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Development and Morphogenesis |
2Royal Botanic Garden, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK; and Institute of Cell and Molecular Biology, The University of Edinburgh, Edinburgh EH9 3JH, Scotland, UK
Received for publication January 7, 2003. Accepted for publication June 11, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1–2.5 mm long) and numerous. They consist of a small portion of stem (bract-stem) topped by opposite storage bracts that enclose a minute apical meristem. A secondary root develops from the side of the bract-stem. The floral meristem of T. oldhamii has three possible fates: (1) bulbil formation, (2) flower formation, or (3) bracteose proliferation. Bracteose proliferation rarely occurs and appears to be a developmental transition between the bulbiliferous and racemose inflorescence forms. It is strongly reminiscent of the floricaula and squamosa mutants of Antirrhinum. In the bulbiliferous form a single floral primordium, which would normally produce one flower, gives rise to 50–70 bulbils by repeated subdivision of the meristem. This form of bulbil production appears to be unique to Titanotrichum. Occasionally a floral meristem divides, but the subdivision forms multiflowered units of up to four flowers rather than bulbils, suggesting that meristem fate is reversible up to the first or second meristem subdivision. In Titanotrichum, therefore, primordium fate is apparently not determined at inception but becomes irreversibly determined shortly after the appearance of developmental characteristics of the floral or bulbil pathway.
Key Words: bracteose proliferation • bulbil • China • floral meristem • floricaula • gemmae • Gesneriaceae • Japan • squamosa • Taiwan • Titanotrichum oldhamii • vivipary
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1895
; Solereder, 1909
; Sealy, 1949
). Titanotrichum oldhamii was cultivated in Europe as an ornamental for its distinctively deep yellow corolla tube with lobes blotched dark crimson-brown. The inflorescence of T. oldhamii is an indeterminate raceme, although the family Gesneriaceae, to which it belongs, usually produces pair-flower cymes (Weber, 1973
, 1978
, 1982
, 1995
; Pan et al., 2002
).
It grows in shaded habitats along creeks, particularly on dripping cliffs or moist limestone slopes in dense forest and on rocks near caves and waterfalls. It is not a common plant but has a scattered distribution in Taiwan, the Fujien province of China, and the Ryukyu Islands of Japan (Henry, 1898
; Hayata, 1908
, 1911
; Hemsley, 1909
; Walker, 1976
; Wang et al., 1998
). Interestingly, although it produces many flowers in the wild, it rarely sets seed and appears to rely largely on asexual reproduction by bulbils and rhizomes. Genetic variation and the failure of seed set are being studied at Edinburgh (C.-N. Wang, unpublished data).
Gesneriaceae species are known for their great range of morphological variation, resulting from variation in meristem behavior (Jong and Burtt, 1975
; Möller and Cronk, 2001
). While in most Gesneriaceae the unusual meristem behavior affects only vegetative parts (Burtt, 1970
; Tsukaya, 1997
; Imaichi et al., 2000
), Titanotrichum is unusual in having variable meristem behavior in reproductive parts.
There are many plants in which all or some flowers of an inflorescence are converted into asexual bulbils. In most cases, a single floral meristem is replaced by a single bulbil (e.g., Polygonum viviparum L., Ranunculus ficaria L., Saxifraga cernua L., Allium spp., Festuca vivipara (Rosenv.) E. B. Alexeev.; Kerner, 1904
; Troll, 1964
; Engell, 1973
; Arizaga and Ezcurra, 1995
; Briggs and Walters, 1997
; Diggle, 1997
). In Titanotrichum however, a single floral meristem is replaced by a cluster of 50–70 bulbils (Stapf, 1911
; Hayata, 1912
). In Mimulus gemmiparus W. A. Weber, it is not the floral meristem but the adjacent proximal meristem (dormant in other species of Mimulus) that develops into a bulbil (Weber, 1972
; Moody et al., 1999
). Pseudovivipary, often found in alpine or arctic habitats, is often assumed to be an adaptation to poor sexual reproduction under extreme conditions (Kerner, 1904
; Youngner, 1960
). In contrast, Titanotrichum grows in a subtropical area with a favorable environment, although sometimes in deep shade.
