Anatomy of the Late Devonian Sphenopsid Rotafolia Songziensis

Anatomy of the Late Devonian Sphenopsid Rotafolia songziensis , with a Discussion of Stelar Architecture of the Sphenophyllales Author(s): De‐Ming Wang, Shou‐Gang Hao, Qi Wang, and Jin‐Zhuang Xue Source: International Journal of Plant Sciences, Vol. 167, No. 2 (March 2006), pp. 373-383 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/499115 . Accessed: 02/04/2015 03:18

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This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 167(2):373–383. 2006. Ó 2006 by The University of Chicago. All rights reserved. 1058-5893/2006/16702-0020$15.00

ANATOMY OF THE LATE DEVONIAN SPHENOPSID ROTAFOLIA SONGZIENSIS, WITH A DISCUSSION OF STELAR ARCHITECTURE OF THE SPHENOPHYLLALES

De-Ming Wang,*,y Shou-Gang Hao,1,* Qi Wang,z and Jin-Zhuang Xue*

*Key Laboratory of Orogenic Belts and Crustal Evolution, Department of Geology, Peking University, Beijing 100871, China; yInstitute for Earth Sciences, University of Graz, A-8010 Graz, Austria; and zKey Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

A previous study of the Late Devonian (Famennian) sphenopsid Rotafolia songziensis Wang, Hao, and Wang provided detailed descriptions of the morphology and a sketchy illustration of a three-ribbed primary xylem. The present anatomical data show that the protostele of this plant also has four-ribbed primary xylem of exarch maturation. Located at the tip of each xylem rib, the tracheids of the protoxylem strand bear helical wall thickenings. Tracheids of metaxylem and secondary xylem possess scalariform pits and/or bordered pits. Ray cells seldom occur in secondary xylem. In contrast to fertile organs demonstrating great diversity in bract shape, structure, and sporangiophore number, the stelar architecture of the Sphenophyllales is consistent in ribbed primary xylem of fundamentally exarch maturation, although secondary xylem indicates moderate structural variations. Stelar architecture of the Sphenophyllales is compared with that of basal euphyllophytes and lycophytes. The position of peripheral protoxylem strands in the Sphenophyllales and Iridopteridales corresponds to the presence of leaves or leaf precursors. The origination of these strands differs from that of radiate protoxylem strands in the Aneurophytales.

Keywords: Rotafolia songziensis, Late Devonian, stelar architecture, sphenopsid, Sphenophyllales.

Introduction referring to advanced trimerophytes, aneurophytalean progymnosperms, and some early seed plants and the latter Phylogenetic analyses (Kenrick and Crane 1997a, 1997b; referring to some primitive ferns (e.g., iridopteridalean clado- Doyle 1998) recognized two major monophyletic lineages xylopsids) and early sphenopsids. within the fossil and living vascular plants (tracheophytes). The sphenopsids (also known as equisetophytes, horsetails, One lineage is the lycophytes (i.e., Lycophytina), and the articulates, or arthrophytes) represent one distinctive clade of other is the euphyllophytes (i.e., Euphyllophytina), which are land vascular plants that are characterized by whorled ar- two land-plant sister groups. The lycophytes contain leaﬂess rangement of fertile units and highly reduced vegetative zosterophylls and derived microphyllous lycopsids (club- leaves. The Sphenopsida comprise two major orders, i.e., the mosses). They are characterized by exarch primary xylem Sphenophyllales and the Equisetales. The extinct Sphenophyl- with multiple peripheral protoxylem strands around the cy- lales appeared as early as the Late Devonian, reached their lindrical protostele. Among them, the Lycopodiaceae and maximum development in the Late Carboniferous, and then the Drepanophycales (prelycopsids) possess distinctive ribbed disappeared by the Early Permian. The only extant element primary xylem. The euphyllophytes include ancestral trimer- of the sphenopsids is the genus Equisetum, which belongs ophytes and descended ferns, sphenopsids, progymnosperms, to the Equisetales. A novel sphenophyllalean plant Rotafolia and seed plants. The stelar architecture of this lineage is dif- songziensis (Wang et al. 2005) came from the Late Devonian ferent from and more diversiﬁed than that of the lycophytes. (Famennian) Xiejingsi Formation, southwestern Hubei Prov- For example, the trimerophytes have protostele with cen- ince, China. Former study concerned detailed morphological trarch primary xylem, primitive ferns (e.g., cladoxylopsids) description of its branches, vegetative leaves, strobili, and possess actinostele or plectostele with mesarch primary xy- a sketchy illustration of a three-ribbed primary xylem. We re- lem, the sphenopsids bear ribbed or highly separated primary cently obtained additional material of this plant from the xylem of exarch or mesarch/endarch development, aneuro- same locality; thus, it is possible to provide more information phytalean progymnosperms contain ribbed primary xylem of of the internal structure in R. songziensis and compare the mesarch maturation, and seed plants are often provided with stelar architecture of the Sphenophyllales with that of the Iri- eustele. According to Beck and Stein (1993), the euphyllo- dopteridales, Aneurophytales, Equisetales, and Lycophytina. phytes could be anatomically divided into ‘‘radiate protoxylem’’ and ‘‘permanent protoxylem’’ groups, with the former Material and Methods

