| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Reproductive Biology |
Department of Botany, Miami University, Oxford, Ohio 45056 USA
Received for publication February 5, 2002. Accepted for publication April 19, 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: breeding system • Cactaceae • Consolea spinosissima • embryology • Jamaica • sex determination • sexual morphs • subdioecy
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Despite its broad taxonomic range, dioecy is relatively rare, being found in only 4% of all angiosperm species (Yampolsky and Yampolsky, 1922
). It is, however, more prevalent on oceanic islands, such as Hawaii, New Zealand, Juan Fernández, and Tonga, than in temperate inland regions (Sakai and Weller, 1999
).
Dioecious species vary in their sexual expression resulting in gynodioecy, androdioecy, and trioecy or subdioecy (Sakai and Weller, 1999
). The latter refers to populations that regularly contain imperfectly differentiated individuals (of either or both sexes) in addition to strictly unisexual individuals (Ross, 1982
). However, if the sex of the unisexual individuals is not evident, then a distinctive subset has been established to include those species that are functionally but cryptically dioecious. Mayer and Charlesworth (1991)
defined cryptically dioecious systems as including taxa that have unisexual morphs, of which at least one will appear to have perfect flowers. Typically, flowers of cryptically dioecious individuals retain nonfunctional organs such as gynoecia in functionally staminate flowers and androecia in functionally pistillate ones. Cryptically dioecious and subdioecious breeding systems are difficult to recognize, given that the nonfunctional organs can be comparable in size and appearance to the functional parts. At least 78 species from 20 families, including the Cactaceae, have been recognized as cryptically dioecious (Mayer and Charlesworth, 1991
).
Mayer and Charlesworth (1991)
have discussed the retention of the nonfunctional organs, suggesting that there has not been enough evolutionary time for their suppression, or genetic correlations between androecium and gynoecium delay the suppression of one or the other in functionally unisexual flowers, or because they are important in the attraction of pollinators. Davis (1997)
refuted the latter hypothesis for Thalictrum pubescens Pursch and suggested that it might be proper to revisit the first two hypotheses.
The Cactaceae breeding system includes outcrossing (Mandujano, Montana, and Eguiarte, 1996
; Fleming, 2000
), self-incompatibility (Ross, 1981
; Boyle, 1996
; Negrón-Ortiz, 1998
), self-compatibility (Boyle, Menalled, and O'Leary, 1994
), agamospermy (Maheshwari and Chopra, 1955
; García-Aguilar and Pimienta-Barrios, 1996
; Fleming, 2000
), dioecy (Parfitt, 1985
), trioecy, and gynodioecy (Fleming et al., 1994
; Rebman, 1998
; Fleming, 2000
). Dioecy is not common in the family and has been reported to occur in only ten species of five genera (Opuntia Miller, Echinocereus Engelmann, Selenicereus [Berger] Britton and Rose, Pachycereus [Berger] Britton and Rose, and Mammillaria Haworth; Parfitt, 1985
; Ferguson, 1989
). Opuntia sanfelipensis J. Rebman and O. wolfii (L. D. Benson) M. Baker are presumably gynodioecious (Rebman, 1998
). One species of Selenicereus has been described as questionably gynodioecious, and Mammillaria dioica K. Brandegee, M. neopalmeri R.T. Craig, and Pachycereus pringlei (S. Watson) Britton and Rose have various mating systems, including gynodioecy and/or trioecy (Parfitt, 1985
; Fleming et al., 1994
; Fleming, 2000
). Opuntia robusta H. Wendland is trioecious (del Castillo, 1986 in Fleming et al., 1994
), O. quimilo K. Schumann is reported as functionally dioecious (Díaz and Cocucci, 2001
), but is really gynodioecious, and Echinocereus coccineus Engelmann, reported as functionally dioecious, is the only known cryptically dioecious cactus (Hoffman, 1992
).
