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Seed characters and their usefulness in the separation of Asteraceae species/Caracteres de sementes e sua utilidade na separacao de especies de Asteraceae.

Introduction

While most botanists are satisfied with external features of the achene and a few researches have analyzed the development of the embryo and ovule, little attention has been given to the seed-coat of Asteraceae (Compositae) (CORNER, 1976). However, this author complements that the seed-coat not completely deteriorate in the achene but has retained an exxotestal palisade (Cynareae), a variety in the thickening of the exotestal cells, in the retention of the mesophyll and in the vascular supply.

Pallone and Souza (2014) showed that the seeds of Crepis japonica (L.) Benth., Porophyllum ruderale (Jacq.) Cass. and Tridax procumbens L. consist of endothelium in the developing seeds, and the seedcoat does not completely deteriorate in the cypsela of the three species, mainly in C. japonica, which has exotestal seed composed of thick-walled cells.

Besides the intrinsically interesting features of the cypsela (achene) structure, we sought to contribute to a better understanding of the seed characters of nine Asteraceae species, which occur with relative frequency as weed plants in Brazil. An attempt is made to answer the question concerning the usefulness of the seed characters in the separation of these species of Asteraceae.

Material and methods

Developing flowers and cypselas of nine Asteraceae species: Cosmos sulphureus Cav., Eclipta alba Hassak., Elephantopus mollis Kunth, Emilia sonchifolia (L.) DC., Erechtites valerianifolius (Link ex Spreng.) DC, Galinsoga quadriradiata Ruiz & Pav., Parthenium hysterophorus L., Praxelis clematidea (Griseb.) R. M. King & H. Rob. and Sigiesbeckia orientalis L. (all listed in Table 1) were collected in the region of Maringa, Parana State, Brazil. Voucher material was deposited in the UEM Herbarium (HUEM).

Flower and fruit samples were fixed in glutaraldehyde 24 hours (1% in 0.1 M phosphate buffer, pH 7.2). These were dehydrated and embedded in historesin Leica according to the method of Guerrits (1991). Sections were serially cut from the embedded samples with a rotary microtome to the thickness 8-12 fim. Sections were stained with 0.05% Toluidine Blue, pH 4.7 (O'BRIEN et al., 1964). Light microscope photographs were taken with a Leica EZ4D digital camera, and subsequently processed using the software Leica Application Suite 1.8. The following stains and reagents were used for specific color tests: Iodine-Potassium Iodide Test, for starch; Sudan IV, for lipids; and Ferric Chloride for phenolic substances (JOHANSEN, 1940; RUZIN, 1999).

Results

Developing seed

Seeds originate from anatropous, unitegmic and tenuinucellate ovules (Figure 1A). Ovules are sessile, but Sigiesbeckia orientalis has a short funicle (Figure 1B). The vascular supply of the ovules has postchalazal course (Figure 1C). The integument consists of outer epidermis with narrow and tangentially elongated cells and (Figure 1C) in the micropyle region the cells are short and quadrilateral. The multiseriate parenchyma mesophyll is made up of polygonal and large cells, eventually elongated attached to the outer epidermis (Figure 1C). The integument inner epidermis shows cuboid or slightly prismatic cells (Figure 1C). The hypostase is well-defined in the chalaza by the cells more densely stained (Figure 1C). More developed ovules undergo longitudinal elongation (Figure 1D).

Young seeds also show a hypostase and the inner epidermis cells become specially differentiated in endothelium, in which the cells have pronounced radial elongation and more intense staining (Figure 1E).

Ovary general view with a single ovule in longitudinal section. B. Ovule with short funicle in longitudinal section. C. Detail of chalazal and micropylar region of the ovule in longitudinal section. D. Longitudinal section of the ovary and more developed ovule. E. Cross section of the young seed showing the mesotesta and endotesta (endothelium) (black asterisk). Outer ovule epidermis (white arrow-head), inner ovule epidermis (black arrow-head), procambial strand with postchalazal branches (white arrow), hypostase (white asterisk), mesophyll (double arrow), ovary (ov) and ovule (ou).

Internally to the inner epidermis, there are mesotesta cells, which are more stained than the other cells (Figure 1E) and later are crushed (Figure 2A). The partial collapse of the developing seed coat is a common feature in the studied species of Asteraceae. Subepidermal mesotesta, inner epidermis and central cells of the chalazal region undergo collapse in the nine species (Figure 2B). As consequence, the embryonic cavity increases in size to some extent (Figure 2B).

Outer epidermis of the developing seed coat of Elephantolus mollis (Figure 2C) and Parthenium hysterophorus is strikingly different from the other species herein investigated, due to the thickened cell walls.

Endosperm formation in the analyzed nine species is of the cellular type (Figure 2D), in which ontogenetic seed studies are needed to precisely evaluate the endosperm type. Abortive seeds were found in Emilia sonchifolia (Figure 2E and F), Cosmos sulphureus and Praxelis clematidea.

Ripe seed

The testa is formed of crushed and thin-walled cells in almost all of the species studied here, but the cellular collapse is more pronounced in seeds of Eclipta alba, Emilia sonchifolia (Figure 3A) and Sigiesbeckia orientalis, except for the located cells in the raphe region. On the other hand, seeds of Elephantopus mollis and Parthenium hysterophorus (Figure 3B) showed exotesta cells with U-shaped thickening.

The endosperm persists in the ripe seed, and it is composed of one or two layers of relatively thick-walled cells (Figure 3A, B, C and E).

All nine species have seed vasculature consisting of a single collateral vascular bundle that terminates blindly in the proximities of the micropyle. The embryo of the nine Asteraceae species is erect, and consists of two cotyledons with homogeneous mesophyll (Figure 3C), plumule with leaf primordia (Figure 3D), and hypocotyl-radicle axis relatively long (Figure 3E).

Discussion

Ovules and young seeds of the analyzed species maintain the structural pattern observed in Asteraceae (Compositae) (CORNER, 1976). The endothelium is normally restricted to tenuinucellate and generally unitegmic ovules and it is registered in Asteranae (DAHLGREN, 1991) and (CORNER, 1976; BOUMAN, 1984). In several Asteraceae species, the endothelium was reported, for instance, in Vernonia platensis (Spreng.) Less. (GALASTRI; OLIVEIRA, 2010), C. japonica, P. ruderale and T. procumbens (PALLONE; SOUZA, 2014), and it is apparently involved with several processes (WERKER, 1997). There seems to be no doubt that the endothelium is a nutritive layer, whose main role is to work as an intermediate for the transport of nutrients from the integument to the embryo sac (MAHESHWARI, 1971). In a literature review on endothelium, Werker (1997) suggests several functions for this tissue, such as transference of nutrients, temporary accumulation of nutrients, ability to act in metabolizing dissolved products in its own cells, secretion of digestive enzymes, and also act as a limiting barrier, preventing the embryo and endosperm from excessive growth. The presence of endothelium may be considered a derived character (VON TEICHMAN; VAN WIK, 1991).

The collapse of the integument and the increase in the cavity, observed in the nine species, were also evidenced in other species, as Vernonia cinerea Less. (PANDEY; SINGH, 1980), Schlechtendalia luzulifolia Less. (MELLO et al., 2009), Vernonia platensis (Spreng.) Less. (GALASTRI; OLIVEIRA, 2010), C. japonica, P. ruderale and T. procumbens L. (PALLONE; SOUZA, 2014).

The endosperm is of the cellular type, however Dahlgren (1991), mentioning Wunderlich (1959), argued that the endosperm formation in Asteraceae is surprisingly variable, suggesting that both the cellular and the nuclear types are associated with most Asteraceous tribes, and are also reported for many genera, which is extremely unusual in eudicots. Other authors, such as Singh (1964) and Corner (1976), also indicate both the cellular and nuclear types of endosperm for the family.

