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Floral morphology and organogenesis in Tinantia pringlei, along with a review of floral developmental variation in the spiderwort family, Commelinaceae.

Introduction

Floral organogenesis in the spiderwort family, Commelinaceae, has previously been investigated in 11 species from eight of 42 genera, three of nine subtribes or their equivalent, and two of three tribes in the family (Hardy & Stevenson, 2000a, b; Hardy et al., 2000, 2004, 2009; Masters, 1872; Payer, 1857; Rohweder, 1963; Stevenson & Owens, 1978). Although many of these investigations were carried out to assess homology or to investigate the developmental basis for certain interesting morphologies or pollination syndromes peculiar to particular species or genera, it now appears that there are variations in development that could be employed to assess homology and phylogenetic relationships at larger taxonomic levels such as subtribal and tribal relationships. This article is intended to review these developmental variations, as well as to document, for the first time, the developmental morphology of the flowers from a member of the heretofore uninvestigated subtribe Thyrsantheminae (sensu Faden, 1998), Tinantia pringlei (S. Watson) Rohweder.

The Mesoamerican subtribe Thyrsantheminae includes just 21 species, but contains nearly the full range of morphological and ecological diversity in the family: from fully open to tubular flowers, cleistogamy to chasmogamy, spreading stoloniferous plants to compact rosettes, and from habitats at sea level to 3,000 m in elevation. Although the following study focused on Tinantia, future studies will be aimed at doing the same for other genera of the subtribe, as well as other confamilial subtribes which have not yet been investigated as such.

Tinantia Scheidweiler consists of ca. 14 species distributed from Texas in the southern United States of America to tropical America, and is especially diverse from Mexico to Nicaragua (Faden, 2000). Tinantia pringlei is a Mexican, perennial species commonly found cultivated or growing as a weed in greenhouses in the Northern Hemisphere. The leaves of this species are spotted red to purple above and uniformly purple below (Fig. 1a, b). Flowers are of two main types: chasmogamous flowers from the upper nodes, and cleistogamous flowers from nodes near or below ground level (Hunt, 1975). The cleistogamous flowers arise from usually short, single-flowered inflorescences that perforate the leaf sheaths of the leaf axils they arise from. The chasmogamous flowers arise from multi-flowered, single-cymed thyrses that do not perforate their leaf sheaths. Chasmogamous flowers, the subject of our study, are complex in form, nectarless, monosymmetric, and consist of three blue and three showy, yellow stamens (Figs. 1 and 2; see also Hunt, 1975). Although it has been suggested that the showy, yellow stamens of Tinantia generally may function in providing fodder pollen for pollen-foraging insects in a deceptive pollination system (e.g., Vogel, 1978; Faden, 1992), studies in the related T. anomala have not found strong evidence for this (Simpson et al., 1986), and it appears that these two species are both self-compatible. Further evidence from cultivated sources suggests that sexual reproduction in T. pringlei is achieved frequently and perhaps exclusively through selfing (see also Hunt, 1975).

Materials and Methods

Aerial inflorescences consisting of chasmogamous flowers of varying ages were collected for study from plants of Tinantia pringlei cultivated in the greenhouse of the Millersville University Department of Biology from November 2007 through January 2008. Voucher collections were deposited in the James C. Parks Herbarium (MVSC sensu Holmgren & Holmgren, 1998). These living collections were preserved in FAA (formalin: acetic acid: ethanol; 1:1:8 v/v) and then transferred to 70 % ethanol. Some specimens were then dissected under a dissecting microscope (Olympus SZH10) and then prepared for critical point drying. Other specimens were first critical-point-dried, mounted onto aluminum SEM stubs, and then dissections were carried out through the following technique ingeniously developed by one of us, Jason Ryndock. SEM specimen mounting glue or the adhesive from double-side mounting tape was placed onto the tip of a forcep, and this sticky forcep tip was then used to pull bracteoles, sepals, or petals of the flower bud with greater precision than was possible without the adhesive method.

