Diplospory and obligate apomixis in albicans (Miconieae, ) and an embryological comparison with its sexual congener M. chamissois Author(s): Ana Paula Souza Caetano, Daniela Guimarães Simão, Renata Carmo-Oliveira and Paulo Eugênio Oliveira Source: Systematics and Evolution, Vol. 299, No. 7 (August 2013), pp. 1253-1262 Published by: Springer Stable URL: https://www.jstor.org/stable/23671349 Accessed: 06-07-2021 08:56 UTC

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This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:56:29 UTC All use subject to https://about.jstor.org/terms Plant Syst Evol (2013) 299:1253-1262 DOI 10.1007/s00606-013-0793-y

ORIGINAL ARTICLE

Diplospory and obligate apomixis in Miconia albicans (Miconieae, Melastomataceae) and an embryological comparison with its sexual congener M. chamissois

Ana Paula Souza Caetano • Daniela Guimarâes Simâo Renata Carmo-Oliveira • Paulo Eugenio Oliveira

Received: 28 November 2012/Accepted: 6 March 2013/Published online: 24 March 2013 © Springer-Verlag Wien 2013

Abstract Apomixis, or asexual reproduction Keywordsthrough Obligate apomixis • Melastomataceae seeds, has been reported for species of the tribe MiconiaMiconieae, • Embryology Melastomataceae, but details of the process have yet to be described. We analyzed and compared sporogenesis and gametogenesis in the apomictic Miconia albicans Introduction and the sexual M. chamissois. The results point to some differences between species, which were related to the apomicticApomixis is the asexual formation of embryos from process. In M. albicans microsporogenesis, problems maternal dur tissues of the ovule, leading to seed development ing meiosis and degeneration of its products led (Nogler to total 1984; Bicknell and Koltunow 2004). The apo pollen sterility, while M. chamissois presented mictic normal process can be viewed as a deregulation, in space bicellular pollen grains in the mature anther. The and absence time, of the sexual processes, leading to putative cell or abnormality of meiosis in M. albicans megasporogenesis fate changes and omission of critical steps in the sexual led to the formation of an unreduced embryo sac process and also(Koltunow and Grossniklaus 2003). Apomixis has to egg cell parthenogenesis, which gave rise tobeen the reported apo in approximately 33 families (Carman 1997) mictic embryo. Embryo and endosperm development and it wereis more ecologically and evolutionarily important autonomous, resulting in seeds and fruits independent than previously of thought (Allem 2004; Hôrandl 2010). But pollination and fertilization. Thus, in this species, morphological apomixis and embryological studies of apomixis have can be classified as diplosporic and obligate. In been contrast, concentrated in some groups of mostly temperate meiosis was as expected in the sexual M. chamissois, (Asker and and Jerling 1992; Koltunow 1993) and spe led to the development of a reduced embryo sac. cies Despite rich tropical groups with high incidence of apomixis the divergent pathways, many embryological characteris have yet to be studied in detail. tics were similar between the studied species and Melastomataceae other is a mostly Neotropical family, with Melastomataceae and they seem to be conservative ca. 4,500 char species in 150-166 genera (Clausing and Renner acter states for the family. 2001). It is very well represented in Brazil, with around 1,300 species, appearing in most biomes and plant forma tions (Baumgratz et al. 2010). Breeding system studies have showed a high frequency of apomixis in this family, especially in the tribe Miconieae Triana, with over 60 % of A. P. S. Caetano autonomous apomictics among approximately 59 species Programa de Pôs-Graduaçâo em Biología Vegetal, Instituto de Biología, Universidade Estadual de Campinas, studied so far (Goldenberg and Shepherd 1998; Santos Campinas, Sâo Paulo CEP 13083-970, Brazil et al. 2012). Apomictic species complexes, comparable to those reported in Asteraceae and Rosaceae, seem to occur D. G. Simíio • R. Carmo-Oliveira • P. E. Oliveira (El) in Miconieae (Goldenberg and Shepherd 1998). Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Minas Gérais CEP 38400-902, Brazil In Melastomataceae, apomixis seems to be related to e-mail: [email protected] polyploid (Goldenberg and Shepherd 1998; Caetano et al.