1 Author for correspondence; e-mail [email protected]. The Huangkuang section is situated in Liujiachang town, Manuscript received July 2005; revised manuscript received October 2005. Songzi district, southwestern Hubei. The Devonian strata at

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This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions 374 INTERNATIONAL JOURNAL OF PLANT SCIENCES this section were divided in ascending order into Yuntaiguan ous sporangia; elongate-cuneate bract bearing a distal and (Givetian of the Middle Devonian), Huangjiadeng (Frasnian many lateral elongate segments. Pendulous elongate sporangia of the Late Devonian), and Xiejingsi (Famennian of the Late abaxially attached to base of bract at the same level. Proto- Devonian) formations. Most anatomical materials of Rotafo- stele comprising three- [sometimes four]-ribbed primary xylem lia songziensis were collected from the lower part of the and radial secondary xylem. Primary xylem maturation ex- Xiejingsi Formation, ca. 2 m below the horizon where Sub- arch, with protoxylem strands at tips of xylem ribs. [Ray cells lepidodendron songziense (Wang et al. 2003) was preserved. rare in secondary xylem.] A few specimens were obtained from the same formation, Tizikou section, Maohutang village, Yidu district, south- Species—Rotafolia songziensis (Feng) Wang, western Hubei. A detailed record of the locality of the Hao, and Wang 2005 emend. Huangkuang and Tizikou sections was presented by Feng (1984) and Wang et al. (2003, 2005). Emended specific diagnosis. Same as for generic diagno- At the Huangkuang section, the fusainized compressions sis. Axes up to 20 cm long, with internodes 1.5-(2.2)-4.8 cm are common in a thin bed and are preserved in hard argilla- long, vegetative axes 0.8-(3.0)-8.3 mm in diameter, and ceous sandstones or silty mudstones of slightly pink or black- branching at angles of 45°–85°. Axial spines 1.0-(2.0)-2.8 gray color. At the Tizikou section, the fusainized material mm long and ca. 0.2 mm wide at base. Wedge- or fan-shaped came from soft silty mudstones of black-gray color. Occa- vegetative leaves six per node of axis, 5.0-(14.5)-24.0 mm sionally, the axes were preserved as limonitic permineraliza- long and 2.0-(11.0)-18.0 mm wide as a whole. Each vegeta- tions (fig. 2a). tive leaf equally or unequally dividing at angles of 20°–80°, In order to know the details of xylem strand and tracheids, two to four times. Below first division, leaf bases 2.7-(6.0)- the fusainized axes were removed from the rock matrix and 9.0 mm long and 0.4-(0.8)-1.5 mm wide. Fertile axes below mounted on a stub for examination with a scanning electron strobili anisotomous at 30°–45°, up to 7.8 cm long and 2.7- microscope (SEM; Amary 1910FE) at 5 kV (figs. 4, 5). In (3.8)-6.4 mm in diameter. Strobili 2.9-(4.9)-8.5 cm long and most examples, the extraxylary tissues were not contained in 1.0-(1.6)-2.2 cm wide, with internodes of strobilar axes 0.5- the axes; therefore, only the xylem column was embedded (0.8)-1.6 cm long. Each strobilus bearing up to 16 whorls of in resin, sectioned at less than 1-mm intervals, ground, and fertile units. Fertile units 6.4-(8.8)-11.0 mm long and 2.0–3.2 then polished to a thickness where the sections could be mm wide and inserted at ca. 60° or 90° to strobilar axis. observed directly in transmitted light. Six and 11 xylem Bract 5.0–6.7 mm long and ca. 2.0 mm wide, with distal and columns were cut into 32 transverse (A01–09,B01–08,C01–03, lateral segments 1.5–8.0 mm long and ca. 0.2 mm wide and D01–03,E01–04,H01–05) and 15 longitudinal (I01–03,J01–02,K 2.0-(3.1)-3.8 mm long and 0.2–0.3 mm wide, respectively. 01–02, L, M, N, O, P, Q, R, S) thin sections, respectively, for Ten to 18 lateral segments attached to bract at 65°–85°. Spo- observation with incident (fig. 1; fig. 2c–2k; fig. 3) or re- rangia 1.4-(2.5)-3.8 mm long and 0.2–0.4 mm wide and six flected (fig. 2a,2b) light. All photographs of the sections to 10 per bract. [Primary xylem ribs varying in radial dimen- were taken with a digital camera, and the figures were ar- sion from 0.6 to 1.2 mm and average 0.5 mm in tangential ranged using Adobe Photoshop 7.0 software. The specimens dimension. Protoxylem tracheids 12-(20)-30 mm in diameter. and slides figured here are housed at the Department of Geol- Metaxylem tracheids 25-(65)-95 mm in size, significantly ogy, Peking University, China. larger than those of protoxylem and secondary xylem. Sec- ondary xylem homogeneous, with radial files of tracheids Systematic Description measuring 17-(38)-65 mm in size. Protoxylem tracheid bearing helical wall thickenings ca. 1.6 mm thick, with intervals In light of new observations on the anatomy presented between two adjacent thickenings ca. 3.5 mm. Tracheids of here, the original generic and specific diagnoses of Rotafolia metaxylem and secondary xylem having scalariform and/or (Wang et al. 2005) are expanded as follows. Additional char- bordered pits. Number of scalariform thickenings per milli- acters are indicated in brackets. meter is 110-(135)-150. Scalariform pits 5.5–45 mm wide and 2.6–7.8 mm high. Circular bordered pit ca. 2.7–12.0 mm Class—Sphenopsida Scott 1909 in diameter and elliptical bordered pit 4.0–16.5 mm wide and 2.3–7.2 mm high. Pit apertures and borders 1.0–2.5 and 1.2– Order—Sphenophyllales 4.0 mm high, respectively.] Stewart and Rothwell 1993 Family—incertae sedis Results Genus—Rotafolia Wang, Hao, and Wang 2005 ememd. Transverse View of Xylem Emended generic diagnosis. Plant with anisotomous axes The protostele of this plant comprises a central primary xy- characterized by slightly expanded nodes and ribbed inter- lem column and a surrounding zone of secondary xylem (fig. nodes. Lateral axes attached at nodes of main axes. Whorls 1a; fig. 4a,4c–4e). In a thin and thick axis, the primary xylem of much divided vegetative leaves inserted at nearly right an- is, respectively, three ribbed (fig. 4a; SEM observation) and gles to nodes of basal axes, at acute angles to nodes of termi- four ribbed (fig. 1a; fig. 4d,4e). The three-ribbed primary xy- nal axes. Terminal strobilus possessing a central axis and lem is somewhat triangular in outline, while the four-ribbed whorls of fertile units; each consisting of a bract and numer- one was possibly compressed during preservation to present