The natures of the breeding systems mentioned above were either determined by experimental manipulations or were inferred from herbarium sheet data; none included embryological data. One exception is the study by García-Aguilar and Pimienta-Barrios (1996)
in which embryological data are used to document agamospermy in Opuntia. Historically, embryological studies have been used to assess taxonomic relationships among families and genera (Johri, Ambegaokar, and Srivastava, 1992
). Engleman (1960)
, for example, revised ovule and seed characters of Astrophytum myriostigma Lemaire, Thelocactus bicolor Brittton and Rose, and Toumeya papyrancanthus Britton and Rose to help determine phylogenetic relationships. Recently, Stuppy (2002)
proposed the resurrection of several genera in the Cactaceae based on their seed characters. General embryological descriptions have been published on various species of Opuntia (Archibald, 1939
; Tiagi, 1954
; Maheshwari and Chopra, 1955
; Chopra, 1957
), as well as on one or two species of Rhipsalis Gaertner, Mammillaria, and Pereskia (Plumier) Miller (Mauritzon, 1934
; Neumann, 1935
). These studies have demonstrated that the Cactaceae are embryologically homogeneous, being characterized by a bitegmic, crassinucellate ovule and by a monosporic megagametophyte (Johri, Ambegaokar, and Srivastava, 1992
). Several other embryological characters such as the funicular hump or the single endosperm layer cap around the radicle had been used to hypothesize that the Cactaceae evolved from the old Centrospermae (Engleman, 1960
).
Consolea Lemaire (Opuntioideae, Cactaceae) is a small group of nine, distinctive, and "tree-like" opuntioids restricted to the Caribbean region. The species range from the Florida Keys, across the Bahamas and the Greater Antilles, to Guadeloupe in the Lesser Antilles (Areces-Mallea, 1996
). Lemaire segregated this genus from Opuntia in 1862 (in Areces-Mallea, 1996
) based on its distinctive cylindrical trunk, asymmetric distal branches, and small flowers. Consolea was not accepted at the generic level by Britton and Rose (1919)
; the constituent species (excluding Opuntia bahamana Britton and Rose) were included in the series Spinosissimae of the genus Opuntia. Their inclusion in Opuntia was accepted until recently when Areces-Mallea (1996
, 2000
, 2001
) clearly supported the distinctness of this genus based on the characters used by Lemaire, as well as embryological and palynological data. Many taxonomic works (Britton and Rose, 1919
; Backeberg, 1976
; Areces-Mallea, 1996
, 2000
, 2001
) referring to Consolea species described the flowers as perfect. The recent work of Areces-Mallea (2000)
on the floral morphology of Consolea picardae (Urban) Areces notes that some flowers have nonfunctional, rudimentary anthers lacking pollen grains. Backeberg (1976)
mentioned that seeds appear to be few in number or often missing in Consolea, and he suggested that asexual propagation is quicker than when the plants develop from seeds. Negrón-Ortiz (1998)
observed that the Florida endemic, Consolea corallicola Small (as Opuntia spinosissima (Martyn) Mill.) rarely sets viable seeds. Extensive hand pollination studies led her to conclude that the 12 known plants of C. corallicola were asexually derived from a single sterile polyploid lineage and were unable to set fruit sexually.
Consolea spinosissima (Mill) Lemaire is endemic to Jamaica. It grows along the southern coast of Jamaica on dogtooth limestone in a moderately disturbed coastal habitat that, due to logging, lacks almost all woody components. The population situated at Hellshire Hills is the most conspicuous population on the island. Herbarium vouchers collected close to the Kingston airport (southeastern Jamaica) and some in St. Elizabeth (southwestern Jamaica) suggest the presence of C. spinosissima all along the southern coast. Preliminary field observations (V. Negrón-Ortiz) suggested that more than one sexual morph was present in the Jamaican population and that the species was distinct from C. corallicola of Florida.
The cryptic nature of C. corallicola's breeding system (Negrón-Ortiz, 1998
) and the possible presence of more than one sexual morph in C. spinosissima led us to investigate both the breeding system and the embryology of the latter species. Specifically, the present study describes, from an embryological perspective, the critical stages for sex determination in C. spinosissima. It also describes ovule and anther development, mega- and micro-sporogenesis, and mega- and micro-gametogenesis.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Herbarium vouchers were collected and deposited in the Willard Sherman Turrell Herbarium (MU), Miami University, Oxford, Ohio, USA, and fixed flower material was deposited in the Bruce Fink laboratory also at Miami University. Flowers in different developmental stages from 18 individuals were collected in formalin-acetic acid-alcohol (FAA) for light microscopy, scanning electron microscopy (SEM), and pollen tube studies. Samples for sectioning were dehydrated in an ascending series of ethanol and embedded in paraffin. Blocks were sectioned at 7–12 µm and stained with safranin and fast-green (D'Ambrogio, 1986
) or with 0.01% aniline blue (Rost, 1992
). Sections were photographed (Nikon Eclipse E600, Kawasaki, Japan) and drawn using an attached drawing tube. Sections of developing flowers were stained with aniline blue and examined for callose deposition using an epifluorescence microscope (Nikon Eclipse E 600).
