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2Department of Environmental Population and Organismic Biology, University of Colorado,Boulder, Colorado 80309-0334, and 3Department of Biology, Colorado State University, Fort Collins, Colorado 80523
Received for publication September 18, 1998. Accepted for publication March 18, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: asexual reproduction • axillary meristem development • brood bulbil • endemic • gemmae • Mimulus gemmiparus; • Mimulus guttatus; • propagule • Scrophulariaceae • supernumerary buds
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Munz and Keck, 1959
) with a variety of life histories. The species range from annuals to herbaceous perennials to woody shrubs (Grant, 1924
; Munz and Keck, 1959
). Within this large and diverse clade, the life history of Mimulus gemmiparus W. A. Weber is unique (Weber, 1972
). Although individual genets are perennial, ramets of M. gemmiparus live for only one growing season. New ramets are produced through the formation of vegetative propagules termed gemmae (Weber, 1972
). The asexual propagules of M. gemmiparus are dispersed when the parent ramet senesces and are capable of overwintering in the soil and germinating the following spring (Beardsley, 1997
). Because sexual reproduction of M. gemmiparus is exceedingly rare, the vegetative propagules are a critical component of the unusual life history of this species (Weber, 1972
; CONPS, 1989
; Beardsley, 1997
).
The propagules of M. gemmiparus have been termed gemmae (Weber, 1972
), yet their morphological nature has not been examined. Unfortunately, the morphological nature of many dispersible vegetative propagules is rarely known. They are often referred to by terms such as bulbils, turions, or gemmae that lack precise morphological meaning. According to the classification of Troll (1937)
such propagules may be modified axillary buds (brood tubers, with storage in the stem component, or brood bulbils, with storage in the leaf component) or roots (see also Goebel, 1900
; Bell, 1991
). However, other types of propagules exist that do not fall within the traditionally recognized categories (e.g., leaf tubers of Dicentra cucullaria; Walton and Hufford, 1994
).
Developmental and morphological comparisons of novel structures, such as the gemmae of M. gemmiparus, with corresponding features in ancestral or sister taxa can provide evidence of their structural identity as well as offer insight into their origin and evolution (Bower, 1898
; Jacob, 1982
; Friedman, 1994
). There are two hypothesized progenitor species of Mimulus gemmiparus: Mimulus guttatus and Mimulus glabratus (Weber, 1972
). For the purpose of this study, we chose M. guttatus as the species for morphological and developmental comparison with M. gemmiparus because the morphology of M. guttatus is considered representative of the genus Mimulus, section Simiolus (Vickery, 1978
).
Here, we compare the morphology of M. gemmiparus with that of its putative sister taxon, M. guttatus. The comparison begins with an architectural analysis of the two species in order to formulate a hypothesis of structural correspondence between the propagules of M. gemmiparus and structures in M. guttatus. We then report a detailed developmental analysis in order to test our hypothesis of morphological correspondence and to understand the modifications of development that have occurred during the evolution of the propagules of M. gemmiparus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). M. gemmiparus is found in the uppermontane/subalpine zone at elevations ranging from 2560 to 3050 m (Weber, 1972
; O'Kane, 1988
). Typically, the populations are located under southfacing overhangs along granite seeps and springs that provide a constant supply of water (Weber, 1972
; Beardsley, 1997
). Specimens were collected on 1 July 1997 and 20 August 1997 from a natural population found along the Hankin's Gulch Trail in the Lost Creek Wilderness Area. This is the largest known population and has been estimated to have up to 100 000 individuals (Beardsley, 1997
). Following collection, plants were either cultivated or preserved for further study. Plants were cultivated with one of two methods. Some plants were placed on soil and allowed to senesce, resulting in new plants that sprouted from the propagules. Other plants were transplanted into flats of soil and allowed to grow. Half of the cultivated plants were placed on greenhouse mist tables under natural light. The remaining half were grown in a growth chamber under 100 µmol photons of illumination with 16-h days at 20°C and 8-h nights at 15°C.
Mimulus guttatus
Mimulus guttatus is distributed extensively along the western coast of North America from Alaska to Mexico and as far east as the Rocky Mountains (Vickery, 1978
). Typically, M. guttatus grows in moist meadows and along streams and springs from sea level up to 3000 m (Vickery, 1978
). Samples of M. guttatus were collected along Columbine Spring at the University of Colorado Mountain Research Station, at 2900 m elevation, on 21 August 1997. In addition, seeds were collected from senescent individuals along a drainage ditch in Pope Valley, Napa County, California on 29 May 1997 and were cultivated in growth chambers under the conditions described above.
Voucher specimens of both species were deposited in the University of Colorado Herbarium.
Microscopy
After field collection, plants were fixed in 4% glutaraldehyde in phosphate buffer at pH 7. Greenhouse and growth chamber plants were harvested at intervals and also fixed in 4% glutaraldehyde. All preserved material was carried through a standard ethanol dehydration series and stored in 70% ethanol.
Material prepared for light microscopy was dehydrated in an ethanol series to 95%, embedded in JB-4 methacrylate resin (Polysciences, Warrington, Pennsylvania), serially sectioned at 5 µm on a Microm ultramicrotome, and stained in 0.1% toluidine blue. In order to localize the site of starch storage, mature propagules were dehydrated in an ethanol series to 100%, transferred to Hemo De (Fisher Scientific, Pittsburgh, Pennsylvania), and embedded in Paraplast (Oxford Labware, St. Louis, Missouri). The propagules were serially sectioned at 8 µm and examined under cross-polarized light. Starch grains were identified by their distinctive pattern of birefringence (Esau, 1977
). Slides were examined with a Zeiss Axioskop and photographed with Fujichrome E-6 tungsten color reversal film (ISO 64) or with an Olympus Vannox AH-3 and photographed with a Sound Vision Cmos-Pro digital camera.
Material prepared for scanning electron microscopy (SEM) was serially dehydrated to 100% microsieved ethanol and critical-point dried in a Ladd critical-point dryer. Samples were then mounted on stubs with silver paste and sputtercoated with gold. These samples were viewed on a Zeiss DSM940A scanning electron microscope at 15 KV and photographed using Polaroid 55 positive/negative instant sheet film (ISO 50).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Mimulus guttatus
The average individual of Mimulus guttatus is 
35 cm in height. The main axis is monopodial with leaves arranged in an opposite and decussate phyllotaxy (Fig. 1). Leaves consist of a clasping base, a slender petiole, and an entire to slightly dentate blade. At all nodes subsequent to the cotyledons, a lateral bud is visible in each leaf axil early in development. This axillary bud can produce either a branch or flower; however, the fate of this bud typically differs between plants from the Colorado and California populations. In the Colorado population, the axillary buds at the first two basal nodes grow out plagiotropically as stolons and root at the nodes (Fig. 1). This is likely a mode of vegetative propagation in M. guttatus. Plants grown in the growth chamber (California population) do not bear stolons; rather, they produce orthotropic lateral branches at the first two or three nodes (Fig. 1). Flowers take the place of stolons and lateral branches at later, more distal nodes in both populations. Later in the development of each node, a second lateral bud appears between the first lateral bud and the leaf base. It remains unexpanded unless the first axillary meristem is damaged or dies.
Hypothesis of structural correspondence
Based on propagule position within the overall architecture of M. gemmiparus, we hypothesize that the propagule is an axillary shoot and that it corresponds to the second axillary bud initiated at each node in M. guttatus. We therefore compare the development of the multiple axillary buds at equivalent nodes of M. gemmiparus and M. guttatus.
Developmental analysis of Mimulus gemmiparus
The shoot apical meristem of the main axis initiates leaf primordia in an opposite and decussate pattern (Fig. 2). In the axils of the most recently initiated leaf primordia, evidence of a meristem is present almost immediately (Figs. 2, 3: D). The axillary meristem is a dome-shaped mass of cells in the axil of the youngest leaf primordium and has bilateral to radial symmetry (the bilateral symmetry disappears as the meristem grows beyond the petiole and the stem and is no longer compressed between the two structures; Fig. 2). A second meristem is evident shortly after the first and is located at the base of the first meristem, in the axil of the subtending leaf (Figs. 2, 4, 5: P). Both meristems have a distinctive tunica-corpus organization (Fig. 5). The two axillary meristems will be referred to as distal (first) and proximal (second). The two meristems in each leaf axil are initiated in rapid succession and close spatial proximity. Subsequent to initiation, the two meristems develop separately and have different morphological and functional fates. The proximal meristem ultimately becomes the propagule and the distal meristem produces either a lateral branch or a flower.
