Significance The evolution of trees and forests in the Mid–Late Devonian Period, 393–359 million years ago, profoundly transformed the terrestrial environment and atmosphere. The oldest fossil trees belong to the Cladoxylopsida. Their water-conducting system is a ring of hundreds of individual strands of xylem (water-conducting cells) that are interconnected in many places. Using anatomically preserved trunks, we show how these trees could grow to a large size by the production of large amounts of soft tissues and new wood around the individual xylem strands and by a controlled structural collapse at the expanding base. We have discovered a complex tree growth strategy unique in Earth history, but with some similarity to that of living palms.

Abstract Cladoxylopsida included the earliest large trees that formed critical components of globally transformative pioneering forest ecosystems in the Mid- and early Late Devonian (ca. 393–372 Ma). Well-known cladoxylopsid fossils include the up to ∼1-m-diameter sandstone casts known as Eospermatopteris from Middle Devonian strata of New York State. Cladoxylopsid trunk structure comprised a more-or-less distinct cylinder of numerous separate cauline xylem strands connected internally with a network of medullary xylem strands and, near the base, externally with downward-growing roots, all embedded within parenchyma. However, the means by which this complex vascular system was able to grow to a large diameter is unknown. We demonstrate—based on exceptional, up to ∼70-cm-diameter silicified fossil trunks with extensive preservation of cellular anatomy from the early Late Devonian (Frasnian, ca. 374 Ma) of Xinjiang, China—that trunk expansion is associated with a cylindrical zone of diffuse secondary growth within ground and cortical parenchyma and with production of a large amount of wood containing both rays and growth increments concentrically around individual xylem strands by normal cambia. The xylem system accommodates expansion by tearing of individual strand interconnections during secondary development. This mode of growth seems indeterminate, capable of producing trees of large size and, despite some unique features, invites comparison with secondary development in some living monocots. Understanding the structure and growth of cladoxylopsids informs analysis of canopy competition within early forests with the potential to drive global processes.

One of the key episodes in the history of the Earth is “afforestation,” the Devonian transition to a forested planet (1)—that is, the development of tree-sized vegetation leading to step changes in the behavior of sediment on flood plains, clay mineral production, weathering rates, CO 2 drawdown, and the hydrological cycle (2, 3). In many ways, this event represents perhaps the most fundamental change in Earth system dynamics between the truly ancient and modern.

The fossil record strongly indicates that the origin of trees was not a solitary evolutionary innovation confined to a single clade. Cladoxylopsid trees appeared first (4) [early Mid-Devonian (Eifelian), 393–388 Ma], followed by archaeopteridalean and lycopsid trees [late Mid-Devonian (Givetian), 388–383 Ma] (5, 6). Archaeopteris, an early lignophyte, has the most familiar tree growth strategy, exhibiting extensive secondary development by producing secondary xylem (wood) laid down in concentric growth increments by a cylindrical bifacial vascular cambium (7, 8). Lycopsids produced limited secondary xylem and expanded their trunk diameter largely by extensive periderm production (9).

Anatomically well-preserved cladoxylopsids known to date, including Pietzschia from the Late Devonian (Famennian, 372–359 Ma) of Morocco (10, 11), probably indicate a primary thickening meristem capable of forming a primary body (and therefore trunks) up to 160 mm across, but demonstrate no secondary increase in diameter. Such plants were likely determinate in growth and limited in size. However, Eospermatopteris bases (12) from the older, Mid-Devonian (ca. 385 Ma) in situ Gilboa fossil forest (New York) (13), reached basal diameters of 1 m supporting long tapering trunks (14). The sandstone casts (Fig. 1) reveal coalified vascular strands but only a little preserved cellular anatomy. Thus, despite fragmentary evidence that radially aligned xylem cells in some partially preserved cladoxylopsid fossils may indicate a limited form of secondary growth (4, 7, 11, 15, 16), it remains unclear how this type of plant dramatically increased its girth. We present here exceptionally preserved large trunks from China (Figs. 2 and 3) that demonstrate direct evidence of how these earliest trees were able to expand their trunk diameter and thereby achieve tree size.

Fig. 1. Vascular system of Eospermatopteris from the Middle Devonian of Gilboa, NY. (A) Schematic representation of the vascular system based on our observations of the large sandstone trunk casts with largely coalified xylem. By analogy with Xinicaulis, black indicates cauline xylem strands, blue indicates medullary xylem strands, and orange indicates adventitious roots. The principal difference between this system and that of Xinicaulis is that the cauline xylem strands are apparently arranged in a single, not double, cylinder. (B) Lateral view of large specimen on display at the roadside in Gilboa, NY, showing overall form, longitudinal parallel cauline xylem strands, and casts of roots on surface. Basal diameter: ∼1 m. (C) Close up view of the rectangle indicated in B, showing proximal parts of roots emerging from the surface of the cast. (Scale bar, 50 mm.) (D) Basal view of upturned stump on open air display at Gilboa Museum, showing outward-dichotomizing cauline xylem strands in base. (Scale bar, 10 cm.) (E) Lateral view of specimen on display at Blenheim-Gilboa Visitors Center, North Blenheim, NY, showing internal network of medullary xylem strands exposed on the sides and underneath. Diameter of base: ∼50 cm.

