Vegetative morphology
Two stems are up to 120 mm long and measure 12–20 mm in diameter (Figure 1a,b). They decrease in diameter acropetally. The proximal bifurcation of the fronds is sometimes visible at an angle of 60° (Figure 1b, middle frond). Rachises of fronds depart from the stem at 45-60°, are up to 60 mm long, and are separately 5.2-10 mm and 5.0-6.3 mm in diameter before and after proximal bifurcation. One stem has three fronds appearing to be alternately arranged (Figure 1a). In another stem (Figure 1b), the upper frond departs at 50°, the middle frond emerges at 20°, while the basal frond (Figure 1b, arrow) plunges into the rock matrix. In this case, the three fronds on this stem are borne helically, approaching a 1/3 phyllotaxis. The interval between the attachment of two adjacent frond rachises is 20–70 mm. Narrow and longitudinally parallel ridges 120–350 μm in width occur on the surface of stems and frond rachises and alternate with narrow grooves. These ridges correspond to the bands of sclerenchyma cells in the outer cortex (see below).
The part and counterpart of a specimen display an axis with lateral branches bearing planate pinnules (Figure 1c, d, Additional file 1: Figure S1a, b). This axis is about 85 mm long and 4.8-5.2 mm in diameter, and possesses longitudinal ridges (Figure 1d, arrow, e). The diameter and striations suggest that this axis may represent the upper part of a frond rachis after initial bifurcation. In this case, there are two orders of pinnae within the frond. Since plant shows little contrast with the rock matrix, the configuration of the pinnules is very difficult to recognize. However, narrow longitudinal ridges are visible on the rachises of the primary pinnae. The rachises of two primary pinnae are 1.8-2.6 mm in diameter, and attached separately at 70° and 30° to the frond rachis. One primary pinna is only basally preserved, whereas another is 76 mm long and bears four secondary pinnae. The rachises of secondary pinnae, up to 60 mm long and 0.8-1.3 mm in width, are alternately arranged. Except for the basal one, the other three secondary pinnae depart at about 90°. The distance between the attachment of two neighboring secondary pinnae is 16–21 mm. Nonlaminate pinnules are borne at 45-90° and alternately on the secondary pinna rachis, and are planate and highly dissected. A pinna rachis possesses at least seven pinnules. The distance between two adjacent pinnules is 4.6-13 mm. Pinnules are up to 21.7 mm long and about 19.4 mm wide. Each pinnule unequally dichotomizes to produce four or more units. These units, which are up to 11 mm long and about 12 mm wide, arise at 20-90°, and divide unequally twice or thrice to form narrow segments which are 0.5-1.2 mm wide (Figure 1f, Additional file 1: Figure S1).
Anatomy
Stems
Transverse sections of stems show a small three-ribbed protostele (actinostele), broad secondary xylem, narrow cortex and circular-oval leaf traces (Figures 2 and 3, Additional file 2: Figure S2 and Additional file 3: Figure S3). Longitudinal sections of stems demonstrate the secondary xylem and cortex (Figure 4a-e), with the former tissue being also observed with SEM (Figure 4f-k). The stems are 7.2-10.5 mm in diameter and the primary xylem is 1.8-2.0 mm in diameter (Figure 2a, b, Additional file 2: Figure S2a-d and Additional file 3: Figure S3a, b, e-g). The ratio of stelar primary xylem diameter to total stem diameter is around 1/5 (calculated from transverse section illustrated in Additional file 2: Figure S2c). The three ribs of primary xylem, which differ in length (Additional file 3: Figure S3a, arrows 1-3), are 0.5-1.2 mm long and 0.2-0.3 mm wide at their tips. The ribs become narrower toward the stelar center, being no more than 0.1-0.2 mm. The angles between two adjacent ribs of a stele are approximately 90°, 125° and 145°. The mesarch primary xylem only with tracheids (Additional file 3: Figure S3 and Additional file 4: Figure S4) possesses a single protoxylem strand located near the periphery of each rib (Additional file 3: Figures S3c, arrow, d, left arrow, h, i, and S4). The xylem rib is longitudinally continuous (Additional file 2: Figure S2a-d, Additional file 3: Figure S3e-g, Additional file 5: Figure S5a-g and Additional file 6: Figure S6a-g). Protoxylem and metaxylem tracheids are 3.0-10 μm and 13–85 μm in diameter, respectively.