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2013) as in Fig. 1 Antherother morphology, microsporogenesis and microgametogen-apomictic | groups (Carman 1997; Savidan 2007). Moreover, esis of apomictic and sexual Miconia. a Bithecate the and tetrasporan apomictic species in this family fre giate anther of M. albicans, b Microsporanga of a young anther of quently presents M. chamissois: anther wall with epidermis, endothecium, low middle layer pollen grain viability or pollen ste rility (Goldenberg and secretory tapetum with uninucleate cells (arrowheads); note the and Shepherd 1998; Goldenberg and Varassin 2001;intersporangial septum (X) and connective Caetano with calcium oxalate et al. 2013). Apparently, adventi tious embryony crystals {arrows), c Mature anther of M. albicans (Subramanyam showing epidermis 1942, 1944, 1948; Borges and endothecium without parietal thickenings; note the intersporan 1991) and gial septumgametophytic degeneration (A), d Sporogenic cells of M. albicans. apomixis (Borges 1991; Caetano 2010) co-occur e Microspore mother cell surrounded in by callóse in Melastomataceae,M. chamissois. but the studies are still scarce. f Tetrahedral tetrads of microspores in M. chamissois evidencing In contrast, Melastomataceae presents many callóse wallsexual (g), h andMicrospore of M. chamissois. i Tetrad of M. albicans, j, k Tetrads and microspores degeneration in M. albicans. self-incompatible species (Goldenberg and 1 ShepherdAnther without 1998;any pollen in M. albicans, m Vacuolate microspore Goldenberg and Varassin 2001; Santos inet M. al. chamissois. 2012), n, proo Asymmetrical microspore mitosis in viding interesting opportunities for comparison M. chamissois. between p Newly formed pollen grain; q developing pollen congeneric apomictics and sexual species. grain and;Miconia r mature pollenalbi grain in M. chamissois. Ep epidermis, End endothecium, ML middle layer, GC generative cell, MMC microspore cans (Sw.) Triana and M. chamissois Naudin are common mother cell, SC sporogenic cell, Ta tapetum, V vacuole, VB vascular species in the Cerrado biome, the Neotropical bundle, VC vegetative savanna cell areas in Central Brazil. The breeding system of each spe cies has been determined using hand pollination experi ments: M. albicans is an apomictic species, in which obligate apomixis has been tentatively reportedrotary microtome. (Golden The sections were stained with toluidine berg and Shepherd 1998) and M. chamissois blue 0.05 is % a (Feder sexual, and O'Brien 1968). Observations and self-incompatible species (Santos et al. 2012). photomicrographs were made with Olympus BX51 Despite the number of apomictic species microscope recorded with for an attached DP70 digital camera. Some the family, detailed embryological studies slides are were still treated lacking with aniline blue and observed in an (Subramanyam 1942, 1944, 1948, 1951; Davis epifluorescence 1966; Johri microscope in order to verify callóse et al. 1992; Medeiros and Morretes 1996; Medeiros and deposition during spore and gametophyte development Roos 1996; Cortez and Carmello-Guerreiro 2008; Cortez (Kapil and Tiwari 1978). et al. 2012). Some species studied so far are from the tribe Miconieae, especially of the genus Miconia Ruiz & Pav. (Medeiros and Roos 1996; Cortez and Carmello-Guerreiro Results 2008; Cortez et al. 2012), but these studies did not focus on the origin of apomictic embryos in the family. We describe below the anther and ovule development and The aim of the present study was to investigate the early structure, detailing early embryology events and comparing embryology, comparing apomictic and sexual species of the apomictic and sexual pathways. Miconia (Miconieae, Melastomataceae) common in the Cerrado vegetation, defining the changes that trigger apo Androecium and anther wall anatomy mictic seed development. We found no significant difference between the species studied here in the androecium and anther wall anatomy. Materials and methods The androecium presented ten bithecate and tetrasporan giate anthers (Fig. la). The two sporangia in each theca The samples were collected between 2004 and were2007 separated in by a septum, formed by parenchymatic Cerrado areas of the Parque do Sabiá (PS) and Clube cells, Caçawhich degenerates during anthesis, forming a single e Pesca Itororó (CCPIU), in Uberlândia, Minas Gérais pollen sac (Fig. lb, c). In the connective, a single vascular State. Voucher specimens were deposited in the Herbarium bundle was surrounded by parenchymatic cells (Fig. la-c), Uberlandense (HUFU): M. albicans (R. Romero et al. which may present calcium oxalate crystals (Fig. lb). 8220) and M. chamissois (R. Romero et al. 8217). Anther wall, during microsporogenesis, was formed by Floral buds and fresh open flowers, and fruits were fixed the epidermis, endothecium, middle layer and secretory in either FAA or FAA with glutaraldehyde solutions (Jo tapetum, all uniseriate (Fig. lb). In the mature anther, the hansen 1940; Lersten and Curtis 1988). The material was epidermis and endothecium were the only parietal strata dehydrated through an ethanol series (Johansen 1940) and present (Fig. lc). embedded in Leica HistoResin (Gerrits and Smid 1983). The endothecium had initially one layer of cells similar Sections between 3.0 and 5.0 pm were obtained using a in size to those from the epidermal and middle layer. As the