Fig. 2. X. lignescens gen. et sp. nov. from the Upper Devonian of Xinjiang, Northwest China. The largest silicified trunk in the field, with a maximum diameter of ∼70 cm. Pieces PB22120 and PB22121 collected from this trunk were cut into serial slices. (A) Oblique transverse view. (B) Lateral view. The trunk is about 1 m long in preserved length.

Fig. 3. X. lignescens gen. et sp. nov. from the Upper Devonian of Xinjiang, Northwest China. (A) Illustrative transverse plane through the small trunk, showing the three naturally fractured parts. Note at least 33 cauline xylem strands forming a double cylinder, some in the process of dividing (S), emitting adventitious roots (R), or emitting medullary strands (M). About 30 medullary xylem strands, of irregular shape, are visible in the almost intact pith. For 3D structure, prepared slices, and strand numbering, see Fig. 4 and Fig. S3. Holotype: PB22119. (B) Transverse slice of the outer region of the large trunk (70-cm diameter; see Fig. 2) showing the exterior roots in parenchyma, eight cauline xylem strands, medullary strands in pith parenchyma, and a sediment-infilled pith cavity (P). PB22120.

Discussion Our results indicate that the large size of Xinicaulis on a scale equivalent to Eospermatopteris was accomplished by a unique form of secondary development, facilitated primarily by a long-acting cylindrical zone of diffuse secondary growth in ground and inner cortical tissues of the base and main trunk. Although similar to some monocots in general behavior (23), secondary growth in the stems of Xinicaulis did not produce distinctive radial files of parenchyma or additional vascular strands. Instead, continued activity served only to increase overall volume of the stem via mostly unordered parenchyma and created patterned fracturing of the vascular strands at primary xylem dichotomies in both proximal and distal directions. Since increase in tissue volume has important consequences, both physiological and structural, it seems very likely that all cladoxylopsid plants of tree size using this mode of growth of necessity would have a hollow pith (Fig. 3B and Fig. S1B). In addition, Xinicaulis is also associated with an equally unusual form of secondary development in which radial files of secondary xylem are produced by cambia around individual cauline strands, medullary strands, and roots rather than forming a single solid cylinder as generally expected in seed plants. Secondary xylem greatly increased both conductive capacity and support presumably to keep pace with increasing size of the plant during development. It is interesting to note that cell walls of the secondary xylem in Xinicaulis are unusually thick, for example, compared with Callixylon (the trunk of the progymnosperm tree Archaeopteris) from the same locality (Fig. S7), possibly indicating relatively greater importance of support over conductive capacity in a fibrous plant body overall (and suggesting a significant capacity for cladoxylopsids to drawn-down atmospheric carbon). Fig. S7. Comparison of Xinicaulis wood with wood from Archaeopteris from the same locality. (A) Representative sample of Xinicaulis wood in thin section, showing the thickness of cell walls. Within the yellow boundaries indicated (excluding the ray) the proportion of the cross-section represented by cell walls is 85%. A ray tracheid runs across the middle of the view (PB22119-C6). (B) Representative sample of the wood of Archaeopteris sp. (Callixylon) from the same locality from an etched thick section. Within the yellow boundary, the proportion of the section represented by cell walls is 31% (PB22122). The manner of secondary development in Xinicaulis seems potentially indeterminate and thus capable of producing trees of very large size. This invites close comparison with Eospermatopteris, with stumps showing similar size and taper as our largest Chinese specimen and with a similar construction of the xylem system including longitudinal cauline xylem strands, anastomosing medullary xylem strands, central pith, and external adventitious roots (12⇓–14). Fragmentary coalified, but clearly formerly woody, xylem strands have also been found preserved within Eospermatopteris casts (Fig. 1). However, unlike in the large Xinjiang Xinicaulis specimen, the very bottom of the trunk is clearly represented. Our observations of Eospermatopteris suggest the initially upright, upward-dichotomizing, upward-expanding part of the vascular system produced during early development may end up as a radially expanded horizontally almost flattened disk (Fig. 1D) in larger trees due to continued lateral diffuse secondary growth combined with longitudinal structural failure with increasing size over time (Fig. 7). Fig. 7. X. lignescens gen. et sp. nov. Schematic model of development showing the position of the blocks describe in this paper. A developmental model showing three growth stages of the trunk in lateral (Upper) and basal (Lower) view. Colors show primary cauline xylem strands formed in a time series from the growing apex. (A) Juvenile stage: the primary body has grown sufficiently to produce about 30 cauline strands by upward dichotomy of individual strands. (B) Intermediate stage with further enlargement of the primary body and a maximum number of cauline xylem strands produced (black lines). (C) Mature stage with maximum secondary growth of cauline xylem strands to produce large diameter trunk. In this model, suggested here by C. M. Berry and W. E. Stein based on observations on Eospermatopteris from New York, the upward-dichotomizing cauline and medullary xylem system is gradually incorporated into the almost flat expanding base (Fig. 1D). The alternative, a tree-fern like basal system, as found in Pietzschia with primary growth only (18), is considered unlikely in such a large trunk. Sp indicates the hypothetical position of the small trunk specimen with largely only primary growth, and Ss indicates the position of the same specimen with secondary growth as illustrated in this paper. Lp indicates the hypothetical position of the large trunk specimen with largely only primary growth, and Ls indicates the position of the large specimen following secondary growth as illustrated in this paper. By contrast, other cladoxylopsid trees such as Pietzschia so far exhibit only primary growth and retain an intact, partially vascularized pith (10, 11). If representative of determinate development, it seems likely that these examples adopted a tree fern strategy (18) whereby upward increasing complexity and size of the primary body (epidogenesis) was supported by an ever-enlarging root mantle. However, given what we know at this point in time, there is no reason to preclude intermediate conditions with various degrees of secondary development and a concomitant shift in support strategy. Most intriguing, perhaps, is the obvious convergence in form and development between Xinicaulis, and by implication some other cladoxylopsids, and living tree-form monocot angiosperms, such as palms, to be contrasted with “true” secondary development via a single well-organized vascular cambium as seen in most lignophytes. Although unique in significant respects (production of secondary xylem around each vascular strand via a normal vascular cambium and patterned fracture of the primary xylem architecture during secondary development), the general mode of development of Xinicaulis is nevertheless eminently recognizable among modern forms. The model of both primary and secondary development in cladoxylopsids that we propose closely follows a long-standing view by Eckhardt (24; also cited in ref. 19, p. 390), so much so that nothing ad hoc seems necessary. Although strikingly similar, it is also reasonably clear that cladoxylopsids and palms evolved these features independently (7), so an analogy in growth can be carried only so far. However, the fact that palms, Xinicaulis, likely Eospermatopteris, and, for that matter, at least some cormose tree lycopsids all share significant structural similarities including few apical meristems, a strong central axis, and many roots of nearly equal size (usually termed “rootlets”) may indicate what is possible, but perhaps also limiting, in plants of tree size lacking a standard single cylindrical vascular cambium.