All specimens were prepared for critical-point-drying by placing them into perforated plastic carrying boats and run through a dehydration series from 70-80 to 93-100 % ethanol, followed by substitution with acetone as follows: 100 % ethanol to 50/30 ethanol/ acetone, then to 100 % acetone. This plant material was then critical-point-dried using a Polaron E3000 and C[O.sub.2]. These specimens were then sputter-coated with gold using a Denton Vacuum Desk II sputter coater. Floral organogenesis was documented using an Amray 1820 scanning electron microscope at Millersville University.

Results

Floral Morphology. The aerial, chasmogamous flowers of Tinantia pringlei are strongly monosymmetric (Figs. 1c and 2) and are open for less than a single day. The calyx is weakly monosymmetfic with three subequal, keeled, pale green sepals tinged distally with purple. Microscopic glandular microhairs (Tomlinson, 1966) occur on both the adaxial and abaxial lamina of the sepals, whereas short uniseriate trichomes occur on the margins and relatively long uniseriate trichomes occur distally along the abaxial midrib (Figs. 2b, 3i). In bud, the sepals are imbricate, with the margins of one sepal (the upper) lying completely outside the others and those of another (one of the lower sepals) lying completely inside. The corolla is weakly monosymmetric with three subequal, blue petals (Figs. 1c, 2a). After floral opening, the petals are at first concave (Fig. 2b) and then convex (Fig. 2a) before senescing by the end of the first and only day that they are open. In bud, the petals are imbricate, with the margins of one petal (the lower) lying completely outside the others and those of another (one of the upper petals) lying completely inside.

The androecium consists of six stamens of three types as follows. There are three short, central, upper stamens inserted opposite the upper petals and upper sepal. These stamens bear pale yellow anthers on filaments that are basally blue, distally white, and bearded by yellow moniliform trichomes (Figs. 1d, g, 2, 3c, g). There are two long, lateral, upper stamens that are, although appearing largely in the upper half of the flower, actually inserted opposite the lower sepals (Figs. 1, 2). These stamens bear blue anthers on blue filaments that are bearded just proximal of center by moniliform trichomes, which are basally blue and distally pale blue (Fig. 1). The last of the stamens is the long, medial, lower stamen inserted opposite the lower petal (Figs. 1c, e, 2). This stamen has a single blue anther on a blue, glabrous filament. The short, central, upper stamens are connate by their filament bases (Figs. 1c, d, 3d). The filaments of the long, lateral, upper stamens are slightly connate basally to those of the short, central, upper stamens (Fig. 3d). All stamens are apparently fertile, and observations of the contents of pre-dehiscent anthers (Fig. 3h) indicates the occurrence of what are probably tapetal raphides, which also are known from other commelinaceous genera and several other related families (Hardy & Stevenson, 2000a, b; Hardy et al., 2000, 2004; Prychid et al., 2003).

The gynoecium consists of three connate carpels forming a single pistil differentiated into a 3-lobed, white ovary, a single upwardly curved, blue style, and a single capitate, papillose, pale-yellow stigma (Figs. 1c, h, 2b, 3e). The ovary is covered by microscopic glandular microhairs (Figs. 1h, 3a, f), but is otherwise glabrous.

Organogenesis. The calyx is the first whorl of organs to emerge, with the upper sepal first, followed by the simultaneous emergence of the lower sepals (Fig. 4a, b). The upper sepal is the largest of the sepals, especially early in floral development (Fig. 4a-g), and will come to envelop the margins of the lower sepals in bud (Fig. 3a-b). Trichomes form on the upper sepal first, with the uniseriate trichomes along the keel emerging before the glandular microhairs (Fig. 4f). The cilial trichomes of the distal margins are the last to emerge (Fig. 3a). The time interval between emergence of uniseriate trichomes and glandular microhairs is contracted and difficult to discern for the lower sepals.