As part of a wider study of reproduction in this species, the morphology of bulbil development was investigated. Titanotrichum is unique in producing large numbers of bulbils in place of a single flower. We were therefore interested in answering the following questions: (1) how a single floral meristem is replaced with numerous bulbil meristems, (2) how an inflorescence changes from flower to bulbil production, and (3) how bulbils differ from seeds as functional reproductive units.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Because Titanotrichum rarely produces seed, mature seeds were obtained from a pollination experiment in Yangmingshan National Park (25°09' N, 121°33' E), Taipei region, during the summer of 1999. Seed germination requires light and was carried out under constant lighting in petri dishes at 22°C and 90% relative humidity in controlled environment growth cabinets, on wet filter paper. Growth experiments were conducted in walk-in growth rooms manufactured by Swann Technology (Royston, UK) with controllable temperature and daylength. Lighting was provided by 13-W cool white fluorescent tubes.
Fixation of plant tissue
Different stages of the inflorescence shoot, seedlings, and germinating bulbils were fixed overnight in FAA (18 parts of 70% ethanol : 1 part glacial acetic acid : 1 part formalin) and taken through an ethanol series to 100% acetone dehydration before proceeding to critical point drying (CPD) with an Emitech K850 machine (Ashford, UK). The dried samples were immediately mounted on aluminium stubs using carbon discs and coated twice with gold palladium for 2 min (from different angles) in an Emscope SC500 sputter coater (Quorum Technologies, Newhaven, UK). To see the development of the meristem clearly, most bracts and bracteoles were removed, especially in the young inflorescence, using fine forceps either before fixation or, less satisfactorily, after CPD.
Scanning electron microscopy
Specimens were examined with a Zeiss DSM scanning electron microscope (Oberkochen, Germany) at a working distance of between 9 and 14 mm and an accelerating voltage of 5 kV.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1 yr old) growing in dense shade are an exception, as they produce only bulbils during the flowering season.
Development of the inflorescence
Titanotrichum oldhamii is a persistent rhizomatous herb. Several shoots can arise from the rhizome, and during early vegetative growth, a pair of two unequal leaves is produced at each node, resulting in a decussate phyllotaxy typical of the Gesneriaceae and other Lamiales such as Antirrhinum (Carpenter et al., 1995
; Vincent et al., 1995
). When it enters the reproductive phase, it converts to spiral phyllotaxy, in which a single "floral" meristem initiates at each node, with a single bract. In most related plants, such as Antirrhinum, these floral primordia would develop straightforwardly into flowers with whorls of floral organs arising from the meristems sequentially (e.g., Bradley et al., 1996a
). However, in Titanotrichum the developmental fate of these meristems is labile, changing during the season. Three different fates can be observed at the apex of the inflorescence (Fig. 3): (1) flower formation (Fig. 3B), (2) bulbil formation (Fig. 3E), and (3) bracteose proliferation (Fig. 3H). Transitional states and reversals are also seen, suggesting that the meristems are uncommitted in very early development.
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). If meristems switch to bulbil production and bracteose proliferation, shoot apex organogenesis appears more compressed. Bulbil primordia are distinguishable from true floral primordia shortly after the "loaf" stage (node 5–7) (Fig. 3C, F, I), as the "pentagon" stage does not form. Instead, in bulbil development, three subsidiary meristems form (node 9–10) (Fig. 4E, F: m1–m3). In bracteose proliferation, more than two bract primordia initiate (Fig. 4I–L, 
+ ß).
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Development of bulbil clusters and the phenomenon of bracteose proliferation
The floral meristems of T. oldhamii can apparently convert to the production of bulbil primordia or into multibract units immediately after their two lateral bracteoles initiate (Fig. 4I, K). When primary meristems enter the bracteole-producing developmental pathway, the two bracteoles continue to enlarge, and the meristems continue to produce more bracteoles (Fig. 4L, U–X). This phenomenon we call "bracteose proliferation," and it does not lead to the production of any reproductive units. Bracteose proliferation appears to be an intermediate state between pathways for flower and bulbil production, as it entails production of bracts like those associated with flowers, but proliferation of units similar to that associated with bulbil production. In addition, bracteose proliferation usually occurs temporally between flower and bulbil production.
In contrast, the initiation of bulbils is more complicated. After the two bracteoles develop, three subsidiary meristems arise laterally to the primary meristem in the axils of the bract and bracteoles (Fig. 4F, G). Then all the meristems proliferate (two new meristems arise on the flanks of existing meristems repeatedly) to generate the numerous bulbil primordia (Fig. 4H, Q–S). Thus, each floral meristem might give rise eventually to 50–70 bulbils (Fig. 4T). Bulbils can also arise from new meristems formed in the axils of bracts and bracteoles as well as by proliferation of the main axillary meristem.