Styles and stigmas of open flowers were softened in 8 mol/L NaOH for 48 h at room temperature, rinsed for a minimum of 1 h in distilled water, stained with aniline blue in 0.1 mol/L K3PO4 for a minimum of 4 h, then squashed and analyzed for pollen tube growth using the epifluorescence microscope (Schou and Philipp, 1982
).
For SEM studies, the preserved materials were dehydrated in a graded series to 100% ethanol and critical point dried with CO2. Specimens were mounted on SEM stubs with sticky tabs, sputter-coated with 21 nm of gold, and viewed and photographed using a Jeol T-200 (Tokyo, Japan) scanning electron microscope.
The terminology of Sakai and Weller (1999)
, in which "male" refers to plants bearing staminate flowers and "female" refers to plants bearing pistillate flowers, is used here.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
|
|
Floral development
Consolea spinosissima floral development was divided into ten stages for which distinctive cellular events could be visualized at the level of the light microscope (Fig. 24). This table summarizes the key events that occur at each stage and enumerates which cells and tissues are present. Flowers of the three sexual morphs start as hermaphrodites and become unisexual at different stages during development. Pistillate flowers of the female morph start to abort the tapetum and microspore mother cells at the meiotic stage (Fig. 24, stages 3–4). Staminate flowers of the male morph abort their ovules later (Fig. 24, stage 7) and reach anthesis with completely consumed ovules (Fig. 24, stages 8–9). Superficially perfect flowers of the weak hermaphrodite morph follow the same abortion pattern as the staminate flowers; however, few apical ovules in some flowers remain viable until anthesis. A detailed description of these developmental changes is given below.
|
|
Microgametogenesis begins with the unequal mitotic division of the microspore resulting in a small generative cell and a large vegetative cell (stage 6). At the time of shedding, the generative nucleus has started mitosis to form two small sperm cells (Fig. 30). The cytoplasm of the vegetative cell contains numerous starch grains (Fig. 30, stages 7–9). Pollen grains are multiporate (Fig. 19), and their exine is reticulate and formed by the muri. There are no supratectal ornamentations. The apertures' membranes possess globular ornamentations (Fig. 19).
Pistillate flowers
Anther wall development generally proceeds as in staminate flowers (Fig. 25; stages 1–2) but the degeneration of the tapetum takes place at an earlier stage, prior to meiosis (Fig. 27; stage 3). The tapetal cells enlarge and become highly vacuolated before the microspore mother cells enter prophase I and degenerate shortly afterward (Figs. 27, 29; stage 3). The mmc's normally degenerate not long after prophase I, although, in some cases, they may form an abnormal "tetrad" (Fig. 7). In some anther locules, callose wall remnants of the aborted mmc's can be observed surrounded by degenerated tapetal and middle layer cells (Figs. 7, 29; stage 5). The endothecial cells do not enlarge as in staminate flowers but persist throughout, although most of them never develop fibrous thickenings (Fig. 31). At maturity, the anther wall is composed of the epidermis, with some stomata, and the endothecium; these surround four empty sporangia (Fig. 31; stage 6). At anthesis anthers are empty, shriveled, and positioned below the stigma level (Figs. 1, 8; stage 9).
Stigma and style
In all the morphs, the stigma is five-lobed and has five receptive zones, each with a distinctive papillate surface (Figs. 5, 13, 23). At anthesis, the stigma lobes of pistillate flowers are divergent with the receptive surfaces exposed (Fig. 5). In functionally staminate flowers, the stigma lobes are closed with the receptive surfaces hidden (Fig. 13). In the superficially perfect flowers of the weak hermaphrodite morph, the stigma lobes vary from closed to fully divergent (Fig. 23).
In transection, the style of all three morphs is semisolid, composed of an outer epidermis, cortical parenchyma, five vascular bundles, mucilaginous cells, transmission tissue, and a glandular epidermal layer surrounding the stylar canal (Fig. 6). The pollen tubes grow through the transmission tissue. In longitudinal section, the cells of the transmission tissue are axially elongated with dense cytoplasm and an elongate nucleus.
