Anther Wall Formation in Solanaceae Species

Abstract

Anther wall formation was studied in 32 species belonging to 27 genera of Solanaceae. Dicotyledonous and basic types of wall formation were observed, as well as several deviations due to subsequent periclinal divisions in the layers formed (middle layers and sometimes the endothecium). One type of wall formation was observed in each species. Some genera are uniform in their type of wall formation, while others are heterogeneous; a similar situation was observed at the tribal level. Summarizing all reported information on anther wall formation in the Solanaceae, 64 % of species show the basic type, while the remaining 36 % show the dicotyledonous type. Thus, neither type predominates, and no single type characterizes genera, tribes or the entire family.

INTRODUCTION

The anther wall is formed by a specific number of cell layers that originate in the earliest developmental stages. Davis (1966) observed different patterns of cell divisions starting in the first two hypodermal layers termed the secondary parietal layers. As a consequence of these divisions, all the wall layers are formed. Four different types of wall formation are recognized: basic, dicotyledonous, monocotyledonous and reduced (Davis, 1966). Many authors have used this classification when describing anther wall ontogeny (Swarajya Lakshmi and Pullaiah, 1989; Hardy and Stevenson, 2000; Strittmatter and Galati, 2000).

Davis (1966) affirmed that dicotyledonous anther wall formation characterized the Solanaceae, with one exception, Withania somnifera Dunal, which develops the basic type. The dicotyledonous type was subsequently observed in additional taxa (Bernardello, 1983; Alemany, 1985; Siddiqui and Khan, 1988), but the basic type has also been reported in other species (Prasad and Singh, 1978; Siddiqui and Khan, 1988; Carrizo García, 1998).

In the context of an extensive study of the androecium in the Solanaceae, a diverse group of species was analysed to determine their type of wall formation, as well as the frequency of each type at different hierarchical levels.

MATERIALS AND METHODS

A total of 32 species belonging to 27 genera was studied (Table 1). All materials examined are deposited at the spirit collection and the herbarium of the Botanical Museum of Cordoba, Argentina (CORD).

Table 1.

Species studied and collection data

Species	Collection data
Athenaea pereirae Barboza et Hunz.	Brazil, Hunziker 25203
Aureliana fasciculata (Vellozo) Sendtn.	Brazil, Hunziker 25147
Browallia americana L.	Colombia, Barboza 130
Brunfelsia australis Benth.	Argentina, cult. (Cordoba), CORD 318
Cestrum lorentzianum Griseb.	Argentina, Barboza et al. 157
Cyphomandra betacea (Cav.) Sendt.	Argentina, cult. (Buenos Aires), Carrizo García s.n.
Cyphomandra endopogon Bitter	Netherlands, cult. (Nijmegen), Carrizo García s.n.
Datura ceratocaula Ortega	Mexico, CORD 855
Duboisia myoporoides R. Br.	Netherlands, cult. (Nijmegen), Carrizo García s.n.
Dyssochroma viridiflorum (Sims) Miers	Brazil, cult. (Rio do Janeiro), Freire de Carvalho s.n.
Eriolarynx iochromoides (Hunz.) Hunz.	Argentina, Hunziker 25528
Exodeconus prostratus (L’Herit.) Raf.	Peru, Bernardello et Leiva 870
Fabiana patagonica Speg.	Argentina, Luti 9002
Hawkesiophyton panamense (Standl.) Hunz.	England, cult. (Birmingham), Hunziker s.n
Iochroma sp.	Argentina, cult. (Buenos Aires), Carrizo García s.n.
Leptoglossis linifolia (Miers) Griseb.	Argentina, A. A. Cocucci 243
Nicotiana glauca Graham	Argentina, CORD 582
Nicotianapaa Mart.‐Crov.	Argentina, Hunziker et al. 25524
Nierembergiabrowallioides Griseb.	Argentina, Hunziker 10094
Normaniatriphylla (Lowe) Lowe	Netherlands, cult. (Nijmegen), Carrizo García s.n.
Petuniaaxillaris (Lam.) Britton, Stern et Poggenb.	Argentina, CORD 583
Physochlainaorientalis G. Don	Netherlands, cult. (Nijmegen), van der Weerden s.n.
Saracha sp.	Netherlands, cult. (Nijmegen), Carrizo García s.n.
Schizanthusgrahamii Gill.	Argentina, A. A. Cocucci 105
Schwenckiaamericana L.	Argentina, CORD 589
Schwenckialateriflora (Vahl) Carvalho	Venezuela, Benítez de Rojas 5936
Solanumamericanum Mill.	Argentina, CORD 585
Solanumargentinum Bitter et Lillo	Argentina, CORD 581
Solanumglaucophyllum Desf.	Argentina, CORD 588
Streptosolenjamesonii (Benth.) Miers	Argentina, cult. (Capital Federal), CORD 405
Tubocapsicumanomalum (Franch. et Sav.) Makino	Netherlands, cult. (Nijmegen), Carrizo García s.n.
Vestiafoetida (Ruiz et Pav.) Hoffmann.	Netherlands, cult. (Nijmegen), Hunziker s.n.