Seed abortion was observed in fruits of Emilia sonchifolia, Cosmos sulphureus and Praxelis clematidea. Chican and Palser (1982) speculated that the proliferation of the endothelium, failure in embryo formation, and failure in endosperm development seem to be either directly or indirectly involved in abortion of seeds at early stages of development of Cichorium intybus L. The occurrence of self-incompatibility, which is common in Asteraceae (HEENAN et al., 2005-nao consta ne referencia), seems to be a cause of seed abortion. Evidently, all these possible factors in seedless cypselas should be investigated in the species here studied.

The chief protective function for the embryo with unspecialized seed coat (thin-walled and collapsed cells) seems to be exercised by the pericarp wall of the cypsela (achene). In this case, the pericarp wall may to substitute the seed coat which is rather obliterated during the development. The transfer of protecting function of the embryo was already enhanced for Julio and Oliveira (2008). It is probable that in E. mollis and P. hysterophorus, which have exotesta with secondary thickening, the seed coat furnishes additional protection to the embryo. Among the Asteraceae, Wedelia calendulacea Rich. (PANDEY; SINGH, 1994) and C. japonica (PALLONE; SOUZA, 2014) also have exotesta with thick-walled cells. Pandey and Singh (1994) referred to fibrous layers in the seed coat of species belong to the tribes Eupatorieae and Heliantheae.

One or two layers of endosperm of the nine species of Asteraceae persist in the mature seed with cell walls relatively thick. The occurrence of endosperm in mature seeds is also known in Helichrysum bracteatum Andr. and Vicoa indica DC (PANDEY; SINGH, 1983), and P. ruderale and T. procumbens (PALLONE; SOUZA, 2014). It is likely that the persistent endosperm protects the embryo, mainly in the seeds which do not have a specialized seed coat, if the suggestions of Souza and Paoli (2009), who consider the protective function of the endosperm for Bignoniaceae seeds, are taken into consideration.

According to Corner (1976) the vascular supply of Asteraceae (Compositae) could help to solve infrafamilial relationships, and the author proposed three vascular supply states for the families, which may be useful for separation of genus. The seeds of the species analyzed in this study belong to the type I (CORNER, 1976), which is characterized by the "vascular supply as a single bundle extending round the seed from the funicle more or less to the micropyle".

The Spatulate embryo, according to Martin (1946) classification, is defined as "[...] embryo erect; cotyledons variable, thin to thick and slightly expanded to broad; stalk not invested by cotyledons or only slightly so [...]".

The possible relevance of the seed characters in the separation of the nine species of Asteraceae, as suggested by Corner (1976), was not satisfactorily evidenced (as shown in the Table 2). On the contrary, the analysis revealed high uniformity in these characters. Although the number of analyzed species is insufficient, it is important to note that the exotesta with thick-walled cells seems to be relevant in the species of the two genera of the subfamily Cichorioideae (Elephantopus and Crepis) (PALLONE; SOUZA, 2014). This same exotesta character is exhibited in the tribes Asteroideae, Heliantheae (Wedelia) (PANDEY; SINGH, 1994) and Senecioneae (Emilia), but it was not verified in the genera Heliantheae (Cosmos, Eclipta, Galinsoga, Parthenium and Sigesbeckia) studied here.

Doi: 10.4025/actascibiolsci.v37i4.27964

Acknowledgements

We thank CAPES (Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior, Brazil) and CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico, Brazil) for funding this research.

References

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CORNER, E. J. H. The seeds of dicotyledons. Cambridge: University Press, 1976.

CHICAN, M. A.; PALSER B. F. Development of normal and seedless achenes in Cicorium intibus (Compositae). American Journal of Botany, v. 69, n. 06, p. 885-895, 1982.

DAHLGREN, G. Steps toward a natural system of the dicotyledons: embryological characters. Aliso, v. 13, n. 1, p. 107-165, 1991.

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HEENAN, P. B.; SMISSEN, R. D.;DAWSON, M. I. Self-incompatibility in the threatened shrub Oleria adenocarpa (Asteraceae). New Zealand Journal of Botany, v. 43, n.4, p. 831-841, 2005.