Ovule development
The inferior ovary contains approximately 200–250 ovules arranged on five parietal placentas. Along each placenta, a double row of ovules is initiated as small protuberances that bend away from each other (Figs. 9, 32; stage 1). These will grow and give rise to crassinucellate, circinatropous ovules (Figs. 10, 33; stage 2). At maturity the ovule lies in an anatropous position but is completely encased by the funicle, the so-called funicular envelope (Figs. 11, 34–37; stages 5–10). The two true integuments are two cell layers thick, although distally the inner integument becomes multilayered and its protruding, swollen apex forms the micropyle (Figs. 11–12, 35–37).
|
At maturity, the cells of the nucellar epidermis situated at the micropyle are radially elongate. These cells, which constitute the epistase, have a thick inner tangential primary wall, and it is through these cells that the pollen tube penetrates to reach the embryo sac (Figs. 11–12, 35–37). A group of elongated, cytoplasm-dense nucellar cells, the hypostase, delimit the embryo sac at the chalazal end (Figs. 11, 20, 35–36).
Megasporogenesis, megagametogenesis, and fertilization
Pistillate flowers
Prior to megasporogenesis, a single large hypodermal archesporial cell (Fig. 40) divides periclinally to form a small outer primary parietal cell and a large inner megaspore mother cell (MMC, Fig. 32; stage 2). The primary parietal cell undergoes only anticlinal divisions, establishing a cell layer between the MMC and the nucellar epidermis (Figs. 10, 33). Megasporogenesis takes place when the elongated MMC starts meiosis (Fig. 41; stages 3–4). Successive cytokineses result in a linear megaspore tetrad (Figs. 42–43). The three micropylar megaspores degenerate, and the chalazal megaspore develops into the megagametophyte (Figs. 44–50; stages 5–8).
|
2.43 µm, N = 50) are distributed in the region of the egg apparatus and surrounding the polar nuclei (Figs. 48, 50). Even though the pollen tubes are difficult to trace in the ovary, the penetration tube can be observed in the nucellar cap cells (epistase). A conspicuous callose plug and a destroyed synergid (Fig. 12) are evidence of the discharge of the tube contents into one of the synergids. In several ovules, the sperm cell was observed close to the egg cell or secondary nucleus. In all examined ovules (N = 653) derived from incipient fruits, evidence of fertilization was observed (Fig. 12, stage 10).
Functionally staminate flowers
Megasporogenesis and megagametogenesis in both functionally staminate and superficially perfect flowers follow the same pattern as in pistillate flowers (stages 1–6) until ovule degeneration begins (stage 7). Degeneration of the ovules is initially evidenced by a considerable reduction in the nucellar tissue, due to disintegration of the nucellar cells surrounding the embryo sac (Fig. 38; stage 7). This nucellar degradation is correlated with the appearance of numerous, large starch grains ( 6.5 µm, N = 50) in the eight-nucleate embryo sac (Figs. 21–22, 38–39, 51–52) and by a thinning of the funicle (Figs. 21, 38–39). The starch grains are significantly larger than those found in healthy embryo sacs (T = 21, P < 0.0005, df = 48; Figs. 51–52).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, 2000
, 2001
). In addition, flowers of the weak hermaphrodite morph cannot be consistently told from those of the male morph. For these reasons we consider C. spinosissima to be cryptic and subdioecious.
The female morph has pistillate flowers that exhibit divergent stigma lobes and set fruit, but do not produce pollen grains; thus the androecium is vestigial. Persistence of the nonfunctional anthers could be the consequence of a relatively recent evolutionary move towards dimorphism. Alternatively, they could have been retained because they are adaptive; the empty, yellowish anthers mimic the appearance of the anthers of the male and weak hermaphrodite morphs, perhaps aiding in pollinator attraction (Mayer and Charlesworth, 1991
).
The male morph is cryptic and has staminate flowers with viable pollen grains and a nonfunctional gynoecium, which does not set seeds. At anthesis, the staminate flowers have numerous pollen tubes within and on the stigma but none grow in the style. In addition, the stigma lobes remain closed throughout anthesis, hiding the receptive surface. This indicates that the gynoecium of this morph is nonfunctional and vestigial. Being vestigial, the style might lack the ability to produce the nutrients and the chemical signals that allow pollen tubes to grow. In addition, the ovules that are aborted and consumed likely do not produce the guidance signals needed to attract pollen tubes (Cheung, 1996
). Both explanations are supported by Herrero and Hormaza (1996)
, who document that a reduction in the availability of transmitting tissue reserves can affect the number of pollen tubes growing within the style.