For each species young buds of different sizes were fixed using FAA (formalin, ethilic alcohol and acetic acid), dehydrated, embedded in Paraplast™ and transversely sectioned using a microtome. The sections, 8–12 µm thick, were stained with Cresyl Brilliant Blue (modified from Pérez and Tomasi, 1997) or Cresyl Violet (D’Ambrogio, 1986). Sections were observed under a compound light microscope.

RESULTS

All the species examined showed the same type of wall formation until the development of the two secondary parietal layers, the outer and the inner. Anther wall formation types are defined on the basis of these two layers and subsequent cell divisions. Only the basic and the dicotyledonous types were observed in the samples analysed.

In the basic type of wall formation, all the cells in the secondary parietal layers divide once periclinally, forming four new layers (Fig. 1A and B). These layers differentiate, from outside to inside, into the endothecium, the two middle layers and the tapetum. The dicotyledonous type differs from the basic type in that only the outer secondary parietal cell layer divides periclinally (Fig. 1C). As a consequence, only three layers are formed: the endothecium, one middle layer and the tapetum. The endothecium and the middle layer are formed from the outer secondary parietal layer, and the tapetum is formed from the inner secondary parietal layer.

Fig. 1. Anther wall formation in Solanaceae. A and B, Basic type; C, dicotyledonous type; D and E, basic type with posterior divisions in the middle layers and/or endothecium (arrows); F, dicotyledonous type with posterior divisions in the middle layers (arrows). A, Nicotiana glauca; B and D, Solanum argentinum; C, Schwenckia americana; E, Hawkesiophyton panamense; F, Athenaea pereirae. Bar = 20 µm.

In a number of species, regardless of their wall formation type, new periclinal cell divisions may occur when the tapetum differentiates (Fig. 1D–F). These subsequent divisions do not modify the type of wall formation, since they occur at a later stage. However, a distinction is needed between the basic and dicotyledonous types in ‘stricto sensu’, in which the cell divisions are restricted to those specified for each type, and the basic and dicotyledonous types in which subsequent divisions occur. The subsequent divisions may occur in any of the hypodermal layers, except the tapetum, before they differentiate. In some species these divisions occur in the middle layer(s) (Fig. 1D and F), whereas in others they take place simultaneously in the future endothecium (Fig. 1E). In either case, these divisions usually do not occur in all the cells of every layer. The new cells and layers behave as middle layers.

Anther wall formation may thus be categorized as follows:

Basic type ‘stricto sensu’

Brunfelsia australis, Cestrum lorentzianum, Cypho mandra betacea, Cyphomandra endopogon, Fabiana patagonica, Iochroma sp., Leptoglossis linifolia, Nicotiana glauca (Fig. 1A), Nicotiana paa, Saracha sp., Schizanthus grahamii, Streptosolen jamesonii, Tubocapsicum anomalum and Vestia foetida.

Basic type ‘with subsequent divisions’

Aureliana fasciculata, Datura ceratocaula, Dyssochroma viridiflorum, Nierembergia browallioides and Solanum glaucophyllum: only one subsequent division in cells of the outer middle layer. More unusual in Aureliana fasciculata, Datura ceratocaula and Solanum glaucophyllum. Up to three middle layers will be formed.

Solanumargentinum: subsequent divisions are observed in the outer middle layer and/or the endothecium (Fig. 1D). Three or four middle layers are formed.

Hawkesiophyton panamense and Normania triphylla: the subsequent divisions may occur simultaneously in the two middle layers and in the endothecium. Up to six middle layers may be formed in Normania triphylla and nine in Hawkesiophyton panamense (Fig.  1E).

Dicotyledonous type ‘stricto sensu’

Browallia americana, Schwenckia americana (Fig. 1C) and Schwenckia lateriflora.

Dicotyledonous type ‘with subsequent divisions’

Athenaea pereirae (Fig. 1F), Duboisia myoporoides, Eriolarynx iochromoides, Exodeconus prostratus, Petunia axillaris, Physochlaina orientalis and Solanum americanum: subsequent divisions are observed in the middle layer. Eventually, other divisions occur in some endothecial cells, except in Athenaea pereirae. In general, two middle layers, rarely three, are formed.

DISCUSSION

Wall formation usually receives little attention in the study of anther ontogeny. With regard to the Solanaceae, wall formation has been studied in a few genera (Table 2). Data in this paper are reported for the first time for many genera (e.g. Streptosolen, Dyssochroma, Schizanthus, Normania, Tubocapsicum).