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Development at node 2
Axillary meristem initiation at the second node of M. gemmiparus contrasts with that observed in later nodes. The second node of a ramet bears the first pair of photosynthetic leaves. These leaves are preformed during propagule development and only reach maturity following germination. When mature, leaves at node 2 have unmodified petioles and do not bear propagules in the axils. Initially, there are no meristems present in the axils of the preformed leaf primordia. By the third plastochron, a distal meristem is initiated in each leaf axil (Fig. 19: D). This meristem ultimately becomes a lateral branch (Figs. 20, 21: D*). A proximal meristem is not initiated until approximately the seventh plastochron and is located at the base of the distal meristem in the axil of the subtending leaf (Fig. 21: P). This meristem will initiate two to three pairs of leaf primordia, but typically will remain unexpanded and quiescent in the leaf axil throughout the ontogeny of the ramet.
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Following initiation of the distal meristem, when the node is four to many plastochrons removed from the shoot apical meristem, a second meristem (the proximal meristem) is initiated in the leaf axil between the distal meristem and the leaf base (Fig. 9: P). The proximal meristem is inactive compared to the distal meristem; it may initiate one to two leaf primordia, but these remain small and immature (Fig. 10). Subsequently, the proximal meristem becomes quiescent (Figs. 1, 10) and remains so unless the distal meristem is damaged or dies.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Beardsley, 1997
), persistence of this rare species from one year to the next depends critically on the production of asexual propagules. These propagules are dispersed from the parent ramet, overwinter in a quiescent state, and produce new, physiologically independent ramets in the following spring (Beardsley, 1997
). Despite the vital importance of asexual reproduction in the life history of M. gemmiparus, the development and morphological identity of the propagules, termed gemmae, have not been previously investigated.
Morphological identity of the propagule
Architectural, morphological, and developmental analyses demonstrate that the gemmae of M. gemmiparus are axillary buds. They are located in the axils of leaves and are the products of shoot apical meristems, identified as such by both histological and morphological criteria. The meristems have the cellular organization and staining characteristics typical of angiosperms (Fig. 5; Clowes, 1961
; Esau, 1977
), are radially symmetrical in cross section, and initiate leaves as lateral appendages (Figs. 2, 11, 12; Troll, 1937
; Goebel, 1900
). Thus, the gemmae correspond positionally, anatomically, and morphologically to axillary shoots.
Axillary buds that function as asexual propagules are termed brood shoots. Two morphological types of brood shoots can be distinguished based on the location of stored nutrients (Troll, 1937
): brood bulbils have nutrient storage in leaves or leaf bases, whereas brood tubers store nutrients in the stem. Based on the presence of starch reserves in the thickened, basal pair of leaves (Fig. 13), the gemmae of M. gemmiparus are brood bulbils.
At dispersal, brood bulbils of M. gemmiparus consist of a short stem bearing two pairs of leaves and terminated by an apical meristem (Fig. 15). The basal, starch-storing pair of leaves is mature at dispersal and completely encloses the rest of the bulbil. The distal leaves are small, preformed primordia that do not complete their development until the dispersed propagule "germinates," i.e., begins to develop into a new ramet. The small stem of the bulbil also bears root primordia within the first node. The presence of preformed leaf and root primordia may facilitate rapid establishment of the new ramet following germination; root and shoot growth can begin immediately without the delay associated with the initiation of new organs.
The propagule of M. gemmiparus does not consist solely of the brood bulbil. When mature and ready for dispersal, the bulbil is enclosed by the expanded petiole of the subtending leaf, and the leaf and bulbil are dispersed as a unit. Separation of the propagule from the parent ramet typically occurs at a constricted area of relatively small cells located between the petiole and leaf base (Fig. 18). Addicott (1982)
recognizes such areas of distinctive cells as abscission zones. Development of a distinct abscission zone likely facilitates joint dispersal of the bulbil and the ensheathing petiole. Following abscission from the parent ramet, the covering provided by the petiole may prevent desiccation of the bulbil and may be important for the survival of the bulbil during winter quiescence (Beardsley, 1997
).
