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The Stomatal Ontogeny and Structure of the Liassic Pteridosperm (Caytoniales) from Hungary

Article in International Journal of Sciences · February 2000 Impact Factor: 1.53 · DOI: 10.1086/314240 · Source: PubMed

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All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Maria Barbacka letting you access and read them immediately. Retrieved on: 14 April 2016 Int. J. Plant Sci. 161(1):149–157. 2000. ᭧ 2000 by The University of Chicago. All rights reserved. 1058-5893/2000/16101-0016$03.00

THE STOMATAL ONTOGENY AND STRUCTURE OF THE LIASSIC PTERIDOSPERM SAGENOPTERIS (CAYTONIALES) FROM HUNGARY

Maria Barbacka1 and Ka´roly Bo´ka

Botanical Department of the Hungarian Natural History Museum, P.O. Box 222, H-1476 Budapest, Hungary; and Eo¨tvo¨s Lora´nd University, Department of Plant Anatomy, Puskin u. 11-13, H-1088 Budapest, Hungary

Stomatal ontogeny is often inferred but rarely documented for extinct because it requires observations from young leaves that are rarely preserved as . The discovery of several very young leaves of the plant Sagenopteris (Caytoniales) in the Mecsek Mountains (southern Hungary) in a good state of preservation provides the opportunity for studying the stomatal ontogenesis of this genus. The specimens show perigenous anomocytic stomata. This feature confirms the evolutionarily high position of Sagenopteris among fossil and supports the opinion that the ancestors of angiosperms and some groups of pteridosperms might be closely related. Such clear examples of stomatal development have not previously been documented for fossil material.

Keywords: paleobotany, Early Jurassic, pteridosperms, Sagenopteris, ontogeny of stomata.

Introduction ported by direct observations of ontogeny but inferred from mature developed stomata. The examination of stomatal structure and ontogeny be- Different systems of stomatal classification have been gan at the end of the nineteenth century. In 1888 I. P. Bo- proposed from both ontogenetic and morphologic points rodin (Borodin 1900) and in 1889 M. J. Vesque (Vesque of view (Pant 1965; Fryns-Claessens and Cotthem 1973; 1889) were the first botanists who paid attention to the Wilkinson 1979; Rasmussen 1981). Some authors also in- origin of stomata and its importance in plant sciences. Sto- vestigated the structure and ontogeny of stomata in some matal ontogeny of living plants has both been applied to recent pteridophytes like filicales (Cotthem 1970) and Se- the investigations of epidermal anatomy and taxonomy and laginella (Brown and Lemmon 1985), which contributed used in assessing the evolutionary and phylogenetic rela- greatly to the understanding of the evolution of stomata. tionships between different groups of plants. Such studies This article illustrates the ontogeny of young Sagenop- are most easily carried out on extant plants, whose young teris stomata in different stages of their development, based leaves are readily available for examination of epidermal on actual observations in young leaves. These observations, ontogeny. Unfortunately, young fossil leaves are extremely which are based on stomatal ontogeny, provide a solid basis rare; moreover, they are very delicate and easily destroyed for a classification of the stomata according to the existing during fossilization. Therefore, it is rarely possible to in- systems (Pant 1965; Fryns-Claessens and Cotthem 1973; vestigate the stomatal ontogeny of extinct plant groups that Wilkinson 1979) and, thus, for the discussion of the evo- preceeded the appearance of angiosperms. lutionary implications of their development. Despite these difficulties, some authors have attempted to interpret the structure and classify the mature stomata Material and Methods in some genera of fossil plants. They described the presumed stomatal ontogeny of recent and fossil and bennet- titalean species, based on observations of adult leaves in Material was collected in the Mecsek Mountains (region of connection with other gymnosperms such as or Komlo´ , southern Hungary), on the dump of a coal mine work- Coniferales (Thomas and Bancroft 1913; Harris 1932; Pant ing in Early Jurassic (Hettangian) deposits. The flora is pter- and Mehra 1964). Krasilov (1978) created an overview of idosperm dominated and accompanied by , species of the structure of fully developed stomata in different gym- Coniferales, and Ginkgoales. Among the pteridosperms the nospermous groups and some genera of angiosperms. most frequent are leaves of Komlopteris nordenskioeldii (Bar- Florin was the first to develop a useful system for the backa 1994) and Ctenozamites cycadea (Barbacka 1997). Sa- phylogenetic classification of stomatal types for gymno- genopteris is represented by three species: S. nilssoniana, S. sperms including Coniferales, Ginkgoales, Cycadales, Gne- hallei, and S. pilosa (Barbacka 1992). Sagenopteris is the only tales, and Bennettitales (Florin 1931, 1933, 1934). This genus of which young leaves were found in such a large num- system, however, in the case of fossil plants, was not sup- ber. However, their characteristics are not clear enough for more exact determination. Thirty-two very young leaves of Sagenopteris were collected. 1 Author for correspondence. Their length varies from 4 to 16 mm (with petiole); the length Manuscript received April 1998; revised manuscript received August 1999. of the leaflets ranges from 2 to 12 mm (figs. 1, 2). For com-

