Journal of Integrative Plant Biology 2006, 48 (10): 1197−1203
Floral Ontogeny of Two Species in Magnolia L.
Feng-Xia Xu*
(South China Botanical Garden, the Chinese Academy of Sciences, Guangzhou 510650, China)
Abstract
Floral ontogeny is described in two species of genus Magnolia (Magnoliaceae), Magnolia albosericea Chun et C. Tsoong, and M. amoena Cheng, representing subgenus Magnolia and subgenus Yulania in Magnolia, by using scanning electron microscope (SEM). The sequence of initiation of floral organs is from proximal to distal. The three distinct outermost and middle organs are initiated in sequence, but ultimately form a single whorl, thus their ontogeny is consistent with a sepal interpretation. The last three tepals (petals) alternate with the preceding tepal whorl. The members of androecium and gynoecium arise spirally, although the androecium shows some intermediacy between a spiral and whorled arrangement. The car- pel primordia initiate in group of four to five. The order of stamen initiation within each tier is not determined. The floral ontogeny is remarkably homogeneous between the subgenus Magnolia and subgenus Yulania that does not support the resuming of genus Yulania.
Key words: floral ontogeny; Magnolia albosericea; Magnolia amoena; subgenus Magnolia; subgenus Yulania.
Xu FX (2006). Floral ontogeny of two species in Magnolia L. J Integr Plant Biol 48(10), 1197−1203. doi: 10.1111/j.1672-9072.2006.00341.x; available online at www.blackwell-synergy.com, www.jipb.net
Magnoliaceae has been considered to be one of the earliest and Magnolieae, including Magnolia, Manglietia, Michelia, and flowering plant. This family is a well-defined and horticulturally six smaller genera. Subsequent authors have proposed sev- important basal angiosperm family of about 230 species of trees eral different infrafamilial taxonomic schemes, but all of them and shrubs characterized by large flowers with numerous divide the family into two subfamilies, of which one, tepals and fertile parts inserted separately on an elongated Liriodendroideae, includes the sole genus Liriodendron, and axis. More than 80% of species of Magnoliaceae are distrib- the other, Magnolioideae includes a variable number of genera. uted in subtropical and tropical regions of eastern Asia; the Law’s (Law 1984) Magnolioideae included two tribes: remainder occurs in America, indicating a relictual tropical dis- Magnolieae, with terminal flowers, and Michelieae, with axil- junction (Azuma et al. 2001). Renewed debate on the system- lary flowers. Nooteboom (1985) and Cheng and Nooteboom atics of the family has been stimulated by several recent cla- (1993) reduced genera of Magnolioideae first to six genera distic analyses, both morphological (Li and Conran 2003) and (Cheng and Nooteboom 1993) and later to two, and discarded molecular (Shi et al. 2000; Kim et al. 2001), but several out- all tribes and subtribes (Nooteboom 2000). standing questions remain. The large magnolia flower was once considered to repre- Dandy (1927) proposed the first comprehensive taxonomic sent the primitive floral type (the Ranalian hypothesis), based treatment of Magnoliaceae, which recognized ten genera dis- mainly on the existence of many fossil forms. However, recent tributed in two tribes: Liriodendreae (sole genus Liriodendron) improved understanding of phylogenetic relationships, together with new fossil discoveries, have demonstrated that small flow- ers with relatively few organs predominate in basal Received 10 Apr. 2006 Accepted 16 Jun. 2006 angiosperms; the large flowers of Magnoliaceae are now nor- Supported by the National Natural Science Foundation of China (30370108 mally regarded as relatively specialized within this grade (for and 30000011) and the Guangdong Provincial Natural Science Foundation reviews see Crane et al. 1994; Endress 1994). Earlier work on of China (5006764). floral ontogeny in Magnoliaceae includes investigations of the * Tel: +86 (0)20 3725 2661; Fax: +86 (0)20 3725 2831; E-mail:
light microscope (LM), of which the spatial reconstruction was carpels are initiated in groups at slightly different levels around obtained by comparing sections afterwards. van Heel (1981, the periphery of the apex. The members of each group of or- 1983) only described the carpel development in Magnolia gans are initiated closely in time. stellata Sieb. et Zucc. and Michelia montana Blume under SEM The three outer tepals are initiated in sequence but ultimately based on bigger flora buds, but unfortunately did not have form a single whorl. At this stage, the shape of the floral access to primordial stages. A brief floral ontogeny in primoridum changes circular form to triangular. The second Liriodendron tulipifera L. and Magnolia denudata Desr. was whorl of three semicircular tepal primordia are initiated at the also included (Erbar and Leins 1994; Leins and Erbar 1994; tips of the three angles formed by the triangular floral primor- Leins 2000). Little information about the early flora apex and dium and alternate with the outer tepal whorl. One of them is initiation of perianth and stamens was provided in their studies. initiated slightly earlier than the other two. Similarly, the inner- A floral ontogenetic investigation could provide more charac- most third whorl of three perianth primordia differ slightly from ters for discussing the relationships of the family. Here floral one another in time of initiation and alternate with those of the ontogeny of subgenus Magnolia and subgenus Yulania were middle whorl and hence are opposite those of the first whorl examined in detail, in order to fill the gaps in our current knowl- (Figures 6–8). Thus, the tepals are initiated in spiral acropetal edge of the family and place them in a systematic context. succession, but are trimerously whorled; the internodes be- tween petals seldom elongate. There is a considerable differ- ence in size between primordia of the first and the second Results whorl during early stages. Following completion of tepal initiation, the central floral primordium is more or less circular. Floral morphology Stamen primordia are initiated slightly later than the third whorl of perianth primordia. One or two stamen primordia arise oppo- Flowers are solitary, bisexual, and haplomorphic, i.e. with spi- site the first tepal primordial (Figure 9). Stamens are initiated rally arranged organs inserted separately onto an elongated acropetally, successively and rapidly around the base of the axis. A ring of three bract-like structures surrounds the flower; apex (Figures 10–14). We could never observe a regularly spi- these are normally interpreted as sepals. The perianth con- ral sequence of stamen primordia. The order of stamen initiation sists of normally nine free tepals which surround numerous within each tier is not determined. During stamen development, free stamens and carpels respectively (Figures 1, 2). the floral apex displays its greatest height and diameter. When all stamen primordia have been initiated and begun to Floral development broaden, the remaining floral apex becomes slightly flatter. Some rounded bulges are initiated in groups of four to five, which are At initiation, the floral apex is circular (Figures 3, 4) in two larger than the stamen primordia (Figures 15, 16). Carpel pri- species examined, and subsequently develops three sepals mordia are free and initiated alternately in acropetal succession. surrounding a triangular floral primordium (Figures 5, 6). During During carpel initiation, the floral apex gradually diminishes in subsequent floral development the shape of the floral apex height and diameter. There is no differentiation of stigma and varies from flat during perianth initiation to highly convex at style at this stage. In older buds of two species examined here, later floral stages. The later convex shape of the apex is main- stamens and carpels are arranged spirally on the flower axis tained through appendage initiations. Tepals, stamens and (Figures 17, 18).