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Fig. 1 Anatomy of Rotafolia songziensis seen through light microscope. a, Transverse section and reverse side of a protostele in fig. 4d to show four-ribbed primary xylem and surrounding secondary xylem with tracheids aligned in radial files. Arrowhead indicates the enlarged part in b. Slide D-02. Scale bar ¼ 500 mm. b, Tip of one primary xylem rib in a to show position of protoxylem tracheids (arrowheads). Scale bar ¼ 200 mm. c, d, Transverse sections of a bifurcate axis obtained from parts below and above dividing point. Main axis on the left has a slightly three-ribbed primary xylem, while the lateral axis on the right possesses inner cortex in oblique transverse view. Arrow in d indicates part enlarged in e. Slides B-02 and B-05. Scale bars ¼ 500 mm. e, Triangular-shaped primary xylem in transverse view. Scale bar ¼ 100 mm. the cruciform configuration. The primary xylem ribs vary in metaxylem or secondary xylem (fig. 1a,1b; fig. 4a,4b). The radial dimension from 0.6 to 1.2 mm and average 0.5 mm in tracheids of the metaxylem are 25-(65)-95 mm and generally tangential dimension. Between two ribs are concave embayments. increase in size centripetally. They are larger than tracheids of As to the four-ribbed primary xylem measuring 3.4 mm long the protoxylem and secondary xylem. Some tracheids may be and 2.4 mm wide (fig. 1a), two opposite ribs are longer than grouped in the metaxylem, with a larger tracheid enclosed by the other two opposite ones in radial extent, and the tips of several smaller concentric ones (fig. 4c, arrowhead; fig. 4e,ar- the four ribs are widely spaced. The primary xylem is entirely rowhead c; fig. 4h). composed of polygonal tracheids. The protoxylem tracheids In transverse section, the compact secondary xylem does are 12-(20)-30 mm in diameter and are located at the tip of not differentiate into fascicular (opposite the primary xylem each primary xylem rib (figs. 1b,4b, arrowheads). In the area ribs) and interfascicular (between the ribs) areas. It means where the protoxylem strand occurs, neither lacunae nor paren- that the tracheids between the above two areas are generally chymatous cells were discovered, although there are cavities of the same size, and no multiseriate vascular rays occur in that resulted from the breakdown of bordering tracheids of the fascicular area. Secondary xylem tracheids are distributed