Comparative analysis of Mimulus gemmiparus and Mimulus guttatus
Architectural and developmental analyses clearly demonstrate that the asexual propagules of M. gemmiparus are highly modified axillary shoots. Only comparative analysis can yield insight into the evolutionary modifications of an axillary shoot that result in novel morphology and function. Although the phylogenetic relationships among species of Mimulus section Simiolus, including the position of M. gemmiparus, are unknown, M. guttatus has been suggested as a sister taxon of M. gemmiparus (Weber, 1972
) and is discussed here as representative of the plesiomorphic vegetative morphology.
Architecture
The architectures of M. gemmiparus and M. guttatus are fundamentally similar (Fig. 1). Both species have monopodial main and lateral axes, both have opposite and decussate phyllotaxy (and therefore, cladotaxy), and both produce supernumerary, serial axillary buds (Figs. 5, 9). In both M. gemmiparus and M. guttatus, the distal bud of the supernumerary pair ultimately produces a lateral branch or flower, and in both species a second bud is located between the leaf axil and the distal bud. The fate of this proximal bud, however, constitutes a critical difference between the two species. In M. guttatus, the proximal bud typically remains inactive throughout the life span of the plant, whereas the proximal bud of M. gemmiparus ultimately becomes the brood bulbil. Thus, the bulbil of M. gemmiparus corresponds positionally, but not functionally, to the dormant proximal axillary bud of M. guttatus.
Development
Because the brood bulbil of M. gemmiparus is fundamentally an axillary bud, it shares many basic developmental features with the proximal axillary buds of M. guttatus. The proximal meristems of the two species, however, differ in timing of initiation and rate and extent of subsequent development.
Although the proximal meristems of both species are initiated in a similar position, between the distal meristem and the subtending leaf base, the timing of initiation differs. The initiation of the proximal meristem in M. gemmiparus is telescoped towards the shoot apex relative to M. guttatus. Initiation of the proximal meristem occurs by the second plastochron in M. gemmiparus (Fig. 4), whereas the proximal meristem in M. guttatus is not initiated until four or more plastochrons following initiation of the subtending leaf (Fig. 9). As a result, the proximal meristem of M. gemmiparus is initiated in close spatial and temporal proximity to the distal meristem. Accelerated initiation of the proximal meristem appears to impose a spatial constraint on the development of the two serial meristems; they are constricted within the axil of a very young leaf primordium and the two meristems nearly converge into one (Fig. 4).
Based on the analysis of M. gemmiparus alone, it is difficult to conclude definitively that the two supernumerary axillary meristems are initiated separately. An alternative interpretation is that they result from a dichotomy of the first (distal) meristem. In M. guttatus, however, there are clearly two separate initiation events; the proximal meristem is initiated subsequent to the distal meristem. Assuming that M. guttatus is representative of the ancestral condition, we infer that there are two separate initiation events in M. gemmiparus that occur in rapid succession. Additional evidence for this conclusion is provided by the sequence and timing of initiation of the two axillary meristems at node 2 of M. gemmiparus (this node does not bear bulbils). Initiation is clearly separate and sequential at this node (Figs. 19–21). Hence, both serial homology within the shoot of M. gemmiparus and comparison with M. guttatus provide evidence that the serial supernumerary buds of M. gemmiparus are produced by successive initiation events. Sandt (1925)
, Garrison (1955)
, and Gerrath and Posluszny (1989)
have also demonstrated separate and sequential initiation of meristems in several other taxa with supernumerary buds.
The accelerated initiation of the proximal meristem in M. gemmiparus may be related to the ultimate epiphyllous position of the brood bulbil. Early initiation of the bulbil meristem, while the base of the subtending leaf primordium is still highly meristematic, enables differential growth at the leaf base to carry the bulbil into an epiphyllous position. Epiphylly, in turn, allows the petiole to enfold the bulbil, forming the dispersal unit. Thus, precocious initiation, epiphylly, and the formation of an ensheathing petiole are developmentally and functionally interrelated features of the propagule of M. gemmiparus and are not found in the axillary shoots of M. guttatus.