The weak hermaphrodite morph is also cryptic; its flowers superficially resemble the functionally staminate flowers of the male morph and can only be distinguished after careful morphological and embryological analyses. This morph is not as successful in the female function as the female morph, but does have some female capability. Some of its flowers can reach anthesis with a variable number of viable ovules in the upper part of the ovary, while others present all their ovules aborted at anthesis. In flowers of this morph, the gynoecium is partially functional as evidenced by pollen tubes in the style and aborted ovules at anthesis.
The presence of pollen grains on the stigma in perfect and staminate flowers suggests the possibility of autogamy. Self-deposition occurs because, at the beginning of anthesis, the closed stigma lies buried in a mass of open anthers that are full of pollen grains (Figs. 3–4, 13, 23). However, because common floral visitors were observed in flowers of the three morphs, cross-pollination cannot be rejected until experimental manipulations are performed. Therefore, self-incompatibility in perfect flowers cannot be ruled out, because pollen tubes growing within their style could be derived from either cross or self-pollen. The divergent stigma lobes of the pistillate flowers are positioned above the level of the empty, aborted anthers, thus the presence of pollen grains on the female morph stigma are solely the result of cross-pollination. The differences in the number of pollen grains deposited on the stigmas of pistillate flowers vs. staminate and perfect flowers provide additional evidence for self-deposition of pollen grains in staminate and perfect flowers.
Evidence of fertilization was observed in the ovules of open and past-pollinated flowers of pistillate and superficially perfect flowers belonging to the female and weak hermaphrodite morphs, respectively. As demonstrated by Maheshwari and Chopra (1955)
for Opuntia, the fertilization event can be surmised from remnant pollen tubes in the micropylar region of the ovule or from the presence of one degenerating and one healthy synergid. Those signs of fertilization were observed in every ovule of past-pollinated pistillate and perfect flowers of C. spinosissima examined (N = 653 ovules). In some cases, it was possible to observe sperm cells adjacent to the secondary nucleus and egg cell.
Nucellar embryony, a type of agamospermy, is evidenced by the development of neighboring nucellar cap cells that develop into proembryos filling the embryo sac cavity (Maheshwari and Chopra, 1955
). This type of agamospermy was observed in Opuntia aurantiaca Gilles ex Lindley, O. vulgaris P. Miller, and O. rafinesquei Englemann (Archibald, 1939
), and in O. streptacantha Lemaire (García-Aguilar and Pimienta-Barrios, 1996
). None of the 653 ovules of C. spinosissima examined had adventive embryos, at least at the early stages of fruit development examined. These results don't completely rule out the occurrence of agamospermy in C. spinosissima, but suggest that sexual reproduction is responsible for most seeds. In order to completely discard agamospermy, manipulations must be conducted. For instance, extensive hand-pollination experiments conducted on flowers of C. corallicola (Negrón-Ortiz, 1998
) demonstrated that the only seeds produced were by agamospermy. The population of C. corallicola consists of 12 individuals. These individuals rarely set seeds, and, while pollen tubes do reach the ovary, they fail to penetrate the ovules (Negrón-Ortiz, 1998
). Most of those ovules are aborted at anthesis (V. Negrón-Ortiz and L. Strittmatter, unpublished data), a situation that corresponds to some extent to what was observed in the weak hermaphrodite morph of C. spinosissima.
Sex differentiation
The critical stage for sex determination is different in staminate, perfect, and pistillate flowers. Although perfect flowers can maintain their "hermaphroditic" condition at least to some extent throughout their development, ovule abortion at the base of the ovary starts at stage 7 (Fig. 24). Flowers of the female morph become pistillate at a relatively early stage (Fig. 24, stage 3) of development. This condition is the result of the complete abortion of both the mmc's and the tapetum and occurs while the megaspore mother cell is undergoing meiosis (Fig. 24, stages 3–4). Staminate flowers start to become unisexual at stage 7 (Fig. 24). These flowers retain their hermaphroditic condition until the megagametophyte is nearly mature and the anthers are filled with tricellular pollen grains (Fig. 24, stages 7–8). Very similar timing for sex determination (and sexual morphs) was found in the "dioecious" Asparagus officinalis L. (Lazarte and Palser, 1979
). In this system, sexual determination is based on sex chromosomes. The staminate plants are either heterogametic XY or homogametic YY, and pistillate plants are homogametic XX (Lazarte and Palser, 1979
). These three sexual morphs appear to be analogous to the weak hermaphrodite, male, and female morphs of C. spinosissima, respectively. Consolea spinosissima is polyploid (n = 132; H. Cota, University of Saskatchewan, Canada, personal communication), and the presence of sex chromosomes is unknown. The length of florets and panicles were used as developmental markers for identifying critical stages in sexual developmental determination in wild rice (Han and Liu, 1999
). These criteria were not useful for C. spinosissima because the height and diameter of the flowers were too variable.