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Fig. 1 Juvenile leaves of Sagenopteris sp., collection of Hungarian Nat. Hist. Mus. Budapest. Fig. 1.1, BMP 96.281.1.A; fig. 1.2, 96.281.1.B; fig. 1.3, 96.277.1.A; fig. 1.4, 96.270.1.C; fig. 1.5, 96.270.1.B; fig. 1.6, 96.270.1.A; fig. 1.7, 96.295.1; fig. 1.8, 96.279.1; fig. 1.9, 96.280.2; fig. 1.10, 96.494.1; fig. 1.11, 96.496.1.A; fig. 1.12, 96.496.1.B; fig. 1.13, 96.287.1.B; fig. 1.14, 96.507.1; fig. 1.15, 96.508.1; fig. 1.16, 96.286.1.C; fig. 1.17, 96.288.1; fig. 1.18, 96.276.1.A; fig. 1.19, 96.305.1.C; fig. 1.20, 98.24.1; fig. 1.21, 96.276.1.B; fig. 1.22, 96.513.1.B; fig. 1.23, 96.509.1; fig. 1.24, 98.16.2; fig. 1.25, 98.18.1; fig. 1.26, 98.8.1; fig. 1.27, 98.4.1.C; fig. 1.28, 96.399.1.C; fig. 1.29, 98.17.1; fig. 1.30, 96.403.1.H; fig. 1.31, 96.496.1.I; fig. 1.32, 96.378.1. Figs. 1.33–1.35, The intermediate and developed leaves of Sagenopteris sp.; fig. 1.33, 96.513.1.D; fig. 1.34, 96.278.1.A; fig. 1.35, 96.331.1. fig. 1.36, one pinnule of the developed leaf of Sagenopteris sp. 96.60.1. All pictures natural size. parison, the average length of normally developed leaflets from amined under a light microscope and a Nomarski differential- the same locality reaches 20–70 mm (even to 90 mm or more; interferential-contrast microscope. In addition, an especially figs. 1.33–1.36). It was surprising that the cuticle of the sam- well-preserved cuticle of an adult leaf was examined with SEM. ples examined was much better preserved than those of the mature leaves, which are typically very delicate and difficult Observations and Results to prepare. This enabled us to obtain relatively large pieces of cuticle for investigations. The cuticle was prepared in the usual The predominant characteristic discovered in the juvenile way in Schulze’s solution (Stace 1965). The cuticles were ex- leaflet cuticles was a significant number of just-divided cells BARBACKA & BO´ KA—THE STOMATAL ONTOGENY OF SAGENOPTERIS 151

Fig. 2 Juvenile leaves of Sagenopteris sp. Fig. 2.37, 96.399.1.C; fig. 2.38, 96.279.1; fig. 2.39, 98.4.1.C; fig. 2.40, 98.5.1; fig. 2.41, 96.494.1; fig. 2.42, 96.280.2; fig. 2.43, 96.287.1.B; fig. 2.44, 96.305.1.C. on both the lower and upper cuticles. The cells of the upper ranging from small (25 mm) to large (42 mm) and from cuticle are larger and more rectangular in shape than those rounded to elongated (figs. 3.52–3.54, 4.55). of the lower cuticle. They are also often arranged in rows Particular ontogenetic stages are visible in different slides due to multiple division of cells (fig. 3.45). of different specimens. In this way a nearly complete onto- On the lower cuticle, cells are smaller and rather rounded, genetic sequence of developing stomata could be followed. with numerous simple hair bases. In some cases papillae are In the first observed stage, the mother guard cell divides into present. Stomata are rare, and they vary in size and shape, two equal cells (fig. 3.46). Following this, the cells become 152 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 3 Cuticle of the juvenile leaves of Sagenopteris sp. Fig. 3.45, Upper cuticle (96.295.1, slide 795). Figs. 3.46–3.52, Lower cuticle, sequence of the stoma developing. Figs. 3.53–3.54, Mature stomata (fig. 3.46, 96.277.1.A, slide 780; fig. 3.47, 96.295.1, slide 795; fig. 3.48, 96.313.1, slide 904; fig. 3.49, 96.270.C, slide 778; figs. 3.50–3.51, 96.295.1, slide 793; fig. 3.52, 96.313.1, slide 904; figs. 3.53–3.54, 96.289.1, slide 908). BARBACKA & BO´ KA—THE STOMATAL ONTOGENY OF SAGENOPTERIS 153