It is possible to find mixed conditions in which flowers and bulbils have both arisen from the same meristem (Fig. 5), indicating that meristems are not committed to a single pathway at initiation. One to four flowers with associated surrounding bulbils may arise from a single floral meristem (Fig. 5C–F). These multiflowered units suggest that flowers form after the development of multiple meristems characteristic of the bulbil developmental pathway, and therefore that the bulbil developmental pathway is alterable to the floral pathway, at least at an early stage of development.
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Germination of seeds and bulbils
The seeds of Titanotrichum are minute (0.6 mm long, 0.15 mm wide), narrowly ovate to spindle-shaped, with the seed coat shrunken into folds around the embryo (Fig. 6A). Seeds germinate in 7–10(–14) d at 22°C under constant climatic conditions. The germination rate is very variable but is usually about 75%. With the elongation of the hypocotyl, the radicle normally emerges through the micropylar region 7–8 d after sowing (Fig. 6D). Thereafter, the hypocotyl continues to elongate, and a ring of rhizoids is formed at the base of the hypocotyl. These rhizoids probably assist in water absorption before the primary root develops and serve to anchor the seedling (Fig. 6B, C). At 2 wk the cotyledons are fully expanded and green. Many Old World Gesneriaceae show accrescent growth of one cotyledon (anisocotyly). In Titanotrichum most of the seedlings expand their cotyledons at the same rate during their growth, although some (20–40%) had slightly unequal expansion at a very early stage of germination, apparently due to an initial difference in cotyledon size. True anisocotyly shows accrescence in one cotyledon after initial cotyledon expansion, due to the formation of a basal meristem in one cotyledon. This does not appear to happen in Titanotrichum, which is therefore strictly isocotylous. After cotyledon expansion, the primary root elongates and the first pair of true leaves is initiated (Fig. 6E). Although the adult plant is densely covered with multicellular hairs, the seedling has a few glandular hairs only.
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95%. Bulbil germination in Titanotrichum is somewhat different to that of seedlings. Each bulbil has two "storage" bracts and oil bodies are visible in this tissue as droplets within the cells (in cross section under the light microscope). These bracts form a V-shape at the top of a short "bract stem" (Fig. 6F). In comparison to the seed, it is relatively large (1.5 mm long, 0.5 mm wide). When a bulbil is about to germinate, it forms a ring of rhizoids to take up water (like those in true seedlings) (Fig. 6G, H). Then, on the side of the bract stem, a root primordium begins to initiate (Fig. 6H). Furthermore, a first pair of leaves ("bulbil leaves") start to develop between the two storage bracts (Fig. 6I). The bulbil leaves continue to grow on an elongating "bulbil internode" (Fig. 6I). A second pair of leaves arises from the apical meristem between the bulbil leaves 1 wk after the start of germination (Figs. 6J, 7).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The meristem plasticity of Titanotrichum is perhaps unsurprising because the Gesneriaceae as a whole displays unusually variable meristem behavior. Some genera of the Gesneriaceae, such as Streptocarpus (Jong and Burtt, 1975
; Möller and Cronk, 2001
), vary enormously in basic morphology. Three major growth forms occur in Streptocarpus: caulescent, unifoliate, and rosulate (Jong and Burtt, 1975
). Unifoliates have no shoot apical meristem. Instead, they have a single cotyledon with a basal meristem and a separate meristem in the midrib. The variable behavior of the vegetative meristem in Streptocarpus is uncoupled from that of the reproductive meristems, however. Reproductive meristems remain unchanged, producing normal pair-flower cymes like other members of the Gesneriaceae.
Developmental switches and meristem transitions
Developmental and genetic studies on meristem behavior in mutants of Antirrhinum and Arabidopsis provide cases analogous to that in Titanotrichum. For instance, the squamosa (squa) mutant of Antirrhinum majus L. is characterized by excessive formation of bracts and the production of fewer and deformed flowers (Huijser et al., 1992
). Similarly, the floricaula (flo) mutant of Antirrhinum, homologous to the leafy (lfy) mutant of Arabidopsis, produces indeterminate shoots bearing further bracts (instead of flowers) in the axils of bracts (Coen et al., 1990
). These phenotypes combined (as in the flo/squa double mutant) are similar to the bracteose proliferation form in Titanotrichum. The development of the floral meristem in the squa or flo mutant is similar to the wild type until the loaf stage, but the meristem then fails to form sepals in a whorl. Instead, bracteole primordia form at the end of the loaf structure. This meristem may give rise to an indeterminate inflorescence with a spiral array of bracteoles (flo) or remain with two lateral bracteoles plus two ventral primordia without floral parts (squa).