Ovule abortion
Ovules of staminate flowers complete abortion before anthesis, thus precluding the formation of sexually derived seeds. This abortion was evidenced by the degeneration of the nucellar cells that lie adjacent to the megagametophyte cavity and the megagametophyte. Ovule abortion in Asparagus officinalis starts in the sterile tissues of the ovule, i.e., the nucellar cells at the chalazal end and the integuments, and proceeds towards the megagametophyte (Lazarte and Palser, 1979
). In C. spinosissima, both events are apparently simultaneous. Consolea spinosissima embryo sacs, specifically the central cell, accumulates numerous, large starch grains while the egg apparatus degenerates. Abnormal accumulation of starch grains has been also noted in the degenerating embryo sac of Opuntia dillenii (Ker Gawler) Haworth (Tiagi, 1954
), in the embryo sac's central cell of the seedless Ramosmania heterophylla (Balf.f.) Tirv. and Verdc. (Owens et al., 1993
), and in the central cell of the PS-1 mutant (female sterile) of Glycine max (L.) Merrill (Pereira, Lersten, and Palmer, 1997
). Thus the presence of large starch grains appears to correlate with embryo sac abortion.
Anther abortion
Male sterility can be classified on a genetic basis, and according to the inheritance pattern, three different forms, i.e., cytoplasmic, genetic, or cytoplasmic–genetic-based, can be distinguished (Kaul, 1988
). Even though the latter is the most common in natural gynodioecious species (Kaul, 1988
), we cannot determine, based on the structural analysis alone, which type of male sterility C. spinosissima possesses.
Anthers in pistillate flowers of C. spinosissima have a tapetal layer that follows a different developmental pattern than that observed in staminate and perfect flowers. Although abnormal tapetal cells are the first indication of anther abortion, defects in the meiotic processes cannot be ruled out, especially since almost no microspore tetrads are formed. High vacuolization of the tapetal cells mark the beginning of the death of this layer, suggesting that these cells are undergoing programmed cell death (PCD). Programmed cell death, as described by Wredle, Walles, and Hakman (2001)
, refers to cell death that is mediated by the intracellular death program, independently of what triggers it or if it shows the common signs of apoptosis, where the nucleus shows the first signs of degeneration. This pattern of premature degeneration of the tapetum and microspore mother cells was also observed in Arabidopsis thaliana (L.) Heynh. male sterile mutants pollenless1-1 and pollenless2 (Sanders et al., 1999
). The anthers of these two mutants formed fibrous band thickenings in the endothecial cells and dehisced (Sanders et al., 1999
), while anthers of C. spinosissima pistillate flowers failed to do so (Figs. 7, 31).
In summary, the ancestor of C. spinosissima is unknown, but based on the presence and early development of the androecium in the female morph and the gynoecium in the male and weak hermaphrodite morphs, we can hypothesize that it is/was hermaphroditic. The evolutionary stimuli for C. spinosissima evolving towards unisexuality and the nature of the route are questions that remain unanswered. However, one possible pathway that pertains to this issue was examined by Ross (1982)
. The hermaphroditism-gynodioecy-subdioecy pathway is characterized by the presence of well-differentiated females, but incompletely differentiated males (Lloyd, 1976 as in Ross, 1982
). The proposed evolutionary pathway towards unisexuality starts with hermaphroditism, followed by the establishment of females (male-sterile mutant) among the hermaphrodites, resulting in gynodioecy. This is followed by a gradual reduction of seed fertility in the hermaphrodites, such that these function mainly as males. Ross (1982)
remarks that in subdioecious or dioecious species of this pathway, the females are usually strictly female in function, showing rudimentary nonfunctional anthers. The males, in contrast, are more hermaphroditic in appearance, being practically indistinguishable from the hermaphrodites except for the lack of fruits and sometimes defective stigmas. This pathway seems comparable to the route Consolea spinosissima followed towards unisexuality. The embryological results of critical sex determination for C. spinosissima showed that the females are well-differentiated at earlier stages of development (Fig. 24, stages 3–4), whereas the males and weak hermaphrodites differentiate near anthesis (Fig. 24, stage 7).
