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2Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701 USA; 3Department of Biology, Faculty of Science and Science Education, University of Haifa–Oranim, Tivon 36006, Israel
Received for publication August 26, 2004. Accepted for publication February 25, 2005.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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Key Words: Archaeopteris • fossil wood • polar auxin flow • spiral xylem • vascular differentiation
The ability to form a well-developed water-conducting and mechanical system in the form of secondary vascular tissues (wood) was one of the most crucial developments in the evolution of terrestrial ecosystems. This was a key feature enabling the establishment of large stratified plant communities (forests) and extensive biomass production in terrestrial habitats (Chaloner and Sheerin, 1979
; DiMichele et al., 1992
). Archaeopteris Dawson (some stems of which are named Callixylon whiteanum Arnold) (Fig. 1) was the first known true forest tree (Meyer-Berthaud et al., 1999
), forming the canopy vegetation of the most ancient known stratified plant communities (DiMichele et al., 1992
). This taxon is also the best-known representative of the extinct progymnosperms, a group that shared both the character of secondary vascular tissues and a common ancestor with modern seed plants (Crane, 1985
; Beck and Wight, 1988
; Rothwell and Serbet, 1994
).
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), with secondary xylem appearing later, in the Middle Devonian (Wight and Beck, 1984
) (i.e., aneurophytalean progymnosperms, ca. 380 mya). However, secondary vascular tissues evolved independently in at least two major groups of vascular plants. These two lineages of secondary vascular tissues were not homologous (Cichan, 1985
). The first was in a clade that includes the extinct progymnosperms (Crane, 1985
; Rothwell and Serbet, 1994
) and seed plants, where a bifacial vascular cambium usually forms xylem toward the inside and phloem toward the outside (Larson, 1994
). Species of the second group (or groups) produced either a unifacial vascular cambium or a cambium that differentiated secondary vascular tissues only toward the inside, and except for the quillwort Isoetes (Lycopsida), are all extinct (Stewart and Rothwell, 1993
; Rothwell and Karrfalt, 1996
).
Vascular tissue differentiation of living pteridophytes and seed plants is under the control of several plant growth regulators such as auxins, gibberellins, cytokinins, and ethylene (Savidge and Wareing, 1981
; Uggla et al., 1996
; Cooke et al., 2002
). Moreover, polar auxin transport has been found in some algae and bryophytes (Basu et al., 2002
; Cooke et al., 2002
). It has already been proposed that polar auxin flow was involved in the regulation of vascular differentiation in fossil plants (Stein, 1993
; Boyce and Knoll, 2002
). In both living woody seed plants and Archaeopteris, the axially elongated tracheary elements of the secondary xylem follow a uniformly straight or inclined course. When various obstacles such as buds, branches, and wounds disrupt the axial polar auxin flow in or near the cambial region of seed plants (conifers and dicotyledons), polar auxin flow whirlpools are formed in the cambial zone (Sachs and Cohen, 1982
). These auxin whirlpools induce the differentiation of characteristic circular tissue patterns of tracheary elements above axillary buds of woody plants (Hejnowicz and Kurczy
ska, 1987
) and at branch junctions in the wood of conifers (Lev-Yadun and Aloni, 1990
) (Fig. 2) and dicotyledonous woody plants (Lev-Yadun and Aloni, 1990
) (Fig. 3). Identical circular patterns also occur at the same positions in the secondary wood of the Upper Devonian fossil progymnosperm Archaeopteris (Figs. 4, 5), thus providing the first clear fossil evidence of polar auxin flow. Such spiral patterns do not occur in the primary xylem of either fossil progymnosperms or extant seed plants. They are also absent from the primary xylem strands of living ferns and other nonseed plants such as Psilotum nudum (L.) Beauv., and from the Lower Devonian fossil land plants that we have examined [ca. 390–385 million-years-old Aglaophyton major (Kidston and Lang) D. Edwards; Renallia hueberi Gensel; and Psilophyton dawsonii Banks, Leclercq & Hueber].
The 375 million-year-old fossil that has circular vascular patterns is an anatomically well-preserved log 4.0 m long and 0.6 m in diameter (Fig. 1). It was collected from Upper Devonian deposits of Oklahoma, USA, and contains both primary and secondary xylem (Trivett, 1993
). A large number of leaf and branch traces are embedded in the wood of this log, and tangential sections of the secondary xylem reveal distinctive circular patterns of tracheids and accompanying parenchyma cells immediately distal to and adjacent to branch traces (Figs. 4, 5).