Because these phenotypes are artificial mutations, they are not developmentally plastic as in Titanotrichum. Nevertheless, the similarity of developmental stages in both flo and squa with the bracteose proliferation form of Titanotrichum is striking (Figs. 4X, 8). Thus Gesner-FLO and Gesner-SQUA may be candidate genes for the regulation of the bracteose proliferation phenotype in Titanotrichum.
The cluster of bulbil primordia produced at one floral meristem can be likened to a compressed inflorescence side branch (Fig. 4G). Again the Gesner-FLO gene may play a role in this because FLO promotes transitions between floral and vegetative (branching) phases. Moreover, the TERMINAL FLOWER-1 (TFL-1) gene of Arabidopsis (Araki, 2001
) and the homologous CENTRORADIALIS (CEN) gene of Antirrhinum are known to influence whether the inflorescence is determinate or indeterminate (Bradley et al., 1996b
). Overexpression of TFL-1 in Arabidopsis results in a prolonged vegetative phase and a highly branched inflorescence (Ratcliffe et al., 1998
; Schmitz and Theres, 1999
). Similarly, work on meristem reversion of Impatiens suggests that FIMBRIATA (FIM) affects the formation of the whorled phyllotaxy and defines the boundaries of different organ-identity genes (Pouteau et al., 1998a
). Environmental changes can cause the Impatiens balsamina L. flower axis to revert back to a vegetative meristem, resulting in deformed flowers and leaves (bracts) (Pouteau et al., 1997
, 1998b
). Floral meristems in Impatiens can therefore also adopt different fates.
Bulbil formation is scattered widely in angiosperms. Many species, such as Saxifraga cernua (Saxifragaceae), Ranunculus ficaria (Ranunculaceae), and Remusatia vivipara Schott (Araceae) share with Titanotrichum the ability to initiate bulbils in place of the floral meristem (Kerner, 1904
). Mimulus gemmiparus too, although it produces its propagules from lateral meristems (the distal axillary bud adjacent to the floral bud), has an essentially similar pattern of development (Moody et al., 1999
). Thus there may be an analogous developmental switch common to bulbil formation in diverse species. Titanotrichum is unusual in that this developmental switch incorporates successive meristem divisions to produce numerous bulbils from one primordium. Nothing comparable to this is found elsewhere in Gesneriaceae.
Similarity between bulbils and seedlings
With the obvious exception of the two prominent bracts, the Titanotrichum V-shaped bulbil possesses a number of similarities to the seeds. On "germination," a pair of bulbil leaves arises on an elongated bulbil-internode (Fig. 6I). Root initiation in the bulbil is secondary (the root primordium grows endogenously from the side of the bract stem). On the other hand, the seed germinates with a true radicle (primary root), which is persistent in Titanotrichum, although the development of a secondary root seedling, after primary root abortion, is common in many other Old World Gesneriaceae species (Fig. 6D and E). There is no "anisocotyly" in bulbil germination, the bract and leaf pairs produced on germination being equal. Wang et al. (2002)
recently observed seedlings from two individuals of T. oldhamii and concluded that it is anisocotylous. Our observations have not revealed any differential growth of the cotyledons after initial expansion, resulting from the action of a basal meristem (anisocotyly). The initial expansion may however be slightly unequal. To clarify this, it would be useful to examine whether there is an unequal cell division rate in the two cotyledons, as demonstrated by Tsukaya (1997)
in Monophyllaea.
Moody et al. (1999)
, following Troll, defined the vegetative propagules of Mimulus gemmiparus as brood bulbils (with storage in the leaf component), distinct from brood tubers (storage in the stem component). The storage bracts of Titanotrichum are part of the wide range in form of the storage organs of vegetative propagules. For instance, in Dioscoreaceae (Passam et al., 1982
) and in Globba (Zingiberaceae), the vegetative propagules are tuber-like, while in Allium (Alliaceae), globular propagules form at the base of umbel pedicels. The propagules of Saxifraga (Saxifragaceae) have enclosing bracts and replace flowers within the inflorescence. Mimulus gemmiparus (Scrophulariaceae) closely parallels Titanotrichum by possessing V-shaped storage bracts (Moody et al., 1999
). In Titanotrichum however, the whole floral meristem has been replaced by a cluster of bulbils, allowing Titanotrichum to produce large numbers of bulbils, whereas in Mimulus (Moody et al., 1999
), only one propagule arises (from the proximal axillary buds).