As part of an ongoing study into the embryology and breeding system of Consolea, we provide evidence that the breeding system of Consolea spinosissima is cryptic and subdioecious. Our studies document that populations of this species consist of plants with functionally staminate, functionally pistillate, or weakly hermaphroditic flowers, the latter having primarily a male function. Embryological studies document the breakdown of male function within the persistent stamens of the female morph, the complete ovule abortion in the male morph, and the sequential, and oftentimes complete, abortion of ovules in the comparatively rare weak hermaphrodite morph.
|
FOOTNOTES |
|---|
2 Author for reprint requests (strittl1{at}muohio.edu
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Archibald E. E. A. 1939 The development of the ovule and seed of jointed cactus (Opuntia aurantiaca Lindley). South African Journal of Sciences 36: 195-211
Areces-Mallea A. E. 1996 New taxa of Consolea Lemaire (Cactaceae: Opuntioideae) from Cuba. Brittonia 48: 224-236[CrossRef][ISI]
Areces-Mallea A. E. 2000 Consolea picardae (Urban) Areces, comb. Nov.—revalidation of a neglected West Indian opuntioid. Cactus and Succulent Journal (U.S.) 72: 41-45
Areces-Mallea A. E. 2001 A new opuntioid cactus from the Cayman Islands, B.W.I., with a discussion and key to the genus Consolea Lemaire. Brittonia 53: 96-107[ISI]
Backeberg C. 1976 Cactus Lexicon. Enumeratio diagnostica Cactacearum. Blandford Press, Poole, Dorset, UK
Boyle T. H. 1996 Characteristics of self-incompatibility in Schlumbergera truncata and S. x buckleyi (Cactaceae). Sexual Plant Reproduction 9: 49-53
Boyle T. H. F. D. Menalled M. C. O'Leary 1994 Occurrence and physiological breakdown of self-incompatibility in easter cactus. Journal of the American Society of Horticultural Sciences 119: 1060-1067
Britton N. L. J. N. Rose 1919 The Cactaceae. 1. Carnegie Institution, Washington, D.C., USA
Cheung A. Y. 1996 The pollen tube growth pathway: its molecular and biochemical contributions and responses to pollination. Sexual Plant Reproduction 9: 330-336[CrossRef][ISI]
Chopra R. N. 1957 The mode of embryo sac development in Opuntia aurantiaca Lindl.—a reinvestigation. Phytomorphology 7: 403-406
D'Ambrogio A. 1986 Manual de técnicas en Histología Vegetal. Hemisferio Sur S. A., Buenos Aires, Argentina
Davis S. 1997 Stamens are not essential as an attractant for pollinators in females of cryptically dioecious Thalictrum pubescens Pursch. (Ranunculaceae). Sexual Plant Reproduction 10: 293-299[CrossRef][ISI]
Díaz L. A. A. Coccuci 2001 Dioecia funcional en Opuntia quimilo (Cactaceae). Resumen en XXVIII Jornadas Argentinas de Botánica. Boletín de la Sociedad Argentina de Botánica 36: (Supl.) 34.
