Reconstructing Krassilovia mongolica supports recognition of a new and unusual group of Mesozoic conifers

Abstract

Previously unrecognized anatomical features of the cone scales of the enigmatic Early Cretaceous conifer Krassilovia mongolica include the presence of transversely oriented paracytic stomata, which is unusual for all other extinct and extant conifers. Identical stomata are present on co-occurring broad, linear, multiveined leaves assigned to Podozamites harrisii, providing evidence that K. mongolica and P. harrisii are the seed cones and leaves of the same extinct plant. Phylogenetic analyses of the relationships of the reconstructed Krassilovia plant place it in an informal clade that we name the Krassilovia Clade, which also includes Swedenborgia cryptomerioides-Podozamites schenkii, and Cycadocarpidium erdmanni-Podozamites schenkii. All three of these plants have linear leaves that are relatively broad compared to most living conifers, and that are also multiveined with transversely oriented paracytic stomata. We propose that these may be general features of the Krassilovia Clade. Paracytic stomata, and other features of this new group, recall features of extant and fossil Gnetales, raising questions about the phylogenetic homogeneity of the conifer clade similar to those raised by phylogenetic analyses of molecular data.

Fig 1. Seed cones, cone axis, bract-scale complexes, and winged seeds of Krassilovia mongolica and associated leaves of Podozamites harrisii.

(A–C) Articulated seed cones showing tightly imbricate interlocking bract-scale complexes (A: PP55848; B: PP59064; C: PP59065). (D) Isolated cone axis; note conspicuous spirally arranged abscission scars (PP59066). (E) Incomplete leafy shoot showing a cluster of three attached leaves (one represented only by the leaf base); the fourth leaf (left) was attached to the axis when discovered (PP56218). (F) Three detached strap-shaped leaves; note variation in leaf size and shape, and conspicuous parallel venation (PP56226; PP56223; PP56222). (G) Detail of A showing tightly imbricate interlocking bract-scale complexes. (H) Detail of leaf apex showing converging veins (left; PP56228); leaf base showing the absence of a clearly differentiated petiole (right; PP56230). (I) Three isolated bract-scale complexes showing abaxial (top) and adaxial (bottom) surfaces; note three prominent, spiny, distal lobes and two prominent, spiny, proximal lobes (PP59067; PP59068; PP59069). (J) Two isolated seeds showing narrow wings and variation from more or less symmetrical (top; PP59070), to strongly asymmetrical (bottom; PP59071). Scale bars: E, F = 1 cm; A–C, G = 5 mm; D, H, I = 2 mm; J = 1 mm.

Fig 2. Scanning electron micrographs showing similarities between inner surface of cuticles of leaves of Podozamites harrisii (A–C) and bract-scale complexes of Krassilovia mongolica (D–F).

(A, B) Detail of stomatal band from abaxial leaf cuticle showing cell outlines of transversely oriented, paracytic (monocyclic) stomata (PP56233). (C) Detail from adaxial leaf cuticle showing rectangular epidermal cell outlines formed by regular transverse and longitudinal divisions; note that many epidermal cell outlines are arranged in pairs (arrow) (PP56234). (D, E) Cuticle from bract-scale complexes showing cell outlines of paracytic (monocyclic) stomata (arrows) that are transversely oriented relative to the files of epidermal cells (D: PP59072; E: PP56235). (F) Cuticle from bract-scale complex showing rectangular epidermal cell outlines formed by regular transverse and longitudinal divisions; note that many epidermal cell outlines are arranged in pairs (arrow) (PP56236). Scale bars: C = 50 μm; A, B, D–F = 20 μm.

Fig 3. Light micrographs showing anatomy of axis and bract–scale complexes of Krassilovia mongolica (A–F) and leaves of Podozamites harrisii (G, H).

(A) Transverse section of the axis showing collapsed thin-walled cells with scattered sclerenchyma cells (PP59073). (B) Detail of transverse section of a bract-scale complex near the base of the stalk; note sclerenchyma (Sc) and well developed parenchyma (Pc) (PP59074). (C) Detail from B inside Sc showing an extremely small amount of xylem; note xylem with relatively thin walls and wide lumens (arrow). (D) Detail of transverse section of bract-scale complex showing thin cuticle and well developed epidermis; note the dark contents of the epidermal cells (PP59074). (E) Transverse section through a distal lobe of a bract-scale complex showing central vascular tissue with xylem (Vl) surrounded by sclerenchyma (PP59074). (F) Detail of transverse section of bract-scale complex showing well-developed sclerenchyma (Sc) and scattered cells with dark contents (PP59074). (G) Transverse section of leaf showing the position of three vascular bundles (arrows) (PP59075). (H) Detail of transverse section of leaf showing thin cuticle (top arrow), large thin-walled mesophyll cells with dark contents (middle arrow), xylem cells (arrowhead) flanked by large patches of transfusion tracheids-like cells (lower arrow) (PP59075). Scale bars: B, E, G = 200 μm; A, F = 100 μm; D, H = 50 μm; C = 40 μm.

Fig 4. Neutron tomographic reconstruction of isolated bract–scale complex of Krassilovia mongolica (PP59076).

RNA = Relative Neutron Attenuation (high to low), cross-hatch area represents relative transparency (top left box). (A) Volume rendering of lateral view of bract-scale complex; (Abx, abaxial: Adx, adaxial). (B–D) Transverse sections from base to top of stalk for the bract-scale complexes in (A). Epidermis and hypodermis has lowest neutron attenuation (blue); vasculature tissue (Vl) has the intermediate neutron attenuation (green); cortical ground tissues (Gt) have the highest neutron attenuation. (E) Diagrammatic reconstruction near the base of stalks; vasculature appears slightly close to the abaxial (Abx) and the ground tissue forms two strands near the adaxial side (Adx) (see also Fig 3B and 3C and S7 Appendix).

Fig 5. Phylogenetic analyses of selected Late Paleozoic to Early Mesozoic conifers.

(A) Strict consensus of 10 most parsimonious trees of 190 steps showing the Krassilovia Clade with Swedenborgia-Podozamites, Cycadocarpidium-Podozamites, and the Krassilovia plant. (B) Detail of strict consensus of 41 most parsimonious trees of 198 steps with the inclusion of the Dechellyia-Masculostrobus plant, a putative early gnetalean (see S5 Appendix for complete tree). Bootstrap values given for nodes > 50%.

Fig 6. Reconstruction of Krassilovia mongolica.

(A) Complete mature seed cone showing the strongly imbricate spiny bract-scale complexes. (B) Isolated bract-scale complex in adaxial view showing five seed scars (top left), isolated bract-scale complex in adaxial view with five seeds (top middle), isolated bract-scale complex in abaxial view showing the inconspicuous leafy bract (top right); isolated bract-scale complexes in lateral view showing seed scars and leafy bract (bottom). (C) Isolated asymmetrical (top) more or less symmetrical (bottom) winged seeds. (D) Isolated seed cone axes showing prominent abscission scars. Drawings not to scale. Credit: Pollyanna von Knorring.

Fig 7. Reconstruction of a branch of Krassilovia mongolica bearing terminal seed cones and alternately arranged leafy shoots of Podozamites harrisii.

Mature and maturing cones are depicted distally showing the ultimate disarticulation of the bract-scale complexes and the dispersal of the winged seeds. Credit: Pollyanna von Knorring.