Subsequent development of the proximal meristem in M. gemmiparus is also initially precocious with respect to the distal meristem. Although the proximal meristem is initiated slightly later in development, it grows rapidly and temporarily exceeds the distal meristem in size and morphogenesis (Fig. 6). The proximal meristem of M. guttatus is also initiated later than the distal meristem, however, its development does not become precocious. Rather, its development is arrested following the initiation of two pairs of leaves and no further activity of the meristem occurs. Quiescence of meristems is typical of plants with supernumerary buds, and often the additional meristems grow out only if the first meristem is damaged (Troll, 1937
; Bell, 1991
). Interestingly, growth and development of proximal meristems of both species are arrested following the initiation of two pairs of leaves. However, development is arrested only temporarily in M. gemmiparus, as growth is resumed during germination of the propagule.
Other differences between the proximal axillary buds of M. gemmiparus and M. guttatus include the accumulation of starch in the thickened, first pair of leaves and the abscission zone between the petiole and the subtending leaf base of M. gemmiparus. These features do not occur in M. guttatus and are likely associated with the function of the axillary bud of M. gemmiparus as a propagule.
In contrast, some of the features of the bulbil that enhance its function in vegetative propagation are also present in M. guttatus, including the ability to form shoot-borne roots and the capacity for dormancy. The stoloniferous lateral branches of M. guttatus root prolifically and provide a means of clonal growth and propagation in this species (Grant, 1924
). The apical and axillary buds of the rooted stolons can survive the winters of Colorado (A. Moody, personal observation) and elsewhere (e.g., Grant, 1924
; California; Munz and Keck, 1959
), indicating that they are capable of entering a dormant or quiescent state.
Retention of plesiomorphic pattern of development at basal nodes
Ramets of M. gemmiparus bear bulbils at all positions except the first and second nodes of the main axis (Fig. 1). The first node bears the storage leaves and has no axillary buds. The second node bears supernumerary buds in each leaf axil but none become bulbils (Fig. 1). In fact, the developmental fates of the two serial meristems produced in each leaf axil at the second node of M. gemmiparus are more similar to the fates of axillary meristems in M. guttatus than to meristems at subsequent nodes of M. gemmiparus. At node 2 of M. gemmiparus, and at all nodes of M. guttatus, the distal meristem is initiated approximately two to three plastochrons after initiation of the subtending leaf and produces a lateral branch. The proximal meristem is initiated much later than the distal meristem, approximately five (M. guttatus) to seven (M. gemmiparus) plastochrons after the initiation of the subtending leaf. Additionally, the proximal meristems of node 2 of M. gemmiparus, like the proximal meristems of M. guttatus, become quiescent following initiation and remain inactive throughout the ontogeny of the ramet. Thus, the second node of M. gemmiparus appears to retain the plesiomorphic developmental pattern expressed in M. guttatus.
Evolution of the brood bulbil
Based on positional and developmental similarities and the hypothesized phylogenetic relationship between Mimulus gemmiparus and Mimulus guttatus, the brood bulbil of M. gemmiparus is likely homologous to the proximal axillary bud of M. guttatus. The proximal axillary meristem, which contributes little to the morphology and life history of M. guttatus, has been recruited for the function of asexual reproduction in M. gemmiparus. The evolution of the bulbil has involved both incorporation of features already present in the shoots of M. guttatus, such as shoot-borne roots and dormancy, and the acquisition of novel features, such as the thickened storage leaves and the ensheathing petiole. Together, these features facilitate the dispersal and survival of the bulbil, the establishment of new ramets, and enable the bulbil to function as the primary means of perpetuating this rare Colorado endemic.