Table 2.

Types of wall formation in Solanaceae (species arranged according to Hunziker, 2001).

Taxon	Type of anther wall formation	Reference
Subfamily Anthocercidoideae
Tribe Anthocercideae
Duboisia myoporoides	Dicotyledonous*	This paper
Subfamily Cestroideae
Tribe Cestreae
Cestrum lorentzianum	Basic	This paper
Vestia foetida	Basic	This paper
Tribe Nicotianeae
Fabiana patagonica	Basic	This paper
Leptoglossis linifolia	Basic	This paper
Nicotiana tabacum, N. rustica	Basic	Jagannadham, 1988
Nicotiana glauca, N. paa	Basic	This paper
Nierembergia linariaefolia	Dicotyledonous*	Alemany, 1985
Nierembergia browallioides	Basic*	This paper
Petunia axillaris	Dicotyledonous*	This paper
Tribe Francisceae
Brunfelsia australis	Basic	This paper
Tribe Browallieae
Browallia americana	Dicotyledonous	This paper
Streptosolen jamesonii	Basic	This paper
Tribe Schwenckieae
Schwenckia americana, S. lateriflora	Dicotyledonous	This paper
Subfamily Juanulloideae
Tribe Juanulloeae
Dyssochroma viridiflorum	Basic*	This paper
Hawkesiophyton panamense	Basic*	This paper
Subfamily Schizanthoideae
Tribe Schizantheae
Schizanthus grahami	Basic	This paper
Subfamily Solanoideae
Tribe Nicandreae
Nicandra physalodes	Basic*	Prasad and Singh, 1978
Tribe Datureae
Brugmansia candida, B. suaveolens	Basic*	Carrizo García, 1998
Datura metel	Basic*	Thiagarajan, 1986
Datura discolor, D. ferox, D. inoxia, D. kimatocarpa,  D. leichhardtii, D. stramonium	Basic*	Carrizo García, 1998
Datura fastuosa, D. metel, D. stramonium	Dicotyledonous	Sharma, 1984
Datura ceratocaula	Basic*	This paper
Tribe Lycieae
Lycium cestroides	Dicotyledonous	Bernardello, 1983
Tribe Hyoscyameae
Hyoscyamus niger	Dicotyledonous*	Sharma et al., 1987
Physochlaina orientalis	Dicotyledonous*	This paper
Tribe Atropeae
Atropa belladonna, A. acuminata	Dicotyledonous*	Sharma et al., 1987
Tribe Solaneae
Athenaea pereirae	Dicotyledonous*	This paper
Aureliana fasciculata	Basic*	This paper
Cyphomandra betacea, C. endopogon	Basic	This paper
Cyphomandra sciadostylis	Dicotyledonous*	Sazima et al., 1993
Eriolarynx iochromoides	Dicotyledonous*	This paper
Exodeconus prostratus	Dicotyledonous*	This paper
Iochroma sp.	Basic	This paper
Normania triphylla	Basic*	This paper
Saracha sp.	Basic	This paper
Solanum cornutum, S. citrullifolium, S. integrifolium,  S. aethiopicum, S. opacum, S. sisymbrifolium, S. torvum	Dicotyledonous (some species*)	Siddiqui and Khan, 1988
Solanum americanum	Dicotyledonous*	This paper
Solanum argentinum, S. glaucophyllum	Basic*	This paper
Solanum bonariense, S. pseudocapsicum, S. surattense	Basic	Siddiqui and Khan, 1988
Solanum nigrum	Basic and dicotyledonous	Bhandari and Sharma, 1987
Tubocapsicum anomalum	Basic	This paper
Withania somnifera	Basic	Davis, 1966
Tribe Jaboroseae
Jaborosa sativa, J. bergii, J. integrifolia	Basic	Barboza, 1991
Jaborosa runcinata, J. odonelliana,   J. oxipetala, J. leucotricha, J. laciniata, J. kurtzii, J. rotacea,  J. lanigera, J. reflexa	Basic*	Carrizo García, 2000
Salpichroa origanifolia, S. tristis	Dicotyledonous	Carrizo García, 2000

Asterisks indicate cases in which subsequent divisions occur in the middle layers and/or endothecium (some inferred from the reference cited).

Davis (1966) defined wall formation types on the basis that ‘discontinuous variation, however, is apparent in the behaviour of the secondary parietal layers and, although the final product is an anther wall, it is achieved by a precise series of periclinal cell divisions’. This series of cell divisions (dicotyledonous and basic types ‘stricto sensu’) was observed in several of the species analysed (e.g. Schwenckia americana and Brunfelsia australis, respectively). However, irregular divisions subsequent to that series could be observed in other species.

