Paratingia wuhaia J. Wang et al., 2021

Wang, Jun, Hilton, Jason, Pfefferkorn, Hermann W., Wang, Shijun, Zhang, Yi, Bek, Jiri, Pšenička, Josef, Seyfullah, Leyla J. & Dilcher, David, 2021, Ancient noeggerathialean reveals the seed plant sister group diversified alongside the primary seed plant radiation, Proceedings of the National Academy of Sciences 118 (11), pp. 1-7 : 2-4

Species— Paratingia wuhaia J. Wang et al. sp. nov.

Etymology—The specific epithet refers to Wuhai city to which the Wuda Coalfield belongs.

Species diagnosis—Monopodial stem with once-pinnate compound leaves and pseudostrobili forming a crown. Stem eustele with pith; cauline primary xylem strand adaxially curved; secondary xylem pycnoxylic; leaf traces tangentially elongated. Rachis of leaf and pseudostrobilus with a reversed Ω- shaped vascular bundle with protoxylem at lateral margin. Pinnules with radiate venation, arranged in four rows, with two rows of large, lanceolate pinnules on lower surface, two rows of small, oblong pinnules on upper surface of the axis. Pseudostrobilus heterosporous; sporophylls whorled, proximally diskshaped or dissected into segments, distally upturned and dissected. Sporangia attached adaxially and proximally to sporophyll in single ring. Megasporangia in vertical row bearing single functional megaspore. Microspores of the Calamospora type.

Holotype— PB22126 ( Fig. 1 A and SI Appendix, Fig. S2 )

Paratypes— PB22127-22138 (SI Appendix, Figs S3‒S 14) .

Type locality— Wuda Coalfield, Wuhai , Inner Mongolia, China.

Horizon—Uppermost part, Taiyuan Formation.

Stratigraphic age—298.34 ± 0.09 Ma, Asselian, Cisuralian, Permian.

Repository—All specimens are deposited at Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences.

Remarks—Following Wang et al. ( 9), we consider the noeggerathialean fertile shoot to be a pseudostrobilus as despite its radial exterior appearance, it is distinctly bilateral in organization and represents a complex, three-dimensional sporophyll. We use quotation marks to denote that what would traditionally be interpreted as sporophylls on the pseudostrobilus axis represent pinnule homologs and are not in fact sporophylls in the traditional sense. Detailed descriptions, measurement, and further illustrations are provided in the supporting information.

Description. The holotype is 160 cm long and 60 cm wide ( Fig. 1 A and SI Appendix, Fig. S2 ) and comprises a stem with apical crown of helically attached megaphyllous leaves and pseudostrobili. The crown has three parts: a 13-cm-long basal region bearing leaves, a middle 23-cm-long fertile zone, and apically a 6-cm-long region bearing more leaves. Below the crown, the stem is naked, extending for> 32 cm, tapers little, and is ∼ 5 cm wide with a smooth exterior, lacking evidence of abscission structures. More than 60 once-pinnate, megaphyllous leaves are attached to the stem above and below the fertile zone, with typical leaf rachises being 10.4 mm wide and <50 cm long. Most pinnules are not fully discernible and are either matted together, obscured by other parts of the plant overlying them, or remain embedded within the rock. A paratype ( Fig. 1 B and SI Appendix, Fig. S12) demonstrates clearly lanceolate, large pinnules on the lower surface of the leaf, and oval, small pinnules on the upper surface, both with radiate venation.

Anatomically, the stem has an eustele with a large pith ( Fig. 1 C and SI Appendix, Fig. S15); cauline primary xylem strands are adaxially curved ( Fig. 1 F and SI Appendix, Fig. S16 A–C). Secondary xylem is pycnoxylic with uniseriate rays, which are mostly short/low and vary remarkably in size from one to seven cells high ( Fig. 1 H and SI Appendix, Fig. S17 C and D). Secondary tracheid walls have scalariform thickenings ( Fig. 1 G and SI Appendix, Fig. S17 A and B), and the cortex has collenchyma in its outer part. Leaf traces are tangentially elongated.