This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions Fig. 2 Anatomy of Rotafolia songziensis seen through light microscope. Longitudinal sections of xylem. a, Oblique longitudinal view of stele through reflected light showing the boundary between primary and secondary xylem. Slide K-01. Scale bar ¼ 1 mm. b, Higher magnification of a portion in a. Arrowheads indicate small tracheids of inner part of secondary xylem located near large tracheids of metaxylem. Scale bar ¼500 mm. c, Tangential section of secondary xylem to show ray cells that are four cells high. Slide M. Scale bar ¼ 100 mm. d, h, k, Tracheids with wall thickenings and scalariform pits. Slides I-01, I-01, and N. Scale bars ¼ 20, 40, and 20 mm. e, Vascular strand separated from the secondary xylem possibly indicating a lateral axis or leaf. Slide J-01. Scale bar ¼ 200 mm. f, Higher magnification of the vascular strand in e showing tracheids with likely scalariform thickenings. Scale bar ¼ 100 mm. g, Tracheid scalariform wall thickenings that occasionally bifurcate. Slide K-02. Scale bar ¼ 10 mm. i, j, Tracheids with tapering end wall. Slides I-01 and I-02. Scale bars ¼ 50 mm.

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Fig. 3 Anatomy of Rotafolia songziensis seen through light microscope. a, Transverse view of metaxylem tracheids with secondary wall thickenings and gaps at corners. Slide A-08. Scale bar ¼ 10 mm. b, Transverse section of a metaxylem tracheid with thick secondary wall. Slide A-01. Scale bar ¼ 10 mm. c, Longitudinal section of neighboring tracheids to show scalariform pit pairs. Secondary wall thickenings (arrowhead t), pit chambers (arrowhead c), inner (arrowhead i) and outer (arrowhead o) apertures, and pit canals (arrowhead n) are visible in lateral view. Slide P. Scale bar ¼ 10 mm. d, Longitudinal section of a tracheid to show pit membranes (arrowheads). Slide N. Scale bar ¼ 10 mm. e, Face view of circular bordered pits on cell wall of tracheid. Slide J-02. Scale bar ¼ 10 mm. f, Face view of rows of circular and elliptical bordered pits on one facet of cell wall. Slide J-02. Scale bar ¼ 5 mm.

in radial files (fig. 1a,1b; fig. 4a,4c–e,4g; fig. 5a). The files ings (fig. 5b). Rays of the secondary xylem have not yet been vary in tangential dimension and measure 280–650 mm in ra- discovered in transverse sections. dial direction. These tetragonal tracheids of the secondary An axis branching at 35° was cut from the parts below xylem are 17-(38)-65 mm in size, usually with the smaller (fig. 1c) to above (fig. 1d) the dividing point. The main axis ones situated near the periphery of the primary xylem (fig. is on the left, while the lateral axis is on the right (fig. 1d). 4a,4c,4f,4g). From the inner to the outer regions of the sec- These two axes were originally connected at the dividing ondary xylem, the tracheids usually appear relatively con- point but unfortunately were separated during the embedding stant or gradually increase in size (fig. 1b; fig. 4c,4g). With process. The primary xylem of the main axis is in transverse regard to a portion of secondary xylem (fig. 5a), in higher view (fig. 1c,1d), while that of the lateral axis is in oblique magnification, the tracheids are seen to possess wall thicken- transverse view (fig. 1d, arrow; fig. 1e). The primary xylem

This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions Fig. 4 Anatomy of Rotafolia songziensis examined with scanning electron microscope. Transverse view of steles. a, Protostele consisting of three-ribbed primary xylem and surrounding secondary xylem tracheids in radial ﬁles. Scale bar ¼ 200 mm. b, Enlargement of upper left part in a. Tip of a primary xylem rib showing position of protoxylem tracheids (arrowheads). Scale bar ¼ 100 mm. c, Incomplete stele showing boundary between primary and secondary xylem. Arrowhead indicates a large metaxylem tracheid enclosed by several small tracheids. Scale bar ¼ 100 mm. d, e, Part and counterpart of a stele with four-ribbed primary xylem. Arrowheads a–c in e indicate portions enlarged in f–h, respectively. Scale bars ¼ 500 mm. f, g, Boundary between primary and secondary xylem. Scale bars ¼ 100 mm. h, Metaxylem tracheids, with a large one enclosed by several small ones. Scale bar ¼ 50 mm.

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This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions Fig. 5 Anatomy of Rotafolia songziensis examined with scanning electron microscope. c-j, Tracheids in longitudinal view. a, Transverse view of secondary xylem tracheids in radial ﬁles. Arrowhead indicates an area enlarged in b. Scale bar ¼ 500 mm. b, Tracheids bearing secondary wall thickenings. Scale bar ¼ 50 mm. c, Boundary between secondary xylem (left) and metaxylem (right). Small tracheids of secondary xylem bear scalariform pits, while large tracheids of metaxylem bear both scalariform and bordered pits. Scale bar ¼ 50 mm. d, e, Tracheids with tapering end wall. Scale bars ¼ 100 and 50 mm. f, Protoxylem tracheid with distinct helical thickenings (arrowhead). Scale bar ¼ 10 mm. g, Inside view of tracheids with scalariform and bordered pits. Scale bar ¼ 10 mm. h, Enlargement of g showing tracheids with circular and elliptical bordered pits. Scale bar ¼ 5 mm. i, Outside view of a tracheid with distinct pit borders. Scale bar ¼ 10 mm. j, Tracheids with scalariform pits. Scale bar ¼ 10 mm.