Arising close to the stelar center, the secondary xylem extends outward up to a distance of 2.7 mm (Figure 2a, b, Additional file 2: Figure S2a-d). In transverse section, the secondary xylem tracheids are of various shapes (circular, oval, square, rectangular and irregular) as in the metaxylem tracheids, and are 12–75 μm in diameter and arranged in radial files. Multiseriate pits of circular and oval shape occur on both tangential (Figure 4c, e) and radial (Figure 4d, f-i) walls of secondary xylem tracheids. These pits are bordered (Figure 4j, k) and 3.0-13 μm in diameter. Rays occur between every two to about ten rows of secondary xylem tracheids (Figures 2a, b, 3a, g and 4e). Rays are usually 2 and sometimes up to 6 cells wide (Figure 4e, Additional file 3: Figure S3a, arrow), and more than 120 cells high (Figure 4e, f). Ray parenchyma cells are 65–128 μm in radial and 10–32 μm in tangential dimensions, and 22–48 μm high (Figures 3a and 4d, arrow, e-i).
The cortex sometimes appears to have been compressed to present a wing-like outline (Figure 2b, Additional file 2: Figure S2a, b). It is 0.8-1.1 mm thick (Figure 2b, Additional file 2: Figure S2a-d) and lacks sclerotic nests (Figure 3b, c). The inner cortex consists of circular and oval parenchyma cells which are 25–160 μm in diameter. Longitudinal sections show that these cells are up to 180 μm high (Figure 4a, b). Sparganum-type outer cortex contains many radial bands of sclerenchyma cells with thick walls (Figures 2a, b and 3b, c, g). These bands at the periphery of the cortex are 300–700 μm in radial and 100–520 μm in tangential dimensions, and the circular to square sclerenchyma cells range from 14–68 μm in diameter. In longitudinal sections, the sclerenchyma cells are continuous, up to 1.0 mm high and do not anastomose (Figure 4a, lowermost arrow, b, arrow). Intervening parenchyma cells are tangentially elongate between two adjacent bands with intervals of 130–270 μm.
Individual leaf traces are circular and slightly oval in outline, and their diameter is 0.3-0.4 mm near the tip of the primary xylem rib (Additional file 2: Figure S2i, k and Additional file 5: Figure S5d), but becomes 0.4-0.5 mm in the secondary xylem (Additional file 2: Figure S2c, right arrow, d, lower arrow, h, j and S5a-f), and reaches 0.3-0.7 mm in the inner cortex of the stem (Figures 2a, arrows 1–4, b, arrows 1–3, c-f and 3d-f, g, arrows, h-k, Additional file 2: Figure S2a, arrow, c, left arrow, d, upper arrow, e-g). The tracheids of the leaf traces are up to 56 μm in diameter.
Serial transverse sections of a stem indicate that each rib of the primary xylem successively initiates two leaf traces. The first trace is located at the periphery of the inner cortex (Additional file 2: Figure S2a, arrow, e and Additional file 6: Figure S6h). The tip of a xylem rib obliquely and radially expands to form a protoxylem strand representing the incipience of another leaf trace (Additional file 3: Figure S3a, arrow 3, b, d, right arrow). Then, this trace appears to tangentially diverge from the rib tip (Additional file 2: Figure S2i) and afterwards becomes detached within the secondary xylem (Additional file 2: Figure S2c, right arrow, h and Additional file 6: Figure S6i). More distally, a leaf trace diverges from the tip of another rib with protoxylem strand (Additional file 2: Figure S2k, arrow) and is then surrounded by the secondary xylem (Additional file 2: Figure S2d, lower arrow, j). This trace contains two protoxylem strands (Additional file 2: Figure S2j, arrows, k). Another trace thought to depart from the same rib tip is however invisible. It is suggested that two traces may subsequently diverge from the tip of the third rib, thus indicating a 1/3 phyllotaxy.