Following the emergence of the sepals, the floral apex is flat to slightly convex and no other organs have yet emerged. Then the first petal emerges (Fig. 4b), followed by the simultaneous or nearly simultaneous emergence of the remaining petal primordia (Fig. 4c-d). The petal primordia are soon crescent-shaped (Fig. 4c-g) and all are similar in size, although the lower petal primordium is more strongly curved than the upper petal primordia early in development (Fig. 4g). By the time they have become laminar, all petals are similar in size and shape to one another (Fig. 4h-i). The margins of the lower petal will eventually come to envelop the lower margins of the upper petals in bud.

Emergence of the androecium commences with the lower two stamens of the outer androecial whorl (i.e., the long, lateral, upper stamens). In fact, these stamen primordia apparently emerge simultaneously with the remainder of the petal primordia as described above (Fig. 4c-f). The third androecial primordium to emerge is that of the long, lower stamen, which belongs to the inner androecial whorl (Fig. 4e-f). The next to emerge are the primordia of the lateral pair of the short, central, upper stamens, these belonging to the inner androecial whorl (Fig. 4e). The sixth and last stamen primordium to emerge is that of the central member of the upper stamens (Fig. 4g). This stamen will be conspicuously smaller than the other stamen primordia for a substantial period of early development and will be the last of the stamens to differentiate into filament and anther (Figs. 4g-h, 5a-b). Anther differentiation commences with the primordia in the lower floral hemisphere first, as each primordium first becomes dorsiventral and then distally 2-lobed--the two lobes representing the incipient two thecae per anther (Fig. 4g-i). Emergence of the moniliform trichomes on the filaments will not commence until the start of style differentiation in the young gynoecium (micrographs not shown, but occurring between the phases of growth captured in Fig. 5e and f). The stamens of the lower floral hemisphere are the largest of the six throughout the entirety of development (e.g., 4G-I) through maturity (Fig. 2).

Following emergence of all stamen primordia, the floral primordial apex is flat. Expansion of the apex appears retarded as compared to the growth of the surrounding organs and floral bud generally (Figs. 4g-i, 5a). The three carpels emerge nearly simultaneously with one another at the points of the flat, triangular apex (Fig. 5b). To see their emergence, the surrounding calyx, corolla, and androecium must be mechanically removed (e.g., compare Fig. 4i with Fig. 5a and b). The carpel primordia quickly become crescent shaped and, although at first separate, they are soon congenitally fused (Fig. 5c-e). Differentiation into ovary, style, and stigma begins concomitantly with formation of trichomes on the stamens (cf. Fig. 5f).

Discussion

Perianth Organogenesis

Floral development in Tinantia pringlei begins, as in all Commelinaceae taxa investigated thus far, with the apparently precocious emergence and rapid growth of the upper (or outer) sepal, followed by the lower two (or inner) sepals, which emerge substantially later and grow substantially slower than the upper sepal (Payer, 1857; Masters, 1872; Stevenson & Owens, 1978; Hardy & Stevenson, 2000a, b; Hardy et al., 2000, 2004, 2009). Tinantia flower development also is consistent with what appears to be the norm for commelinaceous taxa with monosymmetric flowers--with the upper sepal being the largest and earliest-maturing of the three sepals throughout the entirety of development. Only in Tradescantia and Callisia, both of which have polysymmetric flowers, do the lower sepals quickly approach the upper in size and rate of maturation, such that the calyx is essentially polysymmetric throughout development (Table 1; Hardy & Stevenson, 2000b).

Corolla development also begins as in all other commelinaceous taxa yet studied in a similar manner, with the nearly simultaneous initiation of the petal primordia. Further growth and development of all three petals in T. pringlei proceeds in a uniform (polysymmetric) manner, resembling the uniform petal development known for the polysymmetric flowers of Tradescantia and Callisia (Table 1; Hardy & Stevenson, 2000b). This is in contrast to the development documented previously for other confamilial taxa with monosymmetric flowers (Table 1), even when the mature three petals are all nearly equal in size, where there is a marked dimorphism between the upper and lower petals during early and middle phases of development (i.e., the developing lower petal is much larger than the upper petals in Cochliostema, Hardy & Stevenson, 2000a, Commelina, Hardy et al., 2009, Dichorisandra, Hardy et al., 2000, and Plowmanianthus, Hardy et al., 2004; summarized as such in Table 1).