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This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions 380 INTERNATIONAL JOURNAL OF PLANT SCIENCES column of both main and lateral axes is slightly three ribbed Discussion in outline, with the former xylem column being larger than the latter. In these two steles, the protoxylem strands (fig. 1c– Sphenophyllales and Their Stelar Architecture 1e, arrowheads) are located at the rib tip. The main axis has Sphenophyllales generally comprise two vegetative organ less inner cortex remaining than the lateral one. No tissues genera (Sphenophyllum Brongniart 1828 and Xihuphyllum were closely preserved around the primary xylem of the lat- Chen 1988), several fertile organ genera (Bowmanites Binney eral axis, and the cortex is elongate in radial direction (fig. 1871, Cheirostrobus Scott 1897, Sphenostrobus Levittan and 1d). The main axis possesses little secondary xylem, thus in- Barghoorn 1948, Peltastrobus Baxter 1950), two relatively dicating a possible terminal shoot. completely known genera Hamatophyton (Gu and Zhi 1974) and Rotafolia (Wang et al. 2005; this article). Other possible Longitudinal View of Xylem members are Eviostachya (Leclercq 1957) and Lilpopia (Kerp The primary xylem and secondary xylem are recognized in 1984). Sphenophyllum usually applies to wedge-shaped leaves oblique longitudinal section (fig. 2a). Under higher magnifi- at axis nodes (e.g., Sphenophyllum emarginatum Batenburg cation, smaller tracheids, possibly belonging to secondary xy- 1977) or permineralized axes (e.g., Sphenophyllum plurifolia- lem (fig. 2b, arrowheads), are located near the periphery of tum Baxter 1948; Eggert and Gaunt 1973) or roots (Scott the metaxylem. It could not be decided whether this section 1920). Xihuphyllum megalofolium and Xihuphyllum elonga- has passed the protoxylem strand. However, a protoxylem tum are characterized by wider axes bearing whorls of large tracheid was discovered in a SEM sample (fig. 5f, arrowhead) leaves (up to 11 cm long) that are of flabellate-cuneate shape and measures ca. 18 mm in diameter and bears distinct helical and contain dense flabellate veins (Chen 1988). Fertile organ wall thickenings that are ca. 1.6 mm thick; the intervals be- genera of the Sphenophyllales, e.g., Bowmanites bifurcatus tween two adjacent thickenings are ca. 3.5 mm. In another (Andrews and Mamay 1951), Peltastrobus reedae (Baxter SEM examination (fig. 5c), small secondary xylem tracheids 1950), Cheirostrobus pettycurensis (Scott 1897), and Sphe- on the left possess scalariform pits, while the large metaxy- nostrobus thompsonii (Levittan and Barghoorn 1948), were lem tracheids on the right bear both scalariform and bor- identified by strobili with whorled bracts and spores in situ. dered pits. In a tangential section (fig. 2c), the ray is four The strobilar axes of some genera (e.g., S. thompsonii Levittan cells high and ca. 10 cells wide, and ray cells are 23–46 mm and Barghoorn 1948, Bowmanites moorei Mamay 1959) high and 23–70 mm wide. A single vascular strand of leaf or show three- and sometimes four-ribbed primary xylem in lateral axis measuring ca. 230 mm in diameter is seen to the protostele. Good (1978) gave us a summary of the mor- emerge from the secondary xylem (fig. 2e,2f). The tracheids phological and anatomical characters of the sphenophylla- in the strand seem to bear scalariform wall thickenings. lean strobili. Although Eviostachya (Leclercq 1957) possesses three-ribbed primary xylem in the protostele, it lacks the bract Tracheids being associated with the sporangiophores, which typifies the In transverse view, polygonal metaxylem tracheids show Sphenophyllales. Lilpopia (Kerp 1984) bears unusual clusters secondary wall thickenings, and neighboring tracheids some- of globose sporangia immediately below each bifurcate bract; times create gaps at corners (fig. 3a). In one instance, the however, nothing is known about its stelar structure. thick secondary wall is visible (fig. 3b). In longitudinal view, The sphenophyllaleans demonstrate greater reproductive the tracheids taper distally (fig. 2h–k; fig. 5d,5e), but their diversity in bract shape, structure, and sporangiophore num- exact length could not be determined. Many tracheids have ber. For example, Bowmanites has variously constructed scalariform thickenings and pits (fig. 2d,2h–k; fig. 5c–e,5j). bracts adaxially attached by a variable number of sporangio- The number of these thickenings per millimeter is 110-(135)- phores with anatropous or orthotropous terminal sporangia 150. The thickenings are ca. 5.0 mm thick and occasionally (Good 1978). Each bract of the Sphenostrobus strobilus has are bifurcate (fig. 2g). Measuring 5.5–45 mm wide and 2.6– a single axillary sporangiophore ending in one sporangium 7.8 mm high, the scalariform pits are horizontally elongate (Levittan and Barghoorn 1948). In Peltastrobus (Leisman (fig. 2d,2h,2i; fig. 5d) or elliptical in outline (figs. 2k,5j). In and Graves 1964), the more complex strobilus consists of the longitudinal section of adjacent tracheids (fig. 3c), scalari- a whorl of three sterile and three fertile units at each node. form pit pairs were revealed; secondary wall thickenings (t), Each fertile unit comprises a bract and a cluster of five axil- pit chambers (c), inner (i) and outer (o) apertures, and pit ca- lary peltate sporangiophores bearing several concentric cycles nals (n) are visible in lateral view. Pit membranes were occa- of sporangia; two sporangiophores are distally directed, two sionally preserved (fig. 3d, arrowheads). From the face view are proximally directed, and one is at 90° to the strobilar of the tracheidal lumen (fig. 3e,3f; fig. 5g,5h) and middle la- axis. The bracts of Rotafolia (Wang et al. 2005) are indepen- mella (fig. 5i), circular and elliptical bordered pits are ar- dent and bear distal and lateral elongate segments; at the ranged in rows on the secondary cell wall. These two-shaped same level, clusters of elongate sporangia abaxially occur to bordered pits sometimes appear on a facet of the same tra- the base of the bracts. In contrast to other members of the cheid (figs. 3f,5h). A circular bordered pit is 2.7–12.0 mmin sphenophyllaleans, the stalks of Hamatophyton are devoid of diameter. An elliptical bordered pit measures 4.0–16.5 mm leafy appendages (this article). wide and 2.3–7.2 mm high, with its long axis perpendicular However, this group of vascular plants is well defined by to that of the tracheid. Pit apertures (a) and borders (b) are whorled lateral appendages and protostele with three- (some- distinct (e.g., fig. 3f), 1.0–2.5 and 1.2–4.0 mm high, respec- times four)-ribbed primary xylem. With protoxylem strand tively. located at the rib tip, the primary xylem is of exarch