Davis (1966) did consider the subsequent divisions, but these divisions are generally overlooked in descriptions of wall development, even when it can be deduced that they have occurred. For example, two middle layers are mentioned in the wall of Nierembergia linariaefolia Graham (syn = Nierembergia hippomanica Miers; Alemany, 1985), as well as in Atropa spp. (Sharma et al., 1987), although the dicotyledonous type is reported in both cases. In contrast, Prasad and Singh (1978) mentioned the subsequent divisions in Nicandra physalodes (L.) Gaertn. and reported that both secondary parietal layers divide, and the outer derivative continues dividing to form a five to six‐layered wall. These subsequent divisions cannot be ignored for several reasons. First, they highlight the different properties of the cells, such as the ability to divide. Secondly, the cell divisions determine the number of wall layers formed and, consequently, the wall structure (e.g. up to three middle layers in Nierembergia browallioides, and nine in Hawkesiophyton panamense). Finally, they show the difficulty in interpreting wall formation type because subsequent divisions may obscure the analysis and lead to incorrect conclusions. For instance, four layers are formed in the basic type ‘stricto sensu’; however, wall formation is not always of the basic type in all species with four layers since the four layers may have originated from the dicotyledonous type with one subsequent division. When summarizing all available information regarding anther wall formation in the Solanaceae, it is apparent that subsequent divisions are frequent within the family (asterisks in Table 2) although there is no apparent consistency within taxonomical groups.

It is worth mentioning that a single type of anther wall formation was observed in each species. The only exception reported in the Solanaceae to date is in Solanum nigrum L., in which basic and dicotyledonous types develop simultaneously in the same anther (Bhandari and Sharma, 1987).

With regard to the distribution of the types of wall formation in supraspecific taxa (Hunziker, 2001), several generalizations can be made (Table 2). Of the genera in which more than one species has been studied, Nicotiana seems to be relatively constant, although only four of the approx. 60 species have been examined (Jagannadham, 1988). The two Schwenckia species share the dicotyledonous type, being the first records for the genera. Other genera which to date have a uniform wall formation type include Brugmansia (Carrizo García, 1998) and Jaborosa (Barboza, 1991; Carrizo García, 2000) with the basic type, and Atropa (Sharma et al., 1987) and Salpichroa (Carrizo García, 2000) with the dicotyledonous type.

In contrast, other genera are heterogeneous (Table 1). The dicotyledonous type is reported in Cyphomandra sciadostylis Sendt. (Sazima et al., 1993), but the basic type occurs in C. betacea and C. endopogon. A similar situation is found in Nierembergia, where the basic type was observed in N. browallioides, whereas N. linariaefolia develops the dicotyledonous type (Alemany, 1985). Both types have been reported in species of Solanum (Siddiqui and Khan, 1988), and both types were found in the three species examined in this research.

The genus Datura is exceptional. Only one species was included in this study, Datura ceratocaula, whose wall formation type (basic) is the same as that of another six Datura species reported previously (Carrizo García, 1998). However, the dicotyledonous type (Sharma, 1984) and the basic type are reported in Datura stramonium L. and Datura metel L. [Carrizo García (1998) and Thiagarajan (1986), respectively]. Research is needed to resolve this problem.

At the tribal level, among non‐monotypic tribes, Nicotianeae, Browallieae and Solaneae appear to be heterogeneous, and contain both the dicotyledonous and the basic types (Table 2). The same situation has been reported previously in two other tribes, Datureae (Sharma, 1984; Thiagarajan, 1986; Carrizo García, 1998) and Jaboroseae (Carrizo García, 2000). In contrast, in the tribes Cestreae, Juanulloeae and Hyoscyameae the same type was found in the two genera analysed for each tribe (Table 2).

Of all the species studied to date (including data in the literature), and ignoring the subsequent divisions, 64 % show the basic type of anther wall formation, while the remaining 36 % develop the dicotyledonous type. In contrast to Davis’ suggestion (1966), the dicotyledonous type is less frequent than the basic type indicating that the dicotyledonous type does not characterize the family. In agreement with previous reports, the presence of both the basic and the dicotyledonous types of wall formation is confirmed in the Solanaceae. Neither type predominates, and no single type characterizes genera, tribes or the entire family.

ACKNOWLEDGEMENTS

I thank Drs G. Barboza and M. E. Carrizo García for critical revision, and Dr P. Hermann for encouragement. I am grateful to Consejo Nacional de Investigaciones Científicas y Técnicas and Agencia Córdoba Ciencia for financial support.

Received: 22 April 2002; Returned for revision: 6 August 2002; Accepted: 22 August 2002    Published electronically: 16 October 2002