Approximately 8 to 10 pseudostrobili are attached to the circumference of the fertile zone and about 20 more longitudinally attached along the stem ( Fig. 1 A and SI Appendix, Fig. S2 ); we estimate an entire fertile zone would comprise 160 to 200 pseudostrobili. Pseudostrobili are elongated with parallel sides and bluntly rounded apices, and are attached more or less at right angles to the stem with one-third to one-quarter of their width without a stalk. They are 50 to 65 mm long and 13 mm wide ( Fig. 1 A and SI Appendix, Figs. S3–S 8).

Both the leaf ( Fig. 1 B and SI Appendix, Figs. S15 and S19 A and B) and pseudostrobili ( Fig. 1 D and SI Appendix, Fig. S22 A–C) rachises have a reversed Ω- shaped vascular bundle. Protoxylem strands occur at the lateral margins of the bundle, while pinnule traces and sporophyll (i.e., pinnule homolog) traces are given off from the lateral ends of the vascular bundles of the rachis and “strobilus” axis, respectively (SI Appendix, Figs. S19 E, S20 A‒C, and S22 C).

Many pseudostrobili show four to five rows of sporangia with rows arranged parallel to the rachis ( Fig. 1 I and K and SI Appendix, Figs. S5‒S8). As the specimens have been affected by postmortem compression (SI Appendix, Figs. S5‒S8), we consider that there must have been a row of sporangia on either side that was laterally flattened; we estimate that a complete pseudostrobilus comprised 8 or 10 sporangia per whorl. Sporophylls are proximally fused laterally to adjacent sporophylls, while distally they are free with a small heel and upturned apex (SI Appendix, Figs. S21 D and S23 E). There are 32 to 35 sporangia per row in the pseudostrobili depending on the length of the pseudostrobili, producing five sporangia per centimeter’ s length. Sporangia are sessile, attached to the sporophylls adaxial surface ( Fig. 1 I–M ). Megasporangia occur in a single vertical row on the pseudostrobilus axis ( Fig. 1 K–M and SI Appendix, Figs. S21 B and F and S23 A) and, although poorly preserved, have a single functional megaspore. As pseudostrobili are born horizontally from the stem, the vertical row of megaspores would have been organized horizontally in life. Due to preservation limitations, we cannot determine where in life the megasporangial row was positioned, but we suspect it was at the bottom of the pseudostrobilus and caused pooling of the hormone auxin under gravity to trigger megasporangial expression ( 9). Microspores are of the Calamospora type; trilete circular, subcircular to oval, 30 to 40 μm in diameter, with straight rays of the trilete mark forming a labrum extending 3/4 or the whole radius a laevigate exine that forms irregular folds usually parallel to the margin ( Fig. 1 N and SI Appendix, Fig. S23 D).

Detailed descriptions, measurement, and further illustrations are provided in SI Appendix, Detailed Description.

P. wuhaia J. Wang et al. is reconstructed as a small, slender, unbranched palm-like tree in Fig. 2 , two to many meters high. Its major characteristics are illustrated by a diagrammatic reconstruction as shown in Fig. 3 . The details of its stem anatomy are consistent with that of progymnosperms and early seed plants (SI Appendix, Figs. S16–S18).

Comparisons. Following Wang et al. ( 9), we consider the noeggerathialean fertile shoot to be a pseudostrobilus because despite its radial exterior appearance, it is distinctly bilateral in organization and represents a complex, three-dimensional “sporophyll” (SI Appendix, Terminology). We use quotation marks to denote what would traditionally be interpreted as sporophylls on the pseudostrobilus axis that represent pinnule homologs and are not in fact sporophylls in the traditional sense.