Materials and Methods We predominantly studied thick transverse and longitudinal sections of the silicified trunks. These were cut by saw and then polished by hand on a grinding wheel or on a vibrating lap to give a uniform black finish. The exposed surfaces were etched for 45–90 s in hydrofluoric acid (HF) in a dedicated HF fume hood. Testing of these samples showed that there was no need to pretreat the material in HCl to remove carbonates as none were present. The reaction with HF resulted in the carbonized cell walls being clearly visible against the white frosted silica. The sections were subsequently rinsed in water with the runoff neutralized in supersaturated sodium carbonate solution. After neutralization, the specimens were further washed in running water for several hours and then air-dried. Standard protocols and personal protective equipment for HF work were adopted while handling HF and HF-contaminated specimens. The dry specimens were photographed with a Nikon D800 camera and 60-mm macro lens or Leica M12 microscope. Some small thin sections were ground by hand using traditional techniques to study histological details. They were photographed using a Leica DMR compound microscope and Leica cameras. Measurements were made using Leica LAS software. All specimens were deposited in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China, with the prefix PB.

Acknowledgments This study was financially supported by the Natural Science Foundation of China (Grants 41530103 and 41772012). Natural Environment Research Council Grant NE/J007897/1 (to C.M.B. with W.E.S. as visiting researcher) made possible the collaboration between W.E.S., H.-H.X., and C.M.B., and the parallel study of Eospermatopteris.

Footnotes Author contributions: H.-H.X., Y.W., P.T., and Q.F. made initial discovery; H.-H.X., Y.W., P.T., and Q.F. did fieldwork; H.-H.X. and Y.W. did geological interpretation; H.-H.X. and C.M.B. designed research; H.-H.X., C.M.B., W.E.S., Y.W., P.T., and Q.F. performed research; H.-H.X., C.M.B., and W.E.S. analyzed data; and H.-H.X., C.M.B., and W.E.S. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

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