MODELING THE EVOLUTION OF STELLAR ARCHITECTURE IN VASCULAR PLANTS

The control of primary vascular tissue differentiation by auxin produc ed by the shoot apex ranks among the better known hormone signaling sy stems in vascular plants. Surprisingly little is known, however, about the relationship between the pattern-forming properties of this syste m and stelar architectures in different major groups of vascular plant s, including those represented in an extensive and systematically impo rtant fossil record. Expanding upon suggestions by Wight, I present a simple computer model relating known properties of the auxin signaling system with explicit predictions about the configuration of stelar ti ssues suitable for comparison with morphometric data derived from both living and fossil plants. The model divides the continuous acropetal process of vascular tissue determination into a series of vignettes in which target meristematic tissue receives quantified concentrations o f hormone, i.e., auxin, from ''organizing centers'' (OCs), branch or l eaf primordia, serving as hormone sources. Specific parameters of the model include longitudinal spacing, phyllotaxis, variable hormone prod uction rates of the OCs, size of the shoot apex, and reaction of the t arget tissue to specific signals received. To test the applicability o f this approach, model predictions are compared with detailed morphome tric data collected from Psilophyton and members of the Aneurophytales . Close correspondence is observed between predicted hormone concentra tions from the model and the configuration of stelar tissues, includin g relative positions of primary xylem, primary phloem, secondary xylem , and the presence of morphological gradients in the primary xylem rel ated to the protoxylem/metaxylem continuum. In addition to the morphom etric comparisons, a wider exploration of the model involving both ort hostichous and Fibonacci phyllotaxis of OCs is conducted. The results are compared with members of the Iridopteridales, Cladoxylopsida, Cala mopityaceae, and Medullosales. Striking correspondence is observed all owing for reinterpretation of the evolution of vascular plant stelar a rchitecture not just in terms of historical patterns of important matu re structures but also as a system of evolving developmental dynamics underlying these structures. All comparisons made so far ser-ve to und erscore the fundamental relationship in early vascular plants between the evolution of increased complexity in stelar architectures and the evolution of complex lateral branches and leaves. Among evolutionary e vents occurring in the fossil record, the model of hormone determinati on offers important insights into (1) origin of fibbed protostelic sys tems from primitive columnar architectures as a consequence of increas ed compactness of the shoot apex and orthostichous phyllotaxis; (2) co nspicuous differences in the three-dimensional configuration of protox ylem strands supporting a developmental distinction between Devonian ' 'radiate protoxylem'' and ''permanent protoxylem'' groups; (3) quantif iable differences in protoxylem/metaxylem tissue fabric probably relat ed to differences in hormonal activity of lateral appendage primordia during early development; (4) origin of pith at the center of the stel e related to changes in the geometry of the shoot apex under several p ossible models of hormone determination; and (5) dissection of the ste le into discrete primary vascular bundles possibly related to changing receptivity to the hormone signal and the geometric consequences of f low rates in three dimensions over developmentally significant interva ls of time. In each instance, the computer model provides new ways to interpret evolutionary change within and between major groups of vascu lar plants, with specific stelar architectures of these plants offerin g reciprocal illumination for further improvement of the model. Becaus e of the unique nature of their development and excellent fossil recor d, I suggest that vascular plants in many ways seem to be the ideal st udy group for integrating developmental process directly into analysis of homology and estimation of phylogenetic relationship.