Serial transverse sections of another stem clearly show the successive origination of two leaf traces. One trace in the secondary xylem has been tangentially produced from a tip of the primary xylem rib (Additional file 5: Figure S5a and Additional file 6: Figure S6a), then gradually moves toward (Additional file 5: Figure S5b, c and Additional file 6: Figure S6b, c) and reaches the periphery of the inner cortex (Additional file 5: Figure S5d-g and Additional file 6: Figure S6d-g). Here (Additional file 5: Figure S5g, arrow) the trace with two protoxylem strands is tangentially elongate (Additional file 5: Figure S5i, arrows), thus indicating further division. The same rib tip obliquely and radially expands to produce a protoxylem strand representing the incipience of another trace (Additional file 5: Figure S5a-c and Additional file 6: S6a-c), which radially diverges, then passes through the secondary xylem (Additional file 5: Figure S5d-f and Additional file 6: Figure S6d-f) and reaches the inner cortex (Additional file 5: Figure S5g and Additional file 6: S6g). Because of the irregular configuration of ribbed primary xylem, the apparent radial emission of this leaf trace may result from preservation and distortion of the specimen due to compression. This trace in the secondary xylem (Additional file 5: Figure S5f, arrow) displays one protoxylem strand (Additional file 5: Figure S5h, arrow).
In the inner cortex of one stem, two leaf traces derived from a primary xylem rib begin to tangentially divide once (Figure 3g, arrows). The subsequent gradual divisions result in four traces (Figure 3h-k). Four leaf traces from a primary xylem rib occur in the inner cortex of the second stem (Figure 2a, arrows 1–3, c-e), with two traces having just tangentially separated (Figure 2a, arrow 1, c). Four leaf traces from a primary xylem rib are present in the inner cortex of the third stem (Figures 2b, arrows 1–3 and 3d-f), with two traces beginning to separate (Figures 2b, arrow 1 and 3d). Leaf traces in the cortex of these three stems have mesarch primary xylem (two protoxylem strands, see Figures 2f and 3e, k, Additional file 2: Figure S2e).
Frond base with trace
Two successive transverse sections of a stem demonstrate the attachment of a petiole base (Figure 5a-d). This stem has the same structure as the other stems, which includes a three-ribbed primary xylem of mesarch maturation, thick secondary xylem and narrow cortex with sclerenchyma cells (such cells are present only in the first section as shown by Figure 5a, b). The petiole base is ca. 5.6 mm tangentially (Figure 5b). The vascular supply of the petiole consists of four bundles, with two shown in oblique longitudinal section (Figure 5b, arrow, e) and two in oblique transverse section (Figure 5f). The latter two bundles are tangentially oriented, asymmetrical and C- or broadly U-shaped (adaxially concave). They are ca. 2.0 mm tangentially and 0.2-0.4 mm radially, with the concave surface facing the stem center. The inner bundle tends to divide into three portions, with the abaxial surface of two bundles possessing protoxylem strands (Figure 5f, arrows). The two bundles in oblique longitudinal section may present the same shape and structure when they are in transverse view. Therefore, in the upward and outward course through the cortex of the stem, a leaf trace dichotomizes to form four bundles that assume two C-configurations in the petiole base. The tracheids of the vascular bundles are 10–52 μm in diameter and embedded in a ground tissue of parenchyma cells which are 30–110 μm in diameter. Bands of sclerenchyma cells occur in partially preserved sparganum-type outer cortex, and are 450–720 μm and 130–190 μm in radial and tangential dimensions, respectively (Figure 5b). Intervals between adjacent bands are ca. 260 μm.
Systematics
? Class Spermatopsida
Order Incertae sedis
Genus Yiduxylon Wang et Liu gen. nov.
Generic diagnosis
Stems with fronds borne helically in a 1/3 phyllotaxy. Frond rachises bifurcate proximally. Two orders of pinnae with alternately arranged secondary pinna rachises bearing alternate pinnules which are planate and highly dissected. Stems protostelic with small three-ribbed primary xylem, broad secondary xylem, and narrow cortex. Primary xylem mesarch with each rib possessing a single peripheral protoxylem strand. Secondary xylem intermediate between manoxylic and pycnoxylic types. Multiseriate bordered pits on tangential and radial walls of secondary xylem tracheids. Rays usually biseriate and very high. Cortex consisting of an outer sparganum zone and an inner parenchymatous ground tissue. Two leaf traces successively derived tangentially from tip of each primary xylem rib and once divided to produce four traces in stem cortex. Leaf traces possessing mesarch primary xylem. Petiole base containing vascular supply of four bundles in two C-shaped groups (each group with concave surface facing stem center and protoxylem strands on abaxial surface), peripheral and parallel bands of sclerenchyma cells, and ground tissue of parenchyma cells.
Type species Yiduxylon trilobum Wang et Liu sp. nov.
Specific diagnosis
As in generic diagnosis. Stems 7.2-20 mm in diameter and attached by fronds at 45-60°. Frond rachises 5.2-10 mm and 4.8-6.3 mm in diameter before and after proximal bifurcation at about 60°, respectively. Narrow and longitudinally parallel superficial ridges and grooves alternating on stems and rachises of fronds and primary pinnae. Primary pinna rachises 1.8-2.6 mm in diameter. Secondary pinna borne at about 90°, with rachises 0.8-1.3 mm in diameter, and bearing pinnules at 45-90°. Pinnules up to 21.7 mm long and about 19.4 mm wide, with each unequally dividing into four or more units that are anisotomous twice or thrice. Ratio of primary xylem diameter to stem diameter 1/5. Stem primary xylem 1.8-2.0 mm in diameter, with three undivided ribs varying in length and becoming narrower towards stelar center. Secondary xylem up to 5.2 mm thick. Rays 2–6 cells wide and more than 120 cells high. Cortex 0.8-1.1 mm thick and inner cortex lacking sclerotic clusters. Individual leaf traces circular or slightly oval with two protoxylem strands. At petiole base, each C-shaped group of two vascular bundles asymmetrical with inner bundle tending to divide into three portions.
Holotype designated here
Slide HBY-02 (Figure 2a, c-f, Additional file 2: Figure S2b and Additional file 3: Figure S3b).
Paratypes designated here
Specimens PKUB14401 (Figure 1a), PKUB14403 (Figure 1b), PKUB14402a (Figure 1c), PKUB14402b (Figure 1d, e); Slides HBY-04 (Additional file 2: Figure S2c, f, h), HY3-4 (Figures 2b, 3d-f, Additional file 3: Figure S3g), HY9-2 (Figure 4e), 4–6 (Figure 5b, d-f).
Etymology
Generic name from Yidu (where the plant was discovered) and the Greek xylon (xylem). Specific epithet from the Greek treis (tri) and lobos (lobes), meaning three-lobed shape of stem primary vascular system in transverse section.
Locality and horizon
Tizikou, Maohutang village, Wangjiafan Town, Yidu City, Hubei Province, China; Upper Devonian (Famennian) Tizikou Formation.
Repository
All specimens and slides are housed in the Department of Geology, Peking University, Beijing, China.
Comparisons
Although the aneurophyte progymnosperms possess protostele with ribbed primary xylem of mesarch maturation, and secondary xylem with bordered pits on all walls of tracheids [1], they are distinct from Yiduxylon mainly in the geological age, other stelar architectures and vegetative morphology. Aneurophytes existed in the Middle Devonian-Late Devonian (Frasnian) and was characterized by protoxylem strands near the tips and along the midplanes of the primary xylem ribs and in the stelar center, pycnoxylic secondary xylem and radial divergence of branch traces [1,36,37]. Furthermore, except for Triloboxylon ashlandicum and Proteokalon petryi [38,39], the aneurophytes lack planation of the lateral axes (alternate or opposite arrangement) and vegetative ultimate appendages (planate leaves); a decussate pattern occurs in Tetraxylopteris with most orders of branches containing a four-ribbed primary vascular system [36]. Protoxylem strands along the midplanes of the rib of the Aneurophytes and Stenokoleales usually accompany and probably have been derived from a single strand at the stelar center [36,40,41]. Concerning Yiduxylon, the primary xylem is poorly preserved, but many sections indicate the absence of protoxylem strands along stelar ribs and two sections perhaps lack a central protoxylem strand (Additional file 4: Figure S4a, b). The secondary xylem is intermediate between pycnoxylic and manoxylic type (see below). Two leaf traces depart successively from the tip of a stem xylem rib (Additional file 6: Figure S6). One trace diverges and extends up at the boundary between secondary xylem and cortex, and then another trace is initiated. Two leaf traces probably divide tangentially from the rib tip.
Stenokoleales of the Middle Devonian to Early Carboniferous represents a distinct order within the “radiate protoxylem” group comprising plants such as aneurophytes and some early spermatophytes [41]. This order may have a close affinity with the seed plants [42]. Stenokoleales includes Stenokoleos and Crossia known only from anatomy [41,42] and is characterized by a three-ribbed protostele with a single protoxylem strand at the stelar center and numerous protoxylem strands along the midplanes of the primary xylem ribs. Secondary xylem is sometimes present but only in small amounts. In Stenokoleos, successive pairs of traces are produced from the opposite xylem ribs of stem, suggesting that paired fronds are borne alternately [43]. As to Crossia, three stelar ribs of the lower orders of axes divide to form six ribs where branch traces are emitted in pairs [41]. However, Yiduxylon has protoxylem strands restricted near the periphery of three xylem ribs of stem, large amounts of secondary xylem, two leaf traces successively arising from a xylem rib, and helically arranged petioles.