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anther(s) developed, these cells increased, but they did not mother cells, and did not persist in the mature anther. The present parietal thickenings (Fig. lc). The middle layer tapetum was of the secretory type, with a single evident was obliterated during anther development, possibly due to nucleus during microsporogenesis (Fig. lb). This layer the increasing in size of both tapetal and microspores degenerated before microspore release.

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Microsporogenesis and microgametogenesis (Fig. 2a, b). But in the micropylar region, additional anti clinal divisions could occur, increasing the integument There were marked differences between the species, par- thickness in this region. A zigzag micropyle was formed by ticularly after meiosis. In M. albicans and M. chamissois both integuments (Fig. 2a). Only one vascular bundle the sporogenic tissue (Fig. Id), beneath the parietal strata, crossed the raphe and ended near the chalaza (Fig. 2b), proliferated until the cells reach meiotic prophase, differ- where small compact cells of dense cytoplasm, but no entiating into microspore mother cells (Fig. le). These lignification, formed the hypostasis. In M. chamissois, cells differed from the connective and parietal cells since parenchymal cells of the raphe that surrounded the vascular they were larger, with denser cytoplasm and more con- bundle accumulated phenolic compounds (Fig. 2b). spicuous nucleus. The microspore mother cells were sur- In both species, a cell situated right under the nucellar rounded by callóse deposition at the beginning of meiosis epidermis originated the sporogenic and parietal cells. This (Fig. le). Meiosis gave rise to tetrahedral tetrads (Fig. If), last one, through periclinal and anticlinal divisions, formed still surrounded by callóse (Fig. lg). There was no wall at least three parietal layers that eventually separated the formation between the first and second division of meiosis, megaspore mother cell from the nucellar epidermis, char resulting in simultaneous cytokinesis. With the dissolution acterizing the ovule as crassinucellate (Fig. 2c). The spo of the callóse, the microspores were released in the spo- rogenic cell differentiated into a megaspore mother cell, rangium (Fig. lh). which was elongated and presented a dense cytoplasm and In the apomictic M. albicans, it seems that some kind of prominent nucleus (Fig. 2c). In M. chamissois, this cell anomaly occurred during meiosis, at the end of the went through the first meiosis, forming a dyad, and the microsporogenesis, in such a way that all microspores were second meiosis, forming a linear tetrad of megaspores atypical and lacked cytoplasm (Fig. li, j). These microsp- (Fig. 2d). In M. albicans, we rarely observed the mega ores did not follow the normal development, as in the spore mother cell go through complete meiosis. We sexual species, but degenerated during the remainder of the observed megaspore mother cells and developing embryo anther maturation (Fig. Ik), so that the anther was almost sacs, but only in one case we found an ovule after under completely empty when the flower opened (Fig. 11). In going meiosis I forming a dyad (Fig. 2e), and in another M. albicans, viable pollen grains were never observed. case, after meiosis II, showing a linear tetrad of megasp In M. chamissois, microgametogenesis began with the ores (Fig. 2f), which were morphologically similar to that polarization of the microspore nucleus (Fig. lm). Con- observed in sexual M. chamissois. In this latter case the comitantly, a large vacuole developed in the microspore remaining chalazal megaspore presented two nucleoli, (Fig. lm). Each microspore divided asymmetrically evidence of endoreduplication or restitution. (Fig. In, o) forming a two-celled microgametophyte, the In M. chamissois, the chalazal megaspore was also the pollen grain, which contained a large central vegetative cell functional one and originated, through three mitotic divi and a small generative cell (Fig. lp). After mitosis, the sions, the embryo sac (Fig. 3a). In M. albicans the embryo generative cell was positioned along the pollen grain wall sac originated also by three successive mitoses, and was (Fig. lp). Then, it assumed a spherical shape, protruding structurally similar to the one found in M. chamissois into the cytoplasm of the vegetative cell (Fig. lq). In (Fig. 3b). In both species the embryo sac was of the Polyg mature anthers the generative cell became spindle shaped onum-type, formed by three antipodals, a large binucleate (Fig. lr). At anthesis, the bicellular pollen grains were shed central cell, two synergids and the egg cell (Fig. 3b-d). In the in monads (Fig. lr). basal portion of the synergids it was possible to distinguish the filiform apparatus (Fig. 3d). In M. albicans, the embryo Ovule characteristics, megasporogenesis developed parthenogenetically from the unreduced egg cell and megagametogenesis (Fig. 4a-d), since pollen was sterile and pollen tube growth was never observed. In this species, we also observed the Miconia albicans and M. chamissois exhibit very similar early development of an autonomous nuclear endosperm patterns of ovule development. Differences were found in (Fig. 4b-d). But the endosperm was never very conspicuous relation to megasporogenesis, since in M. albicans the in either species, and the surrounding nucellar cells seemed megaspore mother cell often did not go through complete to contribute to embryo nutrition, meiosis or the meiosis was unusual. But embryo sac development was similar between species, as was the final structure of the mature ovule and embryo sac. Discussion In both species the ovule was anatropous, bitegmic and crassinucellate (Fig. 2a). The outer and inner integuments Miconia albicans and M. chamissois present contrasting were formed, respectively, by two and three layers reproductive systems, which were associated with some