Is it possible that the cellular/molecular mechanism that currently induces circular secondary xylem at branch junctions has been conserved for 375 million years? Or, were the circular patterns we describe in Archaeopteris the outcome of an alternative extinct regulatory mechanism? Unlike animals, for which the skeleton is produced at the organismal level and the other soft parts are rarely preserved in fossils, plants have their skeleton at the cellular level (as a cell wall) so that all tissues are routinely fossilized. In addition, plant fossils record a history of their ontogenetic development within their vascular tissues, so that they preserve a detailed fossilized record of their individual developmental history.
We find no need to propose an alternative mechanism because no special assumptions are required to explain our findings within the confines of the current paradigm. In contrast to animals in which members of several phyla (i.e., Coelenterata, Annelida, Mollusca, Arthropoda, Tetrapoda) evolved the land lifestyle independently of one another, vascular land plants are monophyletic (Kenrick and Crane, 1997
). Because the various animal groups were evolutionarily divergent, they evolved analogous solutions to similar challenges. However, the largely polar auxin-transport-based mechanism of vascular tissue patterning is common to primary and secondary vascular tissues. Therefore, it was already present in the common ancestors of vascular land plants that developed secondary vascular tissues. Because such spiral patterns do not occur in the primary xylem of living non-seed plants such as Psilotum nudum and nonwoody monocotyledons at branch junctions, it is obvious that branching itself does not induce spiral vascular tissues.
A comparison of the homology of expressed genes in the differentiating secondary xylem of Pinus taeda (a gymnosperm) with those of Arabidopsis thaliana (an angiosperm) indicates the possible conservation of the mechanism. This is further supported by the fact that polar auxin transport is involved in vascular differentiation of pteridophytes and seed plants (Cooke et al., 2002
), and that it also exists in algae and bryophytes (Basu et al., 2002
; Cooke et al., 2002
). In spite of the at least ca. 300 million years that have passed since their last common ancestor (Rothwell et al., 1997
), ca. 90% of the 1100 base pairs or longer xylem-forming-related pine contigs had an apparent Arabidopsis homolog (Kirst et al., 2003
). Both pines (Lev-Yadun and Aloni, 1990
) and A. thaliana (Lev-Yadun, 1996
) produce spiral secondary xylem above branch junctions like Archaeopteris. The additional 75 million years or less separating the extinct sister group of Pinus taeda and A. thaliana from Archaeopteris does not seem to be enough time to account for the evolution of a totally different mechanism of polar signal transduction in the cambial region in Archaeopteris and thus circular secondary xylem. Moreover, microRNA target sequences of class-III homeodomain-leucine zipper gene family of A. thaliana are conserved in all land plants including bryophytes, lycopods, ferns, gymnosperms, and angiosperms (Floyd and Bowman, 2004
). One of these genes (REVOLUTA/IFL1) is involved in the polar auxin flow in A. thaliana stems (Zhong and Ye, 2001
; Zhong et al., 2001
), the regulatory system discussed here. Therefore, the period of 375 million years discussed here is considerably shorter than the already known period of conservation of some components of polar auxin transport in land plants.
As shown here, the circular-patterned secondary xylem at branch junctions of the 375 million-year-old extinct tree Archaeopteris is the earliest clear structural evidence from the fossil record of deviations in the axial polar auxin flow. Such patterns show that a diagnostic developmental regulatory mechanism originated in seed-plant ancestors at least 375 mya, thus establishing that the fossil record can be employed to identify physiologically based developmental mechanisms of key evolutionary innovations. These data provide strong evidence that secondary vascular tissues in seed plants and their extinct progymnospermous sister groups, such as Archaeopteris, have been regulated by homologous mechanisms of current genetic and physiological control, thereby establishing the developmental origin of the shared derived character (i.e., wood) that allows seed plants and their extinct ancestors to grow into giant trees and to occupy arid regions. This discovery reveals an exciting potential for plant fossils to provide direct evidence of evolutionary diagnostic physiological and developmental mechanisms, and for the use of a combination of fossil evidence and current developmental biology to characterize evolutionary patterns in terms of specific genetic changes in growth regulation.
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FOOTNOTES |
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4 Authors for correspondence (e-mail: rothwell{at}ohio.edu
; levyadun{at}research.haifa.ac.il
)
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LITERATURE CITED |
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TOPABSTRACTLITERATURE CITED |
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