Ecological significance of bulbil production
Bulbil production is the common state of all natural populations of Titanotrichum when autumn approaches (at the beginning of September). Because Titanotrichum usually grows near water, these tiny bulbils disperse by flotation very easily. When attempting to trace the origin of young clonal populations along ditches or tributaries, it is always possible to locate a putative progenitor colony or plant upstream. Bulbils may also be more easily carried by animals (including humans) than seeds. The pointed storage bracts, which have long trichomes, readily catch on human clothing and probably on animal fur. Plants that regenerate from bulbils grow vigorously and establish quickly. They can produce rhizomes in a shorter period than seedlings, which is important for surviving drought or the death of aboveground growth. Although flowers are produced freely in almost all natural populations, seeds are hardly ever set. Propagation by bulbils is thus the major means of mass reproduction and dispersal for Titanotrichum in the wild, especially since seeds are rarely set, perhaps because of a lack of effective pollinators (C.-N. Wang, personal observation).
Bulbils are unusual in tropical or subtropical plants (with certain exceptions such as Remusatia vivipara). Titanotrichum is therefore interesting in being a subtropical plant that uses bulbil propagation as its main reproductive strategy. Titanotrichum often grows in dense shade in which inflorescence growth and flower production is reduced. Individuals under dense shade tend to produce more bulbils relative to flowers compared to individuals in full light. Furthermore, field observations suggest that seedlings rarely establish in deep shade, and most regeneration is by the more robust bulbil-produced juvenile plants and by rhizomatous spread.
It is notable that bulbil formation in glasshouse conditions in Edinburgh is much more pronounced than that in the wild. Almost every leaf axil initiates a bulbil inflorescence resulting in massive bulbil production. We attribute this to low glasshouse temperatures (18°C maximum) and to the rapid decline of daylength after mid-autumn that occurs in Edinburgh. From observations in the wild and from examination of herbarium specimens collected in autumn and winter in Taiwan, the situation in the wild is less marked, and bulbiliferous inflorescences do not so dramatically replace normal flowers and vegetative shoots.
Significance of bulbil production for conservation
Seed set is very low in natural populations of Titanotrichum in Taiwan, adjacent regions of China, and the Ryukyu Islands of Japan, which suggests that bulbil production is the major reproductive strategy for nearly all populations despite regular flower production. In the open, large bees and butterflies sometimes visit the flowers. However, in deep shade, insects rarely visit Titanotrichum flowers, even though other flowering plants nearby, such as Begonia spp., are regularly visited by pollinating insects. Although sexual reproduction appears to be infrequent, occasional seed set and gene flow between populations may be important in maintaining population viability. Surveys of the genetic variation within and between populations are needed in order to determine the extent of clonality and ascertain whether the genetic variation is lower in marginal or threatened populations.
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FOOTNOTES |
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3 Present address: UBC Botanical Garden and Centre for Plant Research, University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
4 Reprint requests: botwang{at}ntu.edu.tw
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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 F. Tooke, M. Ordidge, T. Chiurugwi, and N. Battey Mechanisms and function of flower and inflorescence reversion J. Exp. Bot., October 1, 2005; 56(420): 2587 - 2599. [Abstract] [Full Text] [PDF]
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 C.-N. WANG, M. MOLLER, and Q. C. B. CRONK Population Genetic Structure of Titanotrichum oldhamii (Gesneriaceae), a Subtropical Bulbiliferous Plant with Mixed Sexual and Asexual Reproduction Ann. Bot., February 1, 2004; 93(2): 201 - 209. [Abstract] [Full Text] [PDF]
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= bracteoles (first, second, and third pairs, respectively). In the production of bulbil clusters, the floral meristem has been divided into terminal and three subsidiary meristems, which are denoted by TM, M1, M2, and M3. See text for explanation. Bars = 100 µm. (M–X) Later stages of developing floral meristems. (M–P) Flower formation; (Q–T) bulbil proliferation; (U–X) bracteose proliferation. Abbreviations: C = petals, S = stamen, St = staminode, G = gynoecium. In bulbil cluster formation, the terminal (TM) and three subsidiary meristems (M1–M3), eventually form four major primordia (P0–P3) for clusters of bulbils. In bracteose proliferation, a fourth pair of bracteoles are formed (
), in addition to 