Brood bulbils in other taxa
Arizaga and Ezcurra (1995)
list 48 species from 22 genera and 15 families that are reported to bear bulbils. The term bulbil, however, is used loosely in the literature to denote a propagule located in the aerial portion of a vegetative shoot or within an inflorescence (Gentry, 1982
). Few authors cited by Arizaga and Ezcurra (1995)
make the morphological distinction between brood bulbils and brood tubers. For example, the propagules of Polygonum viviparum (Polygonaceae) are commonly referred to as bulbils (Engell, 1973
; Mabberley, 1987
; Arizaga and Ezcurra, 1995
); however, morphological analysis shows that they are brood tubers (Troll, 1937
; Diggle, 1997
). As a result of the imprecise terminology associated with asexual propagules, the prevalence of brood bulbils and the range of morphologies associated with their function are uncertain.
Brood bulbils have been described in only a few other taxa. Morphological analyses of Allium spp. (Amarylidaceae; Troll, 1937
), Agave spp. (Agavaceae; Gentry, 1982
; Arizaga and Ezcurra, 1995
), Lilium spp. (Liliaceae; Troll, 1937
; Goebel, 1900
), Dentaria bulbifera (Brassicaceae), Poa alpina (Poaceae), Remusatia vivipara (Araceae), Ranunculus ficaria (Ranunculaceae), and Saxifraga granulata (Saxifragaceae; Troll, 1937, 1959
) show that the brood bulbils of these taxa consist of small rosettes of an indeterminate number of spirally arranged, fleshy leaves in various stages of development. Thus, the small, determinate number of leaves present in the bulbils of M. gemmiparus is unusual. Similar to M. gemmiparus, shoot-borne root primordia are typically present in brood bulbils of other species prior to dispersal (Bell, 1991
). Most brood bulbils abscise away from the parent plant following senescence (Arizaga and Ezcurra, 1995
; Szarek et al., 1996
), and some species exhibit prolonged dormancy of the brood bulbils (e.g., Agave spp.; Szarek et al., 1996
). An ensheathing petiole, bract, or other covering subtending the bulbil is not present in any of the other taxa examined; the protective, ensheathing petiole of M. gemmiparus may be a unique feature of its propagule.
Functional and structural convergence
The brood bulbils of M. gemmiparus converge with sexually produced seeds in many ways. The bulbils are functional analogs of the seed of an annual: they are a crucial means of perpetuating the genotype or gene pool from one growing season to the next, they are dispersed and persist over the winter in a dormant state, and they contain a reserve of nutrients that facilitates germination and establishment. Interestingly, there are also structural analogies between the bulbils of M. gemmiparus and sexually produced propagules. The bulbil, with its opposite pair of thickened storage leaves, apical bud, and root primordia, is morphologically similar to the embryo of an exalbuminous seed with large fleshy cotyledons, a small epicotyl and a radicle (although the bulbils are homorhizic, whereas seed plant embryos are allorhizic; Groff and Kaplan, 1988
). In addition, the bulbil is enfolded in a petiole that is similar to a conduplicately folded carpel. The resemblance between the petiole and conduplicate carpel (e.g., Degeneria; Swamy, 1949
) even extends to the presence of interlocking trichomes along the adaxial margins of both structures. Ultimately, the petiole and carpel both serve a similar function: protection of the embryonic plant(s) within.
The functional convergences between brood bulbils and seeds are not unexpected; with the exception of dormancy, they may be common to most vegetative propagules. The extreme structural analogies to embryos and carpels, however, have not been reported for any other asexual propagule (see discussion of other taxa above) and may be unique to M. gemmiparus. During the evolutionary acquisition of a function that is novel within the genus Mimulus (Grant, 1924
), the axillary shoots of M. gemmiparus have acquired a morphology that may be unique among flowering plants.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Arizaga, S., and E. Ezcurra. 1995 Insurance against reproductive failure in a semelparous plant: bulbil formation in Agave macroacantha flowering stalks. Oecologia 101: 329–334.[CrossRef][ISI]
Beardsley, M. 1997 Colorado's rare endemic plant, Mimulus gemmiparus, and its unique mode of vegetative reproduction. Master's thesis, Colorado State University, Fort Collins, CO.
Bell, A. D. 1991 Plant form: an illustrated guide to flowering plant morphology. Oxford University Press, Oxford.