This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions WANG ET AL.—ANATOMY OF ROTAFOLIA SONGZIENSIS 381 maturation in most sphenophyllaleans, e.g., S. plurifoliatum axes bear whorled vegetative/fertile lateral branches as exem- (Reed 1949; Cichan 1985), Sphenophyllum multirame (Dar- plified by Compsocradus and Ibyka (Berry and Stein 2000). rah 1968), Sphenophyllum gilkineti (Schabilion and Baxter The peripheral protoxylem strands of Iridopteris eriensis give 1971), S. thompsonii (Good 1978), and Rotafolia (Wang rise to traces for whorled lateral appendages (Stein 1982). As et al. 2005; this article). However, it is infrequently of mes- explained by Stein (1993), the occurrence of each primary arch maturation, and the protoxylem strand occasionally col- xylem rib requires multiple lateral branch and/or leaf primor- lapses to produce a lacuna (Meyen 1987, p. 87; Stewart and dia serving as hormone sources; these are termed ‘‘organizing Rothwell 1993, p. 191; Taylor and Taylor 1993, p. 309), centers’’ and correspond to protoxylem strands. Therefore, which is present in the stele of some species of Sphenophyl- the primary xylem ribs of the Iridopteridales fit well with the lum, e.g., S. plurifoliatum (Baxter 1948; Eggert and Gaunt whorled and orthostichous lateral organs. In contrast, how- 1973), and Sphenophyllum sp. (Boureau 1964, p. 96). The ever, it is very difficult to interpret the presence of peripheral protoxylem strands at the nodes of the axis provide traces protoxylem strands instead of radiate protoxylem ones in the for lateral appendages as in S. multirame (Good 1973) and Iridopteridales (Stein 1993). S. plurifoliatum (Eggert and Gaunt 1973). In transverse view, Complementary to Wight and Stein’s hypothesis of the the area of the primary xylem in Sphenophyllum is much stelar ontogeny being biased toward the Euphyllophytina, smaller than that in Rotafolia. The secondary xylem of Sphe- Kenrick and Crane (1997a, pp. 279–280) explained the pri- nophyllum often shows distinct fascicular and interfascicular mary xylem structure of the Lycophytina. They suggested regions (Baxter 1948; Reed 1949; Boureau 1964, p. 96; that the numerous peripheral protoxylem strands around the Darrah 1968; Cichan and Taylor 1982; Cichan 1985). It also cylindrical stele of the zosterophylls-lycopsids lineage were exhibits unique vertical strands of parenchymatous cells at affected by the spirally and closely spaced lateral sporangia the corners of four neighboring tracheids, which are con- and especially microphylls. The protostele of some lycopsids, nected with short horizontal (radial) ray of parenchymatous e.g., Leclercqia (Bonamo and Grierson 1981), bears multiple cells (Baxter 1948; Eggert and Gaunt 1973; Cichan 1985; protoxylem ridges where leaf traces depart. In other lycopsids, Stewart and Rothwell 1993, pp. 192–193). In contrast, the e.g., Oxroadia, Paurodendron,andLepidophloios, these ridges secondary xylem of Rotafolia lacks the differentiation of are longitudinally continuous (Bateman et al. 1992). fascicular/interfascicular regions, and ray cells are seldom re- Like the Iridopteridales, the Sphenophyllales have lateral corded. These differences in primary and chiefly in secondary appendages arranged in whorls. The lateral fertile units (e.g., xylem between Sphenophyllum and Rotafolia illustrate the Rotafolia Wang et al. 2005, their figs. 24, 27, arrows) and moderate structural variations in the anatomy of the Sphe- vegetative leaves (e.g., Hamatophyton; this article) are also nophyllales. in longitudinal orthostichies, thus explaining the occurrence of primary xylem ribs in the protostele. As mentioned by Beck and Stein (1993), the Iridopteridales and Sphenophyl- Stelar Architecture Comparison among Sphenophyllaleans, lales share peripheral protoxylem strands. These strands are Anuerophytaleans, Iridopteridaleans, and Lycophytes longitudinally continuous in serial stelar transverse sections Wight (1987) and Stein (1993) discussed the stelar archi- of I. eriensis (Stein 1982) and in those of Rotafolia, which tecture of some primitive members of the Euphyllophytina were represented by one specimen (Wang et al. 2005, their (sensu Kenrick and Crane 1997a, 1997b) and concluded that fig. 43). Central protoxylem strand is absent in the stele of the shape of primary xylem is influenced by the position and the Sphenophyllales and the Iridopteridales (Beck and Stein number of lateral appendages. They considered that the pro- 1993). Therefore, the peripheral protoxylem strands of these tostele with ribbed primary xylem of the aneurophytalean two groups may not be derived from the central strand, dif- progymnosperms (e.g., Triloboxylon and Tetraxylopteris) re- fering from the origination of the radiate protoxylem strands sulted from the cylindrical stele of the trimerophytes (e.g., of the Aneurophytales. Only the central protoxylem strand Psilophyton) and the xylem ribs were related to lateral of the Aneurophytales is entirely longitudinally continuous, branches closely arranged in three/four longitudinal ortho- and the primary xylem maturation is thus basically centrarch stichies or helix. In transverse view, multiple protoxylem (Wight 1987). In contrast, as mentioned above, mesarch pri- strands occur along the midplane of the primary xylem rib to mary xylem typifies the Iridopteridales and was also docu- form the radiate protoxylem stelar type (sensu Beck and Stein mented in the Sphenophyllales. The fundamentally exarch 1993). According to Wight (1987), the radiate protoxylem stele of the Sphenophyllales may evolve from the mesarch strands of the Aneurophytales were derived from a central stele of some primitive ferns by loss of the outer metaxylem and longitudinally continuous protoxylem strand in the stele; (Doyle 1998, p. 573). Within this evolutionary scenario, in serial transverse sections, these strands were displaced cen- some lateral vegetative branches of the Iridopteridales (e.g., trifugally to provide vascular supply for the laterals, and thus Ibyka Skog and Banks 1973, Compsocradus Berry and Stein they are not longitudinally continuous in either number or 2000) might act as leaflike branches or leaf precursor, with position. especially basal ones attached in whorls and differing in na- Iridopteridales, a group of primitive ferns, are character- ture from the lateral axial branches of the Aneurophytales. In ized by actinostele of the permanent protoxylem type (sensu the Sphenophyllales, planate leaves and/or much divided Beck and Stein 1993). A single and distinct mesarch protoxy- branchlike leaves are common in many plants, e.g., Spheno- lem strand is situated near the tip of each primary xylem rib phyllum (Batenburg 1977), Hamatophyton (Li et al. 1995), and usually is marked by a lacuna to form a peripheral loop and Rotafolia (Wang et al. 2005). These morphological (sensu Stein 1993). Concerning their morphology, the main and anatomical similarities or relationships support the