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Fig. 2 Ovule morphology and megasporogenesis in apomictic and functional megaspore with two nucleoli (arrows) and degeneration of sexual Miconia. a Longitudinal section of the ovule in M. albicans. three micropylar megaspores (arrowheads). DM dyad of megaspores, b Transversal section in M. chamissois. c Megaspore mother cell of ES embryo sac, 11 inner integument, M micropyle, MMC megaspore M. chamissois. d Linear tetrad of megaspores in M. chamissois. mother cell, Ol outer integument, R raphe, TM tetrad of megaspores, e Dyad and f tetrad of megaspores in M. albicans, with chalazal VB vascular bundle

differences during sporogenesis and gametogenesis. Apomixis-related characteristics Despite these differences, the two species shared most embryological characteristics, which seem to be constant in The presence of degenerating microspores inside the tetr the Melastomataceae. ads in M. albicans should be a result of some kind of

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Fig. 3 Megagametogenesis and embryo sac morphology of apomic mature embryo sac of M. chamissois. d synergids (filiform apparatus tic and sexual Miconia. a Tetranucleate embryo sac of M. chamissois. arrow) and egg cell in mature embryo sac of M. chamissois. b Mature embryo sac of M. albicans, c Egg cell and polar nucleus in A antipodes, EC egg cell, PN polar nuclei, S synergids chromosomal imbalance, which usually causes meiotic abnormalities during male meiosis, resulting in a high irregularities and lead to complete pollen sterility, as pre- proportion of non-viable pollen grains (Stebbins 1950; den viously observed in this species (Goldenberg and Shepherd Nijs and Menken 1996; Pagliarini 2000; Risso-Pascotto 1998; Cortez et al. 2012). Chromosomal studies for et al. 2006; Mogie et al. 2007). In Miconieae, abnormalities M. albicans indicate that samples from different regions during meiosis and resulting pollen inviability have been present distinct chromosome numbers (2n = 34 and described for M. fallax (Goldenberg and Shepherd 1998; 2n = 48), the latter sample being of polyploid origin (Soit Caetano et al. 2013), M. stenostachya (Goldenberg and and Wurdack 1980). Possibly, Melastomataceae species Shepherd 1998; Cortez et al. 2012), Clidemia bullosa and with broad distribution, such M. albicans, may vary in C. capitellata (Melo et al. 1999). ploidy level and degree of apomixis (Goldenberg and Low pollen viability in apomictics seems to be a com Shepherd 1998; Santos et al. 2012), explaining the differ- mon trend among autonomous apomictics in general ence in chromosomal number found in distinct populations. (Meirmans et al. 2006; Thompson et al. 2008) and among It is expected that polyploid plants, mainly allopolyploids, the apomictic species of Miconieae in particular (Golden originating from interspecific hybridization, present berg and Shepherd 1998; Goldenberg and Varassin 2001;