Fig. 4 Inner side of the lower cuticle, mature stomata of Sagenopteris sp. (BMP 89.231.1.B); SEM pictures 154 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 5 Sagenopteris sp. (BMP 89.231.1.B), mature stomata. Fig. 5.59, the outer side of the cuticle; fig. 5.60, the inner side of the cuticle, stoma with remains of the inner wall of the guard cells. SEM pictures. more and more semicircular in shape, and the new cell wall rangements in the case of Sagenopteris seem to be only thickens (figs. 3.47, 3.48). The T-pieces become visible at the accidental. future poles (fig. 3.49). In the next stage, the shape of the young guard cells approaches that of mature cells (figs. 3.50, Discussion 3.51). This state probably comes immediately before the sto- matal pore is formed. The completely developed stoma (figs. Although Sagenopteris belongs to an extinct group of 3.52–3.54, 4, 5) possesses kidney-shaped guard cells with plants, the observed process of stomatal ontogeny now al- poles lying on the same level as the stomatal pore. Near the lows their classification according to the systems proposed stomatal pore the outer stomatal ledges (ol) and the inner for recent plants. Two types of classification were established: stomatal ledges (il) are extended (fig. 6). morphological, for the mature forms, and ontogenetic, based The walls of the guard cells beyond the stomatal pore are on the developing phase. In our case, the stomata may be in contact with each other linearly (the stomatal pore reaches classified according to both systems. about one-third of the entire stoma length) and are visible Using the morphological classification, the stomata of Sa- up to the poles. Sometimes the inner walls of guard cells are genopteris may be regarded as the anomocytic type (Wilkin- partly preserved (fig. 5.60). Depending on the degree of pres- son’s classification; Wilkinson 1979). This type of stomata ervation, the guard cells usually form a V-shaped incision at is defined as guard cells surrounded by cells not distinguish- the poles (figs. 4.56, 4.57), or the poles are rounded (figs. able from other epidermal cells. However, the observed se- 4.55, 4.58). In almost all stomata, T-pieces were observed. quence (fig. 7) shows evidence that the mode of stomatal Guard cells are surrounded by unspecialized, irregular epi- development in Sagenopteris is typical of the classic perigen- dermal cells that are sometimes arranged in a similar way to ous type (Pant’s classification; Pant 1965). That is, two guard subsidiary cells in cyclocytic stomata. However, such ar- cells originate from the division of a single maternal cell, BARBACKA & BO´ KA—THE STOMATAL ONTOGENY OF SAGENOPTERIS 155