The stem steles of early seed plants (Late Devonian to Carboniferous Buteoxylonales, Calamopityales and Lyginopteridales of seed ferns) may be divided into three types, i.e. ribbed protostele or actinostele, parenchymatized protostele and eustele with pith [37]. Yiduxylon with protostele differs from the spermatophytes with parenchymatized protosteles, e.g., Buteoxylon [44], Galtiera [15], Heterangium [45,46], Rhetinangium [47-49], Schopfiastrum [50], Microspermopteris [51,52], some species of Calamopitys, e.g., C. saturni and C. annularis [53], and most species of Stenomyelon, e.g., S. muratum [11], S. bifasciculare [54], S. tuedianum [55,56]. Yiduxylon also differs from those with eusteles, e.g., Diichnia [11,12,16], Faironia [4], Lyginopitys [57], Lyginopteris [58], Trivena [20], Triichnia [59], and some species of Calamopitys, e.g., C. solmsii [53].
The spermatophytes with ribbed protosteles include Bostonia [60,61], Elkinsia [10], Kerryoxylon [7], Laceya [8,9], Stenomyelon primaevum [55,56], Tetrastichia [7,62,63], Triradioxylon [64], and Tristichia [7,65,66]. However, Tetrastichia and Kerryoxylon differ from Yiduxylon in having four- and six-ribbed primary xylem, respectively. The primary xylem of Tetrastichia is sometimes three- or five-ribbed, and a single protoxylem strand is present near the stelar center, or along the midplane of each primary xylem rib; the phyllotaxy of fronds is opposite decussate, 1/3 and 2/5. Leaf traces of Kerryoxylon are three-ribbed in the stem cortex.
Yiduxylon resembles Bostonia, Elkinsia, Laceya, Stenomyelon primaevum, Triradioxylon and Tristichia in the protosteles with three primary xylem ribs possessing peripheral protoxylem strands. Nevertheless, Yiduxylon is characterized by two leaf traces successively derived in tangential pattern from a single rib of stem primary xylem. Specifically, the primary xylem of Bostonia comprises three semi-discrete portions and a central portion; the protoxylem strands occur also in the stelar center; neither xylem ribs nor peripheral protoxylem strands are longitudinally continuous; the vascular supply of petioles is three-ribbed and derived from a pair of leaf traces [61]. Protoxylem strands of Elkinsia are located also in the stelar center and sometimes along the midplane of xylem ribs; the peripheral protoxylem strand diverges into different numbers and shapes of leaf traces (one papillionoid, one C-shaped, two bilobed, four elliptical ones), although the frond rachis is vascularized by two C-shaped bundles [10]. The leaf trace initiation of Laceya is caused by repeated divisions of primary xylem rib resulting in a tip with 6–8 united lobes; the U-shaped leaf trace remains undivided and its abaxial surface shows 6–8 protoxylem strands [8]; vascular supply at the petiole base is a U-/V-shaped bundle with 8–12 protoxylem strands on the convex abaxial surface [9]. The primary xylem of Stenomyelon primaevum is separated from the secondary xylem by parenchymatous cells; protoxylem strands occur along the midplanes of xylem ribs and are often associated with a lacuna; pits appear only on radial walls of secondary xylem tracheids; there are eight vascular bundles in each petiole base [56]. One or more protoxylem strands are also located in the stelar center of Triradioxylon, and the leaf traces are undivided and the vascular supply in the petiole is T-shaped [64]. Concerning Tristichia, protoxylem strands sometimes occur also in the stelar center and along the xylem ribs, and the leaf traces are tetrarch and papillionoid [66]. Sclerotic nests characteristic of the inner cortex of Elkinsia, Triradioxylon and Tristichia are absent in Yiduxylon.
As in Yiduxylon, the pinnae and pinnules of Late Devonian Kongshania [3] are alternately arranged. In contrast, the pinnules of Kongshania are laminate and wedge-tongue shaped; the poorly preserved frond rachis in description and diagram consists mainly of two bean-shaped vascular bundles surrounded by secondary xylem, which are however difficult to see in the photographs.