The report by Parks (1935) of the delayed emergence of the petals until after the first stamens in T. pringlei was not verified in our study. We surmise that this discrepancy may be accounted for by Parks's study being based on the subterranean cleistogamous flowers of T. pringlei, whereas our study was of the chasmogamous flowers from the upper nodes of the aerial shoots. The petals of cleistogamous flowers are much smaller than those of chasmogamous flowers and have relinquished their function of pollinator visual attraction; thus, we were not surprised that petal development is in some respects anomalous in the cleistogamous flowers of T. pringlei.

Androecial Organogenesis

Although the stamens typically emerge and mature in a nearly simultaneous manner throughout the family, certain taxa exhibit discernibly centripetal patterns of development while others exhibit discernibly centrifugal patterns (Table 1). Flowers of Tinantia pringlei exhibit the former pattern. Indeed, the centrifugal development seen in Tradescantia and Callisia (Table 1) are unusual for flowers generally, and future similar studies of additional species of Tradescantia, Callisia, and close relatives such as Tripogandra should be undertaken to determine the phylogenetic extent to which this developmental variation occurs.

The relative rates of development of the stamens in T. pringlei also are correlated with the relative sizes of the stamens at anthesis. The stamens of the lower floral hemisphere are the first to emerge and are the largest throughout development as well as at maturity. The next stamens to emerge are the lateral upper stamens (those opposite the upper petals), followed by the medial upper stamen (that opposite the upper sepal), which is slightly smaller than the lateral upper stamens at maturity.

Gynoecial Organogenesis

The carpels in T. pringlei emerge from the floral primordium initially as three separate, rounded primordia. These primordia soon become crescent-shaped and, although initially separate, further development is congenital as a common gynoecial primordium. Unlike in most other confamilial genera for which similar studies have been performed, these carpels do not emerge while the stamen primordia are still small, prior to differentiation of the stamens into anther and filament; rather, the carpels appear delayed in their emergence, not appearing until after stamen differentiation has begun (Table 1). This is similar to the timing documented for carpel emergence in Tradescantia and Callisia. Despite these similarities with Tradescantia and Callisia, the floral apex on which the carpels emerge in Tinantia is flat, and therefore more like confamilial genera other than Tradescantia and Callisia. As reported in Table 1, the floral apex upon which the carpels emerge in Tradescantia and Callisia is distinctively raised. Future studies should be aimed at investigating floral organogenesis for other genera of the subtribe, as well as other confamilial subtribes which have not yet been investigated in such a manner.

Conclusions

Development of the chasmogamous flowers of Tinantia pringlei is largely a unique combination of developmental patterns already known for other commelinaceous taxa. Because some of this developmental variation in the family is not expressed in mature flowers (i.e., Table 1), these variations may prove useful for homology assessment and similarly-oriented phylogenetic studies within the Commelinaceae.

Acknowledgments This article is dedicated to Dr. Dennis Wm. Stevenson, academic mentor and dear friend of the first author of this article. Dennis Stevenson was notably influential in introducing the first author to the study of floral morphology and development in the Commelinaceae and monocots generally, as well as to the microscopic techniques employed here. It is indeed fitting that the current study represents a collaborative effort, in much the same tradition, on the part of the first author and one of his own students, Jason Ryndock. In addition, the biologist and illustrator responsible for Fig. 1, Zel Stoltzfus, also is a former student of the first author.