This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:18:06 AM All use subject to JSTOR Terms and Conditions 382 INTERNATIONAL JOURNAL OF PLANT SCIENCES hypothesis by some investigators (Skog and Banks 1973; branches that alternate at the node of the axis. One of the Stein et al. 1984; Berry and Stein 2000) that the Iridopteri- hypotheses about origin of the sphenopsids (Stein et al. 1984, dales are the best candidate for the ancestors of the Sphenop- their fig. 10d) inferred that the equisetalean stele possibly sida. However, it deserves to be noted that these two groups evolved from the sphenophyllalean protostele, accompanied of plants show some differences in the fertile characters. As by dissection and then loss of (central) metaxylem and final presently known, three taxa of the Iridopteridales have been location of peripheral protoxylem strands with lacunae. How- morphologically described as possessing sporangia terminating ever, it is unclear whether abundant primary xylem ribs ever fertile lateral branches, i.e., Ibyka (Skog and Banks 1973), occurred in this transitional stage from the sphenophyllalean Anapaulia moodyi (Berry and Edwards 1996), and Compsoc- to equisetalean stele, which may relate to leaves/branches ar- radus (Berry and Stein 2000). In contrast, the Sphenophyl- ranged in orthostichies. This uncertainty is due to either the lales are characterized by fertile units usually consisting of lack of intermediate representatives if the above hypothesis bract and adaxial sporangia. Therefore, further studies are by Stein et al. were correct or the large central pith in the needed to explore the origin of the sphenopsids (especially equisetalean stele ‘‘destroying’’ the primary vasculature. the sphenophyllaleans). Exarch and mesarch protoxylem Pith with large amounts of parenchymatous cells in the strands that closely relate to the occurrence of leaves were stele of the Equisetales is another significant difference from also reported in the protostele with ribbed primary xylem of the Sphenophyllales. As suggested by Stein (1993), medulla- Stenomyelon (Meyer-Berthaud and Stein 1995), a kind of tion in the Euphyllophytina (e.g., pteridosperms) depends on pteridosperm. In these basal groups of the euphyllophytes the number of lateral organs of hormone sources and the size (iridopteridaleans, sphenophyllaleans, and pteridosperms), of shoot apical dome. A greater number of laterals favors the therefore, the position of peripheral protoxylem strands cor- occurrence of larger pith. Numerous protoxylem strands corresponds to leaves or leaf precursors. responding to the traces of the leaves and branches at the Besides leaves, the Sphenophyllales are also characterized nodes thus may vindicate the presence of pith in the by lateral organs of fertile units. The relationship between Equisetales, with parenchymatous cells in a larger apical these laterals and the fundamentally exarch maturation of dome receiving inadequate auxin concentration from primor- xylem reminds us of the Lycophytina but perhaps does not dia of lateral appendages (hypoinduction; sensu Stein 1993). necessarily mean that they are close in affinity. Cladistic anal- The pith meristem of Calamites and Equisetum could be ysis supposed that the sphenopsids may not form a monophy- traced to a point immediately beneath the apical cell (Golub letic lineage and that the sphenophyllaleans are possibly and Wetmore 1948) where instead the procambium of Sphe- related to the lycophytes (Tomescu and Rothwell 2001). On nophyllum occurs (Good and Taylor 1972). the basis of exarch primary xylem and evolution of lateral Lacking fascicular and interfascicular regions, as in some organs, Stewart and Rothwell (1993, p. 196) proposed a members of the Sphenophyllales, the secondary xylem of the probable relationship of the Sphenophyllales with the Proto- Equisetales, e.g., Arthropitys (Eggert 1962), is separated into lepidodendrales. However, it was suggested that many simi- many radial portions. Another distinctive character of the larities between the sphenophyllaleans and other sphenopsids Equisetales is the cortex with vallecular canals, which differs make this affinity unlikely (Kenrick and Crane 1997a,p.242). from the homogeneous cortex of the Sphenophyllales. Be- cause of the limited evidence available, the reason for cortical disparity in the sphenopsids is still unclear at present. Stelar Architecture of Sphenophyllaleans and Equisetaleans Acknowledgments Sphenophyllales and Equisetales are two major orders of the Sphenopsida, but they present apparently different stelar This article concerns D.-M. Wang’s postdoctoral research architecture. The unique equisetalean stele is usually identi- at the University of Graz, Austria. We thank Professor fied by discrete mesarch or endarch primary xylem bearing Werner E. Piller (University of Graz, Austria) for his kind multiple peripheral protoxylem strands marked by distinct help. This work was supported by the National Natural carinal canals. The number of protoxylem strands could be Science Foundation of China (grants 40232019 and more than 30 in the Equisetales (e.g., Arthropitys Eggert 40302001), the Foundation for the Author of National Ex- 1962), whereas it could be merely three to four in the Sphe- cellent Doctoral Dissertation of PR China (grant 200429), nophyllales (Stein et al. 1984). As to Calamites (Meyen and a scholarship within the Technology Scholarship Pro- 1987, p. 90) and Equisetum (Bierhorst 1959), multiple proto- gramme for China and Mongolia, financed by the Austrian xylem strands in the stele correspond to numerous leaves and Council for Research and Technology Development.

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