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

Int. J. Plant Sci. 159(6):881–890. 1998. ᭧ 1998 by The University of Chicago. All rights reserved. 1058-5893/98/5906-0001$03.00 TRACHEID STRUCTURE IN A PRIMITIVE EXTANT PLANT PROVIDES AN EVOLUTIONARY LINK TO EARLIEST FOSSIL TRACHEIDS Martha E. Cook and William E. Friedman1 Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, Colorado 80309, U.S.A. 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. Introduction Edwards 1993). Recent phylogenetic analyses indicate that tracheid-bearing plants (tracheophytes) are monophyletic (Ken- The early evolution of vascular plants (tracheophytes) in the rick and Crane 1991, 1997a) and that diversification among Silurian constitutes the first major diversification of photosyn- early tracheophytes produced three major clades (Banks 1975; thetic life on land (Kenrick and Crane 1997a, 1997b). While Kenrick and Crane 1991, 1997a; fig. 1). The earliest members there is evidence for the establishment of terrestrial plant life of each clade are characterized by a distinctive tracheid type by the end of the Ordovician (Gray et al. 1982; Gray 1993), (Kenrick and Crane 1991, 1997a). the fossil record indicates that land plants remained extremely Rhyniopsida is hypothesized to be an early divergent mon- small and structurally simple until the Late Silurian (Knoll and ophyletic clade (or possibly paraphyletic grade) of primitive Rothwell 1981; Gensel and Andrews 1987; Knoll and Niklas vascular plants that is sister to a monophyletic eutracheophyte 1987; Kenrick and Crane 1997a, 1997b). Among the events clade that includes all extant vascular plants as well as many thought to have been associated with the first burst of struc- of their extinct relatives (Kenrick and Crane 1991, 1997a, and tural diversification among land plants is the evolution of tra- references therein). Members of the Rhyniopsida (all extinct) cheids, complex water-conducting cells defined by the presence are characterized by the presence of S-type tracheids, named of lignified cell wall thickenings (Knoll and Rothwell 1981; after the genus Sennicaulis. S-type tracheids have annular or Gensel and Andrews 1987; Knoll and Niklas 1987). helical thickenings and lateral walls that appear to be made Most attempts to understand the early evolution of tracheids of a spongy or reticulate material that may be partially deg- have centered on fossilized Silurian and Devonian vascular radation-resistant in the fossil record (fig. 2). A very thin deg- plants, and these efforts have led to a wealth of new infor- radation-resistant layer of secondary cell wall material with mation on early water-conducting cells (Grierson 1976; Zdeb- micropores appears to overlie the entire spongy layer of wall ska 1982; Kenrick and Edwards 1988; Li 1990; Kenrick and material (Kenrick and Crane 1991; Kenrick et al. 1991). Crane 1991, 1997a; Kenrick et al. 1991; Edwards et al. 1992; The eutracheophyte clade is recognized by the presence of tracheids with a relatively thicker degradation-resistant layer 1 Author for correspondence and reprints; E-mail ned@ of secondary cell wall (Kenrick and Crane 1991, 1997a). Al- colorado.edu. though much work remains to be done on the more precise Manuscript received March 1998; revised manuscript received April 1998. relationships of basal members of the eutracheophyte clade, 881 This content downloaded from 128.103.149.052 on April 12, 2016 13:08:45 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 882 INTERNATIONAL JOURNAL OF PLANT SCIENCES similar to G-type tracheids in possessing secondary cell wall thickenings that appear hollow (fig. 2). Although certain aspects of cell wall patterning differ among Late Silurian and Early Devonian S-, G-, and P-type tracheids, all of these early water-conducting cells possess cell wall thickenings composed of two distinct layers: a degradation-prone layer adjacent to the primary cell wall and a degradation- resistant (possibly lignified) layer next to the cell lumen (fig. 2; Kenrick and Edwards 1988; Kenrick and Crane 1991; Ken- rick et al. 1991; Edwards 1993). Developmental studies of cell wