassifolia and revealed that the sepals are initiated centripetally in a spiral; the Table 1. Material used for floral initiation and develop- petals are initiated almost simultaneously in a whorl, ment studies with six stamens initiated, respectively, in two whorls, but rearranged in a single whorl in the mature flower. Numbers of The carpels are initiated sequentially in three whorls specimens and each whorl has three carpels, but most often the and vouchers Provenance Altitude Date inner two whorls may have 1~3 carpels. This indicates Liu (777377) Langpan Lake 1300 m 1.vii.1993 that the flower of C. parnassifolia is trimerous ab Liu & Lei Langpan Lake 1300 m 4.v.1998 initio. The spirally initiated outer perianth is a prim- (770664) itive character state in the family. There are no Liu (777229) Guaihu Lake 1260 m 25.iv.1999 stamen-pairs in the first stamen whorl, although floral Liu & Lei Langpan Lake 1300 m 26.iii.2000 development conforms to the trimerous alternating (21165) sequence seen in most genera in the family. The devel- Liu & Lei Langpan Lake 1290 m 30.v.2000 opment of the inflorescence is not mentioned in Wang (774663) & Chen (1997).

© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 39–47 DEVELOPMENTAL STUDY OF CALDESIA GRANDIS 41 three bract primordia spirally and, in addition, one process of stamen initiation in the flowers of this basal prophyll (Figs 2, 3). The bract primordia grow species. The third whorl of stamen primordia (only fast and become acutely tipped scoop-like bracts that three) may, or may not, be initiated. Thus, 9–12 will finally become lanceolate (Figs 4–9). The branch stamens are developed in the flowers arranged into primordia of the panicles arise in the axils of the two or three whorls (Fig. 19). During development, the bracts (Figs 1–9) and produce primordia in an asym- stamen primordia change their shape from subglobose metric way such that the primordia arise at the to elliptoid, and eventually become dumbbell-like abaxial lateral positions and the abaxial median because the two ends of each stamen primordium primordium arises much later (Figs 1, 3, 7–9). The swell or broaden (Figs 19–23). Then, on the outer main rachis of the panicle produces spirally three surface of each stamen, two longitudinal protuber-

crescentic bract primordia with triradiate symmetry ances are initiated, which, in addition to the marginal Downloaded from https://academic.oup.com/botlinnean/article/140/1/39/2433605 by guest on 29 September 2021 (Figs 4–9). Each panicle usually produces three lateral parts, develop into the microsporangia, i.e. formation primordia and a terminal primordium, but sometimes of anthers; at this time, the petal primordia begin to the main axis produces six or more lateral primordia broaden, but they are still smaller than the stamens and a terminal primordium (Figs 7–9). Multicellular (Figs 24–26). The furrow between the two outer hairs develop at the base and between the branches of microsporangia becomes deeper and narrower, and the inflorescence (Figs 1–4, 7, 9). finally becomes a slot such that they become The floral primordia arise in the form of transverse appressed. At the same time, the petals take their protuberances in the axils of the bract primordia form (Figs 27, 28, 36). The furrows between the outer (Figs 4–9); an arc-shaped groove is formed between microsporangia and marginal ones are fairly shallow them (Figs 5–9) which then becomes a half-circle and (Figs 28, 36). The mature stamens become irregularly their delimitation becomes obvious. The arc-shaped arranged. A short basally fixed filament forms beneath bract primordium surrounds the new-moon-like floral each anther, and the connective is confined to the primordium (Figs 3–9). ventral part of the anther (Figs 36, 37). The develop- The floral primordium then becomes a round protu- ment of the petals is such that their primordia retain berance, the bract becomes scoop-like with a bracteole their hemispherical shape until the four microsporan- beside it. Three sepal primordia are produced almost gia of stamens have developed and the ovules of the simultaneously and the remaining central part carpels initiated (Figs 23–28). becomes triangular (Fig. 10). The sepal primordia are When all stamen primordia have been initiated and ellipsoid (Figs 10–12). begun to broaden, the remaining floral primordium At the three angles formed by the triangular central becomes slightly flat. Although both the stamen and part of the floral primordium, and alternate with the carpel primordia have no clear-cut differences in three sepal primordia, arise three round protuber- appearance, comparison with mature flowers suggests ances, when the sepal primordia extend transversely that at this time carpel primordia begin to develop. (Figs 11, 12). These three protuberances are petal pri- The first six carpel primordia (apparently smaller mordia. A short pedicel forms on initiation of the sepal than the last-initiated stamen primordia) are pro- and petal primordia (Fig. 11). duced in a whorl in alternate positions opposite and After initiation of the three petal primordia, a pair between the second and the third whorl of stamen pri- of stamen primordia arises on each side of the trian- mordia (Fig. 19). Sometimes, the carpel primordia are gular central floral primordium and opposite each initiated in an irregular way so that more or less than petal primordium (Figs 13–15). Therefore, six stamen six primordia are somehow spirally arranged when the primordia are initiated simultaneously and will stamen primordia of the third whorl are not initiated, develop into the first whorl of stamens. At this time, even when the number of the stamen primordia of the the subtending bracteole elongates and becomes lance- first whorl is less than six (Figs 18, 20, 21). Despite olate (Fig. 16). Rarely, in some flowers, less than six this the succeeding carpel primordia are certainly ini- stamen primordia are initiated in the first whorl, and tiated in spirals (Figs 22–26). During the initiations of hence the initiation of succeeding floral organs is the carpel primordia, some apices of the floral pri- somewhat irregular (Figs 12, 18). At the three posi- mordium become convex and stop producing carpel tions above and opposite the three petal primordia primordium (Figs 23, 25, 26), so the spaces between arise the three primordia of the second whorl of the carpel primordia are larger than between the stamens (Figs 17, 18). The stamen primordia of the earlier initiated ones (Figs 28, 29). Later, the ventral third whorl arise at three points above the stamen part of each carpel primordium becomes concave due pairs of the first whorl, alternating with the three to the outward growth of the marginal parts stamen primordia of the second whorl and opposite to (Figs 27–31) and an ovule initiates at the ventral base the sepals (Figs 17–19). This may be the regular of the concave peltate carpel (Figs 28, 29, 31). Each

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Figures 1–12. Figs 1–9. Development of the inflorescence of Caldesia grandis. Fig. 1. Young inflorescences with several triradiately and spirally arranged bracts (B) and branchlet primordia. Some floral primordia are already initiated. Figs 2–9. Development of short panicles with a prophyll (Pr). The apex of the inflorescence is dome-shaped. The axillary branchlet primordia (bl) with subtending bract primordia (B) are initiated in a spiral sequence and arranged in pseudowhorls. The axillary floral primordia (F) with subtending bract primordia (B) arise in the same way. Note hairs (H) developed at the nodes. Figs 10–12. Development of flowers. Fig. 10. The three sepals (K) have already been initiated almost in a whorl; the remaining floral primordium (F) becomes triangular and nearly flat and there is a bracteole (b) beside it; petal primordia (C) initiated at the angles and stamen primordia (S) arise in pairs near the petal primordia (C). Fig. 11. The petal primordia (C) are alternate to the sepal primordia (C) in a lateral view of a young flower and a short pedicel has developed. Fig. 12. The positional relationship between the sepal primordia (K) and the petal primordia (C) and stamen primordia (S) in an overview of a young flower. Scale bars: Figs 1,10,12 = 50 mm; Fig. 11 = 75 mm; Fig. 8 = 130 mm; Fig. 9 = 150 mm; Figs 3, 6, 7 = 200 mm; Figs 2, 4, 5 = 250 mm.

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Figures 13–24. Initiation and development of floral parts of Caldesia grandis. Figs 13,14. Sepal primordia, the triangular floral primordia, petal primordia and the first whorl of stamen primordia begin to initiate. Fig. 15. The broadened sepal primordia, primordia of three petals (C) and six first-whorl stamens (S). Fig. 16. Lateral view of a young flower showing the positional relationships between sepals and petal primordia (C) as well as stamen primordia of the first whorl. The subtending bract (b) of the flower becomes lanceolate. Fig. 17. The shallow-bowl-shaped sepals, primordia of petals and first two whorls of stamens. The third-whorl stamen is beginning to initiate. The flower is embraced by a prophyll (Pr). Fig. 18. The enlarged shallow-bowl-shaped sepals, petals and all stamens. The first-whorl carpel primordia begin to initiate opposite the third whorl stamens. Figs 19–24. Initiation of carpel primordia (P), outgrowth of stamens (S). The microsporangia begin to differentiate on anthers but the development of petals (C) is delayed since they are smaller than stamens. Sepals have been removed. Scale bars: Figs 13–16,18 = 50 mm; Fig. 17 = 100 mm; Fig. 19 = 107 mm; Figs 20,21,23 = 120 ; Fig. 24 = 150 mm.

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Figures 25–37. Development and differentiation of inner floral organs. Figs 25,26. Petals (C) begin to expand, microsporangia of anthers have differentiated and all carpels have been initiated. Figs 27,28. Petals (C) enlarged and expanded but they are still shorter than well-developed anthers of stamens, carpels hollowed and a single basal ovule initiated. Fig. 29. Carpels on the central part have large intervals between them. Figs 30–35. Carpels are peltate, but rare carpels having a high base develop at the top of the floral apex. A single basal ovule is initiated in each carpel before the closure of the ovaries, and a rostrum-like style develops on the top of the ovary on enclosure (in Figs 32,35). Ventral suture extends to the style (in Fig. 35). The white chips on the carpel in Fig. 30 are aretefacts introduced during the drying process. Figs 36,37. Dorsal and ventral views of mature stamens. Stamen has a long anther and a short filament. The connective of the anther is confined to the ventral side and is a longitudinal protuberance. Scale bars: Figs 30,31 = 20 mm; Fig. 29 = 150 mm; Fig. 25 = 176 mm; Figs 26–28 = 200 mm; Fig. 32 = 0.27; Fig. 35 = 0.37 mm; Figs 33,34,36 = 0.38 mm; Fig. 37 = 0.60 mm.

© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 39–47 DEVELOPMENTAL STUDY OF CALDESIA GRANDIS 45 peltate carpel has a base and the one at the top of the number of stamens can be less than 12 or only 9. the floral apex has a longer base (Figs 30, 31). In total, Stamen initiation is followed by that of carpels. 15–19 or more carpels are initiated in a flower (Figs Although both the stamen and carpel primordia have 32, 33). A mature carpel or fruit has a large oblique no clear-cut differences in initial appearance, we can ovary and a short apex on a ventrally orientated style. judge (by comparison with mature flowers) the point The fruit forms a head. The stigma is not differenti- at which, following initiation of 9 or 12 stamen pri- ated from the style; the ventral suture extends to the mordia, the floral primordium begins to produce carpel style (Figs 34, 35). primordia. Carpels are initiated in an irregular way, in neither whorls nor spirals, apart from the six carpels of the first whorl. There may be up to 21, but DISCUSSION

most often less than 19 carpels. They are peltate Downloaded from https://academic.oup.com/botlinnean/article/140/1/39/2433605 by guest on 29 September 2021 The basic units of the inflorescence of Caldesia grandis according to the types described by Van Heel (1983, are triradiately arranged short panicles with three 1984), Endress (1994), Taylor & Kirchner (1996) and lateral branches and a central rachis. This species Liu & Lu (1999); the carpel at the top of the floral seems to have some differences in inflorescence con- apex has a long base. The carpels are arranged in a struction from others previously described. Specifi- head similar to those of Sagittaria, Echinodorus cally, it seems to have a much simpler inflorescence (Charlton, 1968, 1973); Sattler & Singh, 1978; Singh than C. reniformis. The apex of each panicle gives & Sattler, 1972, 1973, 1977), and in Ranalisma rise to three (or, rarely more) bract primordia in (Charlton, 1991; Charlton & Ahmed, 1973a,b). Calde- spiral sequence, and the primordia are arranged in sia grandis shares more similarities in features of a pseudowhorl. The bract primordia grow fast and floral development with Alsma, Echinodorus, Luro- become acutely tipped scoop-like bracts that then nium and Sagittaria. become lanceolate. The branch primordia of the In C. parnassifolia, all floral parts are trimer- panicle arise at the axils of the bracts and they ously initiated, three sepals in a spiral, three petals produce primordia in an asymmetrical way such that approximately in a whorl; six stamens are initiated in two primodia arise at the abaxial lateral positions and two whorls with three stamens in each; carpels arise the abaxial median one arises much later. The main in 1–3 whorls; and there is no delay in development of rachis of the panicle produces spirally three- or six- petals (Wang & Chen, 1997). The flowers of C. grandis bract primordia with triradiate symmetry such that have more primitive characters. The flowers of C. par- there are three bract primordia in a pseudo-whorl. nassifolia are more reduced. Caldesia parnassifolia is Some multicellular hairs develop at the base of the considered a derived species. panicles, although the plants are described as Inflorescences of most of the Alismataceae have glabrous. The floral primordia arise in the axils of the bracts in sets of three forming pseudowhorls, i.e. a set bract primordia. The remaining apex of the inflores- of bracts or bracts that appears to form a whorl, but cence becomes a terminal floral primordium after the initiation is sequential (Charlton & Posluszny, 1999). initiations of lateral bract primordia and floral pri- The development of the inflorescence of C. grandis mordia. Sepals of each flower are initiated in a whorl apparently conforms to this pattern. of three as are the petals, but the development of the Stamens of the first whorl arising in pairs is a petals is much delayed until the four microsporangia feature common to most genera of the Alismataceae. of the anthers have differentiated and all carpels have In the flowers of Alisma, Echinodorus and Sagittaria initiated. The delay of development of petals is unique (with both unisexual and bisexual flowers), the stamen to the Alismataceae. Stamens are initiated in three pairs are adjacent to the petals, and their initiation is whorls; six stamen primordia of the first whorl are ini- closely related to the initiations of petal primordia. tiated in pairs on the three sides of the triangular They are considered as being derived from so-called central part of the floral primordium and each pair on petal-stamen primordia (CA primordia). The CA pri- each side is opposite to a petal. The three stamen primordia are reported to exist in the floral development mordia of the second whorl are initiated in positions of those three genera (Singh & Sattler, 1972, 1973, opposite the petal primordia; however, each third 1977; Sattler & Singh, 1978; Charlton & Posluszny, whorl is formed opposite the sepals, and at each side 1999). It was suspected that the CA primordia do not is inserted alternately between the stamen primordia exist in the floral developments of Luronium, Ranal- pair of the first whorl. So, in total, there are usually, isma and even in other taxa (Charlton, 1991, 1999a; although not always regularly, 12 stamens initiated in Wang et al., 1998). They may merely represent each flower. There are some variations in the numbers changes in the shape of the apex before petal and of stamen primordia in each whorl and also in timing stamen initiation (Charlton, 1991). In C. grandis, the of initiation. For example, the number of the first- stamen pairs of the first whorl are directly opposite to whorl stamen primordia can be less than six, so that the sepals rather than petals and there are no CA pri-

© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 39–47 46 K.-M. LIU ET AL. mordia. In Ranalisma, sepals, petals, stamens and REFERENCES carpels are initiated unidirectionally, and that is Charlton WA. 1968. Studies in the Alismataceae. I. Develop- unique and primitive in Alismataceae (Charlton & mental morphology of Echinodorus tenellus. Canadian Ahmed, 1973a,b; Charlton, 1991; Wang et al., 1998). Journal of Botany 46: 1345–1360. In Wiesneria (with unisexual flowers) and C. par- Charlton WA. 1973. Studies in the Alismataceae. II. Inflores- nassifolia, there are no stamen-pairs in floral cences of Alismataceae. Canadian Journal of Botany 51: development (Charlton, 1999b). Wiesneria may have 775–789. relationships with Caldesia through C. parnassifolia, Charlton WA. 1991. Studies in the Alismataceae. IX. Devel- although the phylogenies of Les & Haynes (1995), Les opment of the flower in Ranalisma humile. Canadian & Schneider (1995), Les, Cleland & Waycott (1997), Journal of Botany 69: 2790–2796.

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