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Caetano et al. 2013). Unlike pseudogamic apomictics, The final apomeiotic or unreduced embryo sac in which depend on pollination for seed production (e.g., M. albicans was very similar to the one found in M. cha Mendes-Rodrigues et al. 2005), the production of viable missois. This result lends support to the idea that diplosp pollen grains is not necessary to ensure the reproductive oric apomictic species conserve the embryo sac success of those species, and, thus, there is reduced development mechanisms of their sexual relatives (Rut selective pressure for the maintenance of male function. ishauser 1982). Miconia albicans can be characterized as a species with The occurrence of gametophytic apomixis has been gametophytic apomixis of the diplosporic type, because the reported for other Melastomataceae. But while the occur embryo arises from the egg cell of an unreduced embryo rence of diplospory was indicated for Leandra australis sac (Koltunow 1993). Commonly, the meiosis is omitted (Borges 1991), M. fallax seems to develop aposporic and the megaspore mother cell enlarges and gives rise to an embryo sacs (Caetano, unpublished). As suggested by unreduced embryo sac only by somatic division. Another Rutishauser (1982), these gametophytic apomictic pro possibility in this species would be an endoreduplication cesses are not clear-cut and would not be a surprise if just before meiosis, as described in Allium (Hâkansson and different pathways coexist in the same group. Levan 1957; Ozias-Akins and van Dijk 2007), forming The complete pollen sterility and absence of pollen tube unreduced megaspores tetrads, or alternatively restitutional growth or fertilization described in this study, associated meiosis as described for Taraxacum (Van Baarlen et al. with high fruit and seed set (Goldenberg and Shepherd 2002), forming unreduced megaspores dyads. Although 1998) indicate autonomous and obligate apomixis in these processes appear to be rare, they may be important M. albicans. This is an important find, since some researchers since some recombination may occur during meiosis I and believe that obligate apomictics are exceptions in nature increase genetic variability of the offspring (Ozias-Akins (Asker 1979; Mogie 1992; Savidan 2007). Even in and van Dijk 2007). Taraxacum, which diplospory is similar to the observed