Financial support for this study came from the Millersville University Department of Biology and an Arthur and Claribel Gerhart Scholarship award to Jason Ryndock. To that end, we appreciate Susan DiBartolomeis and James Mone for their service on the Gerhart Scholarship Selection Committee. David Dobbins and Mafia Schiza provided invaluable assistance through their efforts in the maintenance of the scanning electron microscope. The plants used in this study were generated from stem cuttings originally donated by Bob and Audrey Faden out of the Smithsonian Institution's greenhouse facility. It is the maintenance of such living collections that enables this type of research.

Literature Cited

Faden, R. B. 1992. Floral attraction and floral hairs in the Commelinaceae. Annals of the Missouri Botanical Garden 79: 46-52.

--1998. Commelinaceae. Pp 109-128. In. K. Kubitzki (ed). The families and genera of vascular plants, Vol. 4. Springer, Berlin.

--2000. Floral biology of Commelinaceae. Pp 309-317. In: K. L. Wilson & D. A. Morrison (eds). Monocots. Systematics and evolution. CSIRO Publishing, Collingwood.

Hardy, C. R. J. I. Davis & D. W. Stevenson. 2004. Floral organogenesis in Plowmanianthus (Commelinaceae). International Journal of Plant Sciences 165: 511-519.

--, L. L. Sloat & R. B. Faden. 2009. Floral Organogenesis and The developmental basis for pollinator deception in the Asiatic dayflower Commelina communis (Commelinaceae). American Journal of Botany 96.

--& D. W. Stevenson. 2000a. Development of the flower, gametophytes, and floral vasculature in Cochliostema odoratissimum (Commelinaceae). Botanical Journal of the Linnean Society 134: 131-157.

--&--. 2000b. Floral organogenesis in some species of Tradescantia and Callisia (Commelinaceae). International Journal of Plant Sciences 161: 551-562.

--& H. G. Kiss. 2000. Development of the flower, gametophytes, and floral vasculature in Dichorisandra thyrsiflora (Commelinaceae). American Journal of Botany 87: 1228-1239.

Holmgren, P. K. & N. H. Holmgren. 1998 [continuously updated]. Index Herbariortma: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http:// sweetgum.nybg.org/ih/.

Hunt, D. R. 1975. Tinantia pringlei. Curtis's botanical magazine 180: 161-164. Masters, M. T. 1872. On the development of the androecium in Cochliostema, Lem. Proceedings of the Linnean Society (Botany) 13: 204-209.

Parks, M. 1935. Embryo sac development and cleistogamy in Commelinantia pringlei. Bulletin of the Torrey Botanical Club 62: 91-104.

Payer, J.-B. 1857. Traite' d'organoge'nie compare'e de la fleur. Masson, Paris.

Pryehid, C. J., C. A. Furness & P. J. Rudall. 2003. Systematic significance of cell inclusions in Haemodoraceae and allied families: silica bodies and tapetal raphides. Annals of Botany 92: 571-580.

Rohweder, O. 1963. Anatomische und histogenetische Untersuchungen an Laubsprossen und Bluten der Conunelinaceen. Botanische Jahrbucher fur Systematik, Pflanzengeschichte und Pflanzengeographie 82: 1-99.

Simpson, B. B., J. L. Neff & G. Dieringer. 1986. Reproductive biology of Tinantia anomala (Commelinaceae). Bulletin o f the Torrey Botanical Club 113: 149-158.

Stevenson, D. W. & S. J. Owens. 1978. Some aspects of the reproductive morphology of Gibasis venustula (Kunth) D.R. Hunt (Commelinaceae). Botanical Journal of the Linnean Society 77: 157-175.

Tomlinson, P. B. 1966. Anatomical data in the classification of Commelinaceae. Botanical Journal of the Linnean Society 59: 371-395.

Vogel, S. 1978. Evolutionary shifts from reward to deception in pollen flowers. Pp 89-104. In: A. J. Richards (ed). The pollination of flowers by insects. Linnean Society Symposium Series No. 6. Academic, New York.