P. wuhaia J. Wang et al. is most similar to the contemporaneous species P. wudensis ( 17) also from the Wuda Coalfield. Within the coalfield, the two species grew in different areas, with P. wuhaia dominating central and northern parts while P. wudensis occurs in low density only in the southern parts. P. wudensis is distinguished from P. wuhaia in forming smaller trees with comparatively larger pseudostrobili, and possessing needlelike small pinnules that are very different from the small, oval pinules in P. wuhaia (see SI Appendix, Systematic Comparisons, for further details). Furthermore P. wudensis has more than one megaspore per megasporangium ( 17) unlike the single megaspores in P. wuhaia megasporangia. The fertile shoots of P. wuhaia are similar to the late Permian heterosporous noeggerathialean pseudostrobilus Dorsalistachya quadrisegmentorum ( 9) that is associated with Plagiozamites oblongifolius megaphyllous leaves; its leaves and pseudostrobili also have Ω- shaped bundles but lack secondary xylem. Dorsalistachya is further distinguished from Paratingia in having winged monomegasporangia in short, vertical rows ( 9) and possessing more complexly divided sporophylls. Adaxially curved and C-shaped primary xylem strands at the innermost part of the xylem cylinder in Paratingia ’s stem differ from those in gymnosperms and Archaeopteris (progymnosperm) in which strands are isodiametric in cross-section. Broad, arc-shaped leaf traces in the innermost part of the xylem cylinder of the progymnosperm Protopitys ( 18) are similar to the c-shaped primary xylem strands in Paratingia stems, but Protopitys stems bear large, distichously arranged fronds with bilateral symmetry and plannated branching bearing terminal sporangia in fertile trusses that lack associated leaves or sporopylls ( 1, 5, 18) (see SI Appendix, Tables S1 and S2 for detailed comparisons).

Figures

Fig. 1. P. wuhaia J. Wang et al. sp. nov. from the early Permian Taiyuan Formation of Wuda Coalfield, Inner Mongolia. (A) Holotype with an entire crown consisting of pseudostrobili and leaves. (B) Once-pinnate compound leaf with both large and small pinnules visible. Reprinted with permission from ref. 15. (C) Cross-section of a crown illustrating pseudostrobili around the stem. (D) Cross-section of pseudostrobilus with microsporangia around the axis with bilateral, inversed Ω-shaped vascular bundle. (E) Cross-section of a leaf rachis showing the same form of vascular bundle as that of pseudostrobili axes. (F–H) Partial cross, radial, and tangential sections of the stem showing the secondary xylem (wood). (I) Tangential section of pseudostrobilus showing sporangial arrangement with single line of megasporangia along with the axis (middle-right pseudostrobilus of the fragmental crown illustrated SI Appendix, Fig. S8; specimen PB22132; magnified in SI Appendix, Fig. S21C.) (J) Radial section of pseudostrobilus showing adaxial sporangia and axis lacking nodes (upmost-left pseudostrobilus of the fragmental crown in SI Appendix, Fig. S8; magnified in SI Appendix, Fig. S21A). (K) Tangential section showing adaxial sporangia and a single line of megasporangia along with the axis (SI Appendix, Fig. S7; specimen PB22131, second up-right pseudostrobilus). (L) Tangential section through same specimen as K showing megasporangial arrangement (magnified in SI Appendix, Figs. S21B and S23A). (M) Detail of the middle part of L showing the megasporangia and microsporangia. (N) Single spore macerated from the holotype. (Scale bars: A, 10 cm; B, 3 cm; C–E, 1 cm; F, 100 μm; G and H, 200 μm; I–L, 5 mm; M, 2 mm; N, 10 μm.)

Fig. 2. Reconstruction of the aerial parts of P. wuhaia J. Wang et al. sp.nov. from the early Permian of China (based on the holotype). Image credit: Yugao Ren and Sijia Tang (artists).

Fig. 3. Diagrammatic reconstruction of the key features of P. wuhaia J. Wang et al. (A) Stem bears pseudostrobili and once-pinnate compound leaves; pseudostrobili are attached to the fertile zone, above which the leaves are shown from the abaxial side, and below which the leaves are shown from the adaxial side. (B) A pseudostrobilus shown its longitudinal surface. (C) Cross-section of a pseudostrobilus showing both megasporangia and microsporangia, the bilateral symmetrical Ω-shaped vascular bundle and sporophylls; noting the relative position of the presumed two megasporangia and the orientation of the opening of the vascular bundle. (D) Partial longitudinal section through the central axis of the pseudostrobilus and the symmetric axis of the vascular bundle, approximately corresponding to the dashed line in C; (E) partial of the leaf showing the arrangement of the small and big pinnules, seen from the abaxial (Upper) and adaxial (Lower) sides, respectively; (F) a pair of small and big pinnules showing the radiate venation; (G and H) cross-section of the stem showing the anatomy; H is the magnification of a part (within the dashed line) of the stem in G. CT, cortex; LT, leaf trace; MEG, megasporangium; MIG, microsporangium; PD, periderm; PT, pith; PX, primary xylem; SP, sporophyll; SX, secondary xylem; VB, vascular bundle.