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This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:56:29 UTC All use subject to https://about.jstor.org/terms 1260 A. P. S. Caetano et al. here for M. albicans, presents obligate but also partially Melastomataceae from other families of , which apomictic populations (Richards 1997; van Baarlen et al. have tapetal cells bi or multinucleated (Tobe and Raven 2002). 1983). Endosperm development in M. albicans is also autono- Many ovule characteristics reported in this study are mous, i.e., not dependent on fertilization. Diplosporic basically the same as previously reported for Melastomat apomictics can show autonomous endosperm production, aceae: anatropous, crassinucellate, bitegmic ovules, non mainly in Asteraceae (Koltunow 1993), as Hieracium vascularized integument, inner integument formed by two (Koltunow et al. 1998) and Taraxacum (Cooper and Brink layers and micropyle formed by both integuments (Subr 1949; Van Baarlen et al. 2002). In sexual and apomictic amanyam 1942, 1951; Davis 1966; Borges 1991; Johri species of Melastomataceae, the endosperm does not et al. 1992; Medeiros and Morretes 1996; Cortez and develop significantly, cell wall formation does not occur, Carmello-Guerreiro 2008). However, the number of layers and the nuclear endosperm is quickly absorbed by the in the outer integument is a variable character state in the developing embryo (Subramanyam 1942, 1951; Johri et al. family (Subramanyam 1951; Medeiros and Morretes 1996) 1992). Moreover, the nucellar cells appear enlarged after or even within species (Cortez and Carmello-Guerreiro anthesis to be consumed later during the embryo devel- 2008). opment. In this case, the availability of nutrients from The patterns of megasporogenesis and megagameto surrounding nucellar cells could have facilitated the evo- genesis observed—linear tetrad of the megaspores, chala lution of the autonomous apomixis in this group. zal functional megaspore and Polygonum-type embryo sac—are also found in other Melastomataceae (Subr Embryological patterns amanyam 1942, 1951; Davis 1966; Borges 1991; Johri et al. 1992; Medeiros and Morretes 1996). Ephemeral Besides the breeding system differences associated with antipodals, which degenerate during anthesis are not only a specific stages of early embryology, both species presented feature of the family (Subramanyam 1942, 1951; Davis morphological and embryological features typical of the 1966; Borges 1991; Johri et al. 1992; Medeiros and Mor Melastomataceae. retes 1996), but represent an embryological characteristic Bithecate and tetrasporangiate anthers are the common which defines the Myrtales as a whole (Tobe and Raven pattern described to Melastomataceae (Subramanyam 1983). 1942, 1951; Venkatesh 1955; Tobe and Raven 1983; Medeiros and Morretes 1996; Medeiros and Roos 1996), Concluding remarks with exception of some Microlicia species, which can present polysporangiate anthers (Baumgratz et al. 1996). Despite embryological and morphological general simi The presence of a non-fibrous endothecium is the most larities, there were specific differences between the studied common character state in anthers of Melastomataceae species, which explain their contrasting breeding systems. (Renner 1993; Medeiros and Morretes 1996; Medeiros and In the one hand, M. chamissois normal sexual patterns of Roos 1996; Caetano and Cortez, unpublished). However, sporogenesis and gametogenesis gave rise to viable pollen there is some variation in this group, since endothecial wall grains and a reduced Polygonum-type embryo sac. On the thickening is reported for Sonerila (Johri et al. 1992). other hand, in M. albicans microsporogenesis, degenera In Melastomataceae the middle layer of the anther can tion of meiotic products causes total pollen inviability. vary in number of layers, from one in Miconia (Subr- During the megasporogenesis, absence or abnormal meio amanyam 1942, 1951; Tobe and Raven 1983; Medeiros sis led to an unreduced embryo sac and an embryo origi and Morretes 1996; Medeiros and Roos 1996) up to seven nated by egg cell parthenogenesis. Due to pollen sterility layers, as in Melastoma malabathricum (Johri et al. 1992). and autonomous diplospory, M. albicans is an obligate We believe that in this family, additional divisions in the apomictic species, presenting only asexual reproduction, middle layer may be related to the size of anthers, since This has ecological consequences since it allows repro M. malabathricum has much larger flowers than Miconia duction by seeds, independent of pollinators, and possibly (Medeiros and Morretes 1996; Caetano, personal leads to large uniparental clonal populations. This may be observation). important, since Miconia species are very frequent in dis Tapetum of the secretory type, with uninucleate cells, turbed areas, where the presence of pollinators would not simultaneous type in microspore mother cells cytokinesis be reliable. The apomixis in these cases would favor col and tetrahedral tetrad, also are recurrent characteristics of onization (Stebbins 1950; Richards 1997) and explain the Melastomataceae (Subramanyam 1942, 1951; Johri et al. wide distribution of many apomictic Melastomataceae 1992; Medeiros and Morretes 1996; Medeiros and Roos (Santos et al. 2012). This also facilitates persistence in the 1996). Moreover, uninucleate tapetal cell distinguishes the Cerrado region, the main agricultural frontier in Brazil,

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This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:56:29 UTC All use subject to https://about.jstor.org/terms Diplospory and obligate apomixis in Miconia albicans 1261 which is under increasing fragmentation Feder N, O'Brien TP (1968)and Plant disturbance microtechnique: some principles and new methods. Am J Bot 55:123-142 pressure (Klink and Machado 2005). Gerrits PO. Smid L (1983) A new, less toxic polymerization system for the embedding of soft tissues in glycol methacrylate and Acknowledgments The research was supported subsequent preparing by ofConselho serial sections. NacJ Microsc 132:81-85 ional de Desenvolvimento Científico Goldenberg e Tecnológico R, Shepherd GJ (CNPq).(1998) Studies We on the reproductive thank Diana Sampaio, Simone Pádua Texeira, biology of Melastomataceaeand Clesnan in "cerrado" Mendes vegetation. Plant Syst Rodrigues for critical reading of different versionsEvol 211:13-29 of this manuscript. 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