probably the only pteridosperm that can be fully compared with the early angiosperms described in detail from the Lower Potomac Group by Upchurch (1984a, 1984b), who also discussed their presumed relationships with later angiosperms. Comparing the structure of stomata of early angiosperms with Sagenopteris, the main difference is the variation in arrangement of subsidiary cells. While in Sagen- opteris all stomata are anomocytic, the angiosperms from the Potomac Group show a large variability in stomatal types. It is especially expressed in specimens from zone 1, which display little interspecific diversity and a high morphological variability of the stomata. In this way stomata from the same leaf may be anomocytic, cyclocytic, hemiparacytic, or later- ocytic (Upchurch 1984a). However, the later group (subzone 2-B) displays a rather higher level of interspecific diversity, Fig. 6 Sagenopteris sp., schematic drawing of reconstructed stoma. while the number of stomatal types within one leaf is reduced. gc, guard cell; sc, subsidiary cell; ol, outer ledge of the stoma; il, inner In Upchurch’s opinion, the evolutionary trend has a tendency ledge of the stoma. “towards decreased stomatal variation in early angiosperms” (Upchurch 1984a, p. 547). Consequently, the uniformly par- while any subsidiary cells are formed independently from the acytic stomata of the Magnoliales, which are generally con- neighboring epidermal cells. Fryns-Claessens and Cotthem sidered as primitive among the angiosperms, are regarded in (1973) suggested another classification with a modified, more this case as stemming from the variable forms observed in detailed terminology that combines both morphological and leaves from zone 1 (Upchurch 1984b). In this context the ontogenetic systems. They recognized 26 different ontoge- uniformly anomocytic stomata of Sagenopteris (which are netic types, one of which, aperigenous anomocytic, may be themselves again progressive in comparison to paracytic used to characterize Sagenopteris. This type is characterized ones; Baranova 1972, 1992) may be regarded as progressive as follows, “The guard mother cell divides once to form the in relation to other contemporary groups of plants. two guard cells, the surrounding epidermal cells are neigh- Based on the classification of Fryns-Claessens and Cotthem bouring cells, independently derived from the protoderm. (1973), the type of stomata observed in Sagenopteris is rather The adult stomata are devoid of subsidiary cells and belong common among extant , ferns, gymnosperms, and an- to the anomocytic type” (Fryns-Claessens and Cotthem 1973, giosperms. However, Fryns-Claessens and Cotthem did not p. 80). present any data on the ontogeny of stomata in recent Although these systems of classification are based on ob- gymnosperms. servations of angiospermous stomata, it would seem to be Based on its stomatal structure, Sagenopteris may be re- useful for Sagenopteris as well because its cuticle clearly garded as a highly developed group of pteridos- shows angiospermous characteristics (Thomas 1925; Stewart perms. It is evident that different characteristics of stomata and Rothwell 1993). are variable in different groups of plants, so the reconstruc- In other ferns, stomata are composed of semicircular, tion of the evolution process is seriously impeded. During often sunken guard cells surrounded by a ring of four to the past decades many authors applied cladistic methods for eight subsidiary cells. Another more or less complete ring of tracing the presumed ancestors of angiosperms. Doyle and encircling cells is often found around them. Papillae are quite Donoghue (1986) chose 20 different groups of fossil plants common (Harris 1932). from the to the Cretaceous and examined them in The kidney-shaped guard cells with poles on the same level reference to 62 characteristics. The Caytoniales (with their as the pores and the absence of specialized subsidiary cells 124-step cladogram) were placed among the possible ances- clearly differentiate the Sagenopteris cuticle from that of tors of flowering plants together with some members of the other gymnosperms. The shape of the guard cells, the absence Bennettitales (125 steps), Corystospermales, and Gnetum of subsidiary cells, and the random orientation of the stomata (136 steps). Later, the Caytoniales were also often considered are more angiosperm-like (Thomas and Bancroft 1913; Har- in similar cladistic analyses. The features that were taken into ris 1932). consideration include the morphology of the leaves and the We know nothing about the stomatal ontogeny of other stomatal structure as well as the morphology and anatomy seed ferns. Our knowledge of this process in extinct gym- of the reproductive organs (Doyle and Donoghue 1992; nosperms is very uncertain. Based on data regarding stomatal Nixon et al. 1994; Doyle 1996). The results described in this structure and ontogeny of the extant Gnetum and Welwit- article on the structure and ontogeny of stomata in Sagen- schia, it is presumed also that Bennettitales with a slightly opteris confirm the position of the Caytoniales among the similar stomata have the same syndetocheilic type of stomatal advanced fossil gymnosperms showing characteristics ap- development. In all remaining extant gymnosperms, the sto- proaching those of angiosperms. mata are haploheilic, perigenous monocyclic, or amphicyclic Conclusions (Napp-Zinn 1966). With its perigenous anomocytic stomata, Sagenopteris is Ontogenesis of stomata may be observed in fossil plants, exceptional in the group to which it belongs. Sagenopteris is provided that the examined leaves are young enough and 156 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 7 Sagenopteris sp., particular stages of stomatal development, the schematic drawing well preserved. On the basis of these observations, stomata cestors of angiosperms and some groups of pteridosperms may be classified using the morphological and even onto- might be closely related. genetical systems used for recent angiosperms. Therefore, the stomata of the Sagenopteris may be considered to be of the Acknowledgments perigenous anomocytic type and to be comparable with an- giospermous stomata. This is one more feature that confirms The authors express their thanks to Zlatko Kvacˇek for his the evolutionary high position of the Sagenopteris among the advice on the research and Steven Manchester for his help and fossil gymnosperms and supports the opinion that the an- corrections made in the manuscript.

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