Bower, F.O. 1898 The British Association. Bristol Meeting. Section K (Botany). Opening address by Prof. F.O. Bower, Sc.D., F.R.S., President of the section. II. Nature 59: 88–91.[CrossRef]
Clowes, F. A. L. 1961 Apical meristems. Blackwell Scientific Publications, Oxford.
CONPS (Colorado Native Plant Society). 1989 Rare plants of Colorado. Rocky Mountain Nature Association, Denver, CO.
Diggle, P. K. 1997 Extreme preformation in alpine Polygonum viviparum: an architectural and developmental analysis. American Journal of Botany 84: 154–169.[Abstract]
Engell, K. 1973 A preliminary morphological, cytological, and embryological investigation in Polygonum viviparum. Botanisk Tidsskrift 67: 305–316.
Esau, K. 1977 The stem: primary state of growth. In Anatomy of seed plants, 257–294. John Wiley & Sons, New York, NY.
Friedman, W. E. 1994 The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm. American Journal of Botany 81: 1468–1486.[CrossRef][ISI]
Garrison, R. 1955 Studies in the development of axillary buds. American Journal of Botany 42:257–266.
Gentry, H. S. 1982 Agaves of continental North America. University of Arizona Press, Tuscon, AZ.
Gerrath, J. M., and U. Posluszny. 1989 Morphological and anatomical development in the Vitaceae. V. Vegetative and floral development in Ampelopsis brevipedunculata. Canadian Journal of Botany 67: 2371–2386.
Goebel, K. 1900 Organography of plants. Part I and II, (English translation by I. B. Balfour). Reprinted by Hafner, New York, NY.
Grant, A. L. 1924 A monograph of the genus Mimulus. Annals of the Missouri Botanical Garden 11: 99–162.
Groff, P. A., and D. R. Kaplan. 1988 The relation of root systems to shoot systems in vascular plants. Botanical Review 54: 387–422.
Jacob, F. 1982 The actual and the possible. University of Washington Press, Seattle,WA.
Mabberley, D. J. 1987 The plant-book: a portable dictionary of the higher plants. Cambridge University Press, Cambridge.
Munz, P. A., and D. D. Keck. 1959 A California flora and supplement. University of California Press, Berkeley, CA.
O'Kane, S. L., Jr. 1988 Colorado's rare flora. Great Basin Naturalist. 48: 434–469.
Sandt, W. 1925 Zur Kenntnis der Beiknospen. Botanische Abhandlung. Heft 7, pp. 1–160.
Swamy, B. G. L. 1949 Further contributions to the morphology of the Degeneriaceae. Journal of the Arnold Arboretum 30: 10–38.
Szarek, S. R., B. Driscoll, C. Shohet, and S. Priebe. 1996 Bulbil production in Agave (Agavaceae) and related genera. Southwestern Naturalist 41: 465–469.
Troll, W. 1937 Vergleichende Morphologie der höheren Pflanzen I. Verlag von Gebrüder Borntraeger, Berlin.
———. 1959 Allgemeine Botanik ein Lehrbuch auf vergleichend-biologischer Grundlage. Dritte Auflage. Ferdinand Enke Verlag, Stuttgart.
Vickery, R. K., Jr. 1978 Case studies in the evolution of species complexes in Mimulus. In M. K. Hecht, W. C. Steere, and B. Wallace [eds.], Evolutionary biology, vol. 11. Plenum, New York, NY.
Walton, G. B., and L. Hufford. 1994 Shoot architecture and evolution of Dicentra cucullaria (Papaveraceae, Fumarioideae). International Journal of Plant Sciences 155: 553–568.[CrossRef]
Weber, W. A. 1972 Mimulus gemmiparus sp. nov. from Colorado. Madroño 21: 423–425.
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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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C.-N. Wang and Q. C. B. Cronk Meristem fate and bulbil formation in Titanotrichum (Gesneriaceae) Am. J. Botany, December 1, 2003; 90(12): 1696 - 1707. [Abstract] [Full Text] [PDF]
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P. M. Beardsley and R. G. Olmstead Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma Am. J. Botany, July 1, 2002; 89(7): 1093 - 1102. [Abstract] [Full Text] [PDF]
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