Tracheid Structure in a Primitive Extant Plant Provides an Evolutionary Link to Earliest Fossil Tracheids

Abstract

Most attempts to understand the early evolution of tracheids have centered on fossil Silurian and Devonian vascular plants, and these efforts have led to a wealth of new information on early water-conducting cells. All of these early tracheids appear to possess secondary cell wall thickenings composed of two distinct layers: a layer adjacent to the primary cell wall that is prone to degradation (presumably during the process of fossilization) and a degradation-resistant (possibly lignified) layer next to the cell lumen. Developmental studies of secondary wall formation in tracheary elements of extant vascular plants have been confined to highly derived seed plants, and it is evident that the basic structure of these secondary cell wall thickenings does not correspond well to those of tracheids of the Late Silurian and Early Devonian. Significantly, secondary cell wall thickenings of tracheary elements of seed plants are not known to display the coupled degradation-prone and degradation-resistant layers characteristic of tracheids in early tracheophytes. We report a previously unknown pattern of cell wall formation in the tracheids of a living plant. We show that in Huperzia, one of the most primitive extant vascular plants, secondary cell wall deposition in tracheids includes a first-formed layer of wall material that is degradation-prone ("template layer") and a later-formed degradation-resistant layer ("resistant layer"). These layers match precisely the pattern of wall thickenings in the tracheids of early fossil vascular plants and provide an evolutionary link between tracheids of living vascular plants and those of their earliest fossil ancestors. Moreover, our developmental data provide the essential information for an explicit model of the early evolution of tracheid secondary wall thickenings. Finally, congruence of tracheid structure in extant Huperzia and Late Silurian and Early Devonian vascular plants supports the hypothesis of a single origin of tracheids in land plants.