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MELLO, M. C.; FIOR, C. S.; OLIVEIRA, J. M. S. Anatomia do fruto de Schlechtendalia luzulifolia Less. (Barnadesioideae, Asteraceae Bercht. & J. Presl). Iheringia: serie botanica, v. 64, n. 1, p. 77-80, 2009.

O'BRIEN, T. P.; FEDER, N.; MCCULLY, M. E. Polychromatic staining of plant cell walls by toluidine blue. O Protoplasma, v. 59, n. 2, p. 368-373, 1964.

PALLONE, S. F.; SOUZA, L. A. Pappus and cipsela ontogeny in Asteraceae: structure considerations of the tribal category. Revista Mexicana de Biodiversidad, v. 85, n. 1, p. 62-77, 2014.

PANDEY, A. K.; SINGH, R. P. Development and structure of seeds and fruits in tribe Vernonieae: some Vernonia and Elephantopus species. Flora, v. 169, n. 1, p. 443-452, 1980.

PANDEY, A.K., SINGH, R. P. Development and structure of seeds and fruits in Compositae: tribe Eupatorie. Journal of the Indian Botanical Society, v. 62, n. 1, p. 276-28, 1983.

PANDEY, A. K.; SINGH, R. P. Development and structure of seed and fruit in Eupatorieae and Heliantheae (Compositae). Proceedings of the National Academy of Sciences of India, v. 64, n. 1, p. 115-126, 1994.

RUZIN, S. E. Plant microtechnique and microscopy. Oxford University Press, New York, 1999.

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Received on May 26, 2015.

Accepted on August 6, 2015.

Michelli Fernandes Batista (1) *, Luciane da Silva Santos (1), Rafael Hespanhol Muller (2) and Luiz Antonio de Souza (2)

(1) Programa de Pos-graduacao em Biologia Comparada, Centro de Ciencias Biologicas, Universidade Estadual de Maringa, Avenida Colombo, 5790, 87020-900, Maringa, Parana, Brazil. (2) Departamento de Biologia, Centro de Ciencias Biologicas, Universidade Estadual de Maringa, Maringa, Parana, Brazil. * Author for correspondence. E-mail: mfernandes_2@hotmail.com

Table 1. Sp ecies from Asteraceae collected at Maringa, Parana
State, Brazil.

Species                           Habit    Accession number

Cosmos sulphureus Cav.           Shrubby      18589 HUEM
Eclipta alba (L.) Hassk.          Herb        18587 HUEM
Elephantopus mollis Kunth         Herb        18588 HUEM
Emilia sonchifolia (L.) DC.       Herb        18586 HUEM
Erechtites valerianifolius        Herb        21182 HUEM
(Link ex Spreng.) DC.
Galinsoga quadriradiata           Herb        18590 HUEM
Ruiz & Pav.
Parthenium hysterophorus L.       Herb        20828 HUEM
Praxelis clematidea (Griseb)      Herb        21181 HUEM
R. M. King & H. Rob.
Sigesbeckia orientalis L.         Herb        20836 HUEM

Table 2. Significant features in seed characterization
of the nine species of Asteraceae.

Species                        Presence of         Seed coat
                                 funicle           (exotesta)

Cosmos sulphureus                Sessile       Non - specialized
Eclipta alba                     Sessile       Non - specialized
Emilia sonchifolia               Sessile      Secondary thickening
Elephantopus mollis              Sessile      Secondary thickening
Erechtites valerianifolius       Sessile       Non - specialized
Galinsoga quadriradiata          Sessile       Non - specialized
Parthenium hysterophorus         Sessile       Non - specialized
Praxelis clematidea              Sessile       Non - specialized
Sigesbeckia orientalis        Short funicle    Non - specialized
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Title Annotation:texto en ingles
Author:Batista, Michelli Fernandes; Santos, Luciane da Silva; Muller, Rafael Hespanhol; de Souza, Luiz Anto
Publication:Acta Scientiarum. Biological Sciences (UEM)
Date:Oct 1, 2015
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