→
Figures 1–8. Mature flowers and development of the tepals (SEM).
1. Flower of Magnolia albosericea Chun et C. Tsoong. 2. Flower of M. amoena Cheng. 3. Floral apex of M. albosericea. 4. Floral apex of M. amoena. 5. Differentiation of three outer tepals surrounding the triangular floral apex (M. albosericea). 6, 7. Differentiation of the second tepal whorl, one slightly earlier than the other two (M. amoena). 8. Differentiation of the third tepal whorl (M. albosericea). f, floral apex; t1, tepal of first whorl; t2, tepal of second whorl; t3, tepal of third whorl. Bars, 100 µm. Floral Ontogeny of Two Species in Magnolia 1199 1200 Journal of Integrative Plant Biology Vol. 48 No. 10 2006
Figures 9–14. Development of stamens (SEM).
9. Differentiation of stamens, opposite the first tepal primordia (arrow) (M. albosericea). 10. Differentiation of stamens (M. amoena). 11, 12. Acropetal differentiation of stamens. At this stage the floral apex reaches its greatest height and diameter (M. albosericea). 13, 14. Acropetal differentiation of stamens (M. amoena). f, floral apex; s, stamen primordium; t2, tepal of second whorl; t3, tepal of third whorl. Bars, 100 µm. Floral Ontogeny of Two Species in Magnolia 1201
Figures 15–18. Development of carpels (SEM).
15, 16. Differentiation of carpels, showing carpel primordia initiated alternately, and in groups of four to five (M. albosericea). 17, 18. Older stage of flower bud, showing spiral arrangement of stamens and carpels (17, M. albosericea; 18, M. amoena). c, carpel primordium; f, floral apex; s, stamen primordium. Bars, 100 µm, except in Figure 17 (Bar, 30 µm).
Discussion the floral apex subdivided simultaneously into numerous small plaques, which implied that no further apical growth occurs in Plantefol (1948) suggested two hypotheses concerning the the floral apex. As described above, it is obvious that apical placement of petals, stamens and carpels on the receptacle. growth continues during floral development in Magnolia, but One was that the “generative centers” proliferate at the level the floral apex gradually diminishes in diameter and height dur- of the petals to produce many “floral helices”. This inferred that ing carpel initiation. The results correspond with Tucker’s (1961) apical growth continues in the flower. Another suggestion was observations on Michelia fuscata. Thus, the flower of that after petal initiation, the remaining productive surface of Magnoliaceae is not a “true” determinate structure, since it does 1202 Journal of Integrative Plant Biology Vol. 48 No. 10 2006
not terminate in an organ or organ whorl, as in typical eudicot 10 : 5). For scanning electron microscope (SEM) examination, flowers. Rather, the floral meristem achieves determinacy by buds were dehydrated in an ethanol series. Dehydrated mate- gradual diminution (Tucker 1960), as with the indeterminate rial was then critical-point-dried using a Baltec CPD 030 critical apex of racemose inflorescences. point drier, mounted onto SEM stubs using double-sided adhe- Genus Yulania Spach was established by Spach in 1839. It sive tape, coated with platinum using an Emitech K550 sputter was later treated as subgenus or section in genus Magnolia coater, and examined using a JEOL cold field emission JSM- (Dandy 1950). Recent researches revealed that subgenus 6360LV at 4−5 kV. Yulania has a closer relationship with genus Michelia instead of Magnolia (Figlar 2000). Fu (2001) and Gong et al. (2001) suggested that the genus Yulania should be resumed based on Acknowledgements morphological differences and procreant insulation. However, floral ontogeny is remarkably homogeneous between these two The author appreciated Dr Paula Rudall and Mrs Chrissie Prychid subgenera. The similarity exists both in the style and the se- in Royal Botanic Gardens, Kew for their supervision and kind quence of the initiation of all floral parts. These results support help in the laboratory. the classification that genus Mangolia consists of subgenus Magnolia and subgenus Yulania. Based on the observation, tepals arranged in a more or less References whorled structure surrounding more or less spirally arranged fertile organs, although the androecium show some interme- Azuma H, Garcia-Franco JG, Rico-Gray V, Thien LB (2001). Mo- diacy between a spiral and whorled arrangement. 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