DOI 10.1007/s12229-012-9108-1

Christopher R. Hardy (1,2,4) * Jason Ryndock (3,1)

(1) James C. Parks Herbarium, Department of Biology, Millersville University, PO Box 1002, Millersville, PA 17551-0302, USA

(2) Department of Botany, MRC-166, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA

(3) Department of Conservation and Natural Resources, Bureau of Forestry, 400 Market St, PO Box 8552, Harrisburg, PA 17105-8552, USA

(4) Author for Correspondence; e-mail: christopher.hardy@millersville.edu

Published online: 10 October 2012

Table 1 Some Known Variations in the Development of Flowers in Taxa of
Commelinaceae, Subfamily Commelinoideae, Organized by Tribe, Subtribe,
then by Genus. These are Variations that are not or not Easily
Correlated with Morphology in the Mature Flowers. These Variations are
Summarized by Genus Based on Limited Sampling Within Each as Follows:
Tradescantia and Callisia is Based on the Studies of T. ohioensis, T.
virginiana, and C. navicularis by Hardy and Stevenson (2000b) and
Payer (1857), Gibasis is Based on G. venustula (Stevenson and Owens
1978) and G. geniculata (Rohweder, 1963), Cochhostenra is Based on C.
odoratissimum (Masters, 1872; Hardy & Stevenson, 2000a), Dichorisandra
is Based on D. thyrsijlora (Hardy et al., 2000), Plowmanianthus is
Based on P dressleri, P. grandi/blius, and P panamensis (Hardy et al.,
2004), and Commelina is Based on C.communis (Hardy et al., 2009)

                     Calyx Organogenesis    Corolla Oganogenesis
                     Following Initiation   Following Initiation

Tradescantieae

Tradescantiinae

Tradescantia         Polysymmetric          Polysymmetric

Callisia             Polysymmetric          Polysymmetric

Gibasis              Polysymmetric          Polysymmetric

Dichorisandrinae

Cochliostema         Monosymmetric          Monosymmetric

Dichorisandra        Monosymmetric          Polysymmetric

Plowmanianthus       Monosymmetric          Monosymmetric

Thyrsantheminae

Tinantia             Monosymmetric          Polysymmetric

Commelineae

Commelina            Monosymmetric          Monosymmetric

                     Androecial
                     Initiation Pattern

Tradescantieae

Tradescantiinae

Tradescantia         Centrifugal

Callisia             Centrifugal

Gibasis              Centripetal to
                     simultaneous

Dichorisandrinae

Cochliostema         Centripetal

Dichorisandra        Centripetal

Plowmanianthus       Centripetal

Thyrsantheminae

Tinantia             Centripetal

Commelineae

Commelina            Centripetal

                     Timing of Carpel
                     Emergence

Tradescantieae

Tradescantiinae

Tradescantia         Late (with anther differentiation)

Callisia             Late (with anther differentiation)

Gibasis              unknown

Dichorisandrinae

Cochliostema         Early (prior to anther differentiation)

Dichorisandra        Early (prior to anther differentiation)

Plowmanianthus       Early (prior to anther differentiation)

Thyrsantheminae

Tinantia             Late (with anther differentiation)

Commelineae

Commelina            Early (prior to anther differentiation)

                     Floral Apical Meristem   Ovary-Style
                     Prior to Carpels         Primordium Junction

Tradescantieae

Tradescantiinae

Tradescantia         Raised and trigonal      <90[degrees]

Callisia             Raised and trigonal      90[degrees]

Gibasis              unknown                  >90[degrees]

Dichorisandrinae

Cochliostema         Unraised and flat        >90[degrees]
                     to slightly concave

Dichorisandra        Unraised and flat        90[degrees]
                     to slightly concave

Plowmanianthus       Unraised and             >90[degrees]
                     slightly convex

Thyrsantheminae

Tinantia             Unraised and flat        >90[degrees]

Commelineae

Commelina            Unraised and             >90[degrees]
                     slightly convex
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Author:Hardy, Christopher R.; Ryndock, Jason
Publication:The Botanical Review
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Geographic Code:1USA
Date:Dec 1, 2012
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