Engleman E. M. 1960 Ovule and seed development in certain cacti. American Journal of Botany 47: 460-467[CrossRef][ISI]
Ferguson D. J. 1989 Revision of the U.S. members of the Echinocereus triglochidiatus group. Cactus and Succulent Journal 61: 217-224
Fleming T. H. 2000 Pollination of cacti in the Sonoran desert. American Scientist 88: 432-439[CrossRef]
Fleming T. H. S. Maurice S. L. Buchmann M. D. Tuttle 1994 Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae). American Journal of Botany 81: 858-867[CrossRef][ISI]
García-Aguilar M. E. Pimienta-Barrios 1996 Cytological evidences of agamospermy in Opuntia (Cactaceae). Haseltonia 4: 39-42
Han S. S. Q. Liu 1999 Developmental events associated with the critical stage for sex determination in wild rice florets. International Journal of Plant Sciences 160: 1127-1133[CrossRef][ISI][Medline]
Herrero M. J. I. Hormaza 1996 Pistil strategies controlling pollen tube growth. Sexual Plant Reproduction 9: 343-347[ISI]
Hoffman M. T. 1992 Functional dioecy in Echinocereus coccineus (Cactaceae): breeding system, sex ratios, and geographic range of floral dimorphism. American Journal of Botany 79: 1382-1388[CrossRef][ISI]
Johri B. M. K. B. Ambegaokar P. S. Srivastava 1992 Comparative embryology of angiosperms. Springer-Verlag, Berlin, Germany
Kaul M. L. H. 1988 Male sterility in higher plants. Springer-Verlag, Berlin, Germany
Lazarte J. E. B. F. Palser 1979 Morphology, vascular anatomy and embryology of pistillate and staminate flowers of Asparagus officinalis. American Journal of Botany 66: 753-764[CrossRef][ISI]
Maheshwari P. R. N. Chopra 1955 The structure and development of the ovule and seed of Opuntia dillenii Haw. Phytomorphology 5: 112-122
Mandujano M. C. C. Montana L. E. Eguiarte 1996 Reproductive ecology and inbreeding depression in Opuntia rastrera (Cactaceae) in the Chihuahuan desert: why are sexually derived recruitments so rare?. American Journal of Botany 83: 63-70[CrossRef][ISI]
Mauritzon J. 1934 Ein Beitrag szur Embryologie der Phytolaccaceen und Cactaceen. Botaniska Notiser 1934: 111-135
Mayer S. S. D. Charlesworth 1991 Cryptic dioecy in flowering plants. Trends in Ecology and Evolution 6: 320-325
Negrón-Ortiz V. 1998 Reproductive biology of a rare cactus, Opuntia spinosissima (Cactaceae), in the Florida Keys: why is seed set very low?. Sexual Plant Reproduction 11: 208-212[CrossRef][ISI]
Neumann M. 1935 Die Entwicklung des Pollens, der Samenanlage und des Embryosackes von Pereskia amapola var. argentina. Oesterreichische Botanische Zeitschrift 84: 1-30[CrossRef]
Owens S. J. A. Jackson M. Maunder P. Rudall M. A. T. Johnson 1993 The breeding system of Ramosmania heterophylla—dioecy or heterostyly?. Botanical Journal of the Linnean Society 113: 77-86[CrossRef]
Parfitt B. D. 1985 Dioecy in North American Cactaceae: a review. Sida 11: 200-206
Pereira T. N. S. N. R. Lersten R. G. Palmer 1997 Genetic and cytological analyses of a partial-female-sterile mutant (PS-1) in soybean (Glycine max; Leguminosae). American Journal of Botany 84: 781-791[Abstract]
Rebman J. P. 1998 A new cholla (Cactaceae) from Baja California, Mexico. Haseltonia 6: 17-21
Ross M. D. 1982 Five evolutionary pathways to subdioecy. American Naturalist 119: 297-318[CrossRef][ISI]
Ross R. 1981 Chromosome counts, cytology, and reproduction in the Cactaceae. American Journal of Botany 68: 463-470[CrossRef][ISI]
Rost F. W. D. 1992 Fluorescence microscopy. Cambridge University Press, Cambridge, UK
Sakai A. K. S. G. Weller 1999 Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants. Springer, Berlin, Germany
Sanders P. M. A. Q. Bui K. Weterings K. N. McIntire Y. C. Hsu P. Y. Lee M. T. Truong T. P. Beals R. B. Goldberg 1999 Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11: 297-322[CrossRef][ISI]
Schou O. M. Philipp 1982 An unusual heteromorphic incompatibility system. II. Pollen tube growth and seed sets following compatible and incompatible crossing within Anchusa officinalis L. (Boraginaceae). In D. L. Mulcahy and E. Ottaviano [eds.], Pollen biology and implications for plant breeding. Elsevier Biomedical, New York, New York, USA
Stuppy W. 2002 Seed characters and classification of Opuntioideae. In D. Hunt and N. Taylor [eds.], Studies in the Opuntioideae (Cactaceae) Succulent Plant Research 6: 25-28
Tiagi Y. D. 1954 Studies in the floral morphology of Opuntia dillenii Haworth. 1. Development of the ovule and gametophytes. Botaniska Notiser 107: 343-356
Wredle U. B. Walles I. Hakman 2001 DNA fragmentation and nuclear degradation during programmed cell death in the suspensor and endosperm of Vicia faba. International Journal of Plant Sciences 162: 1053-1063[CrossRef]
Yampolsky C. H. Yampolsky 1922 Distribution of sex forms in the phanerogamic flora. Bibliotheca Genetica 3: 1-62
| ||||||||||||||||||||||||||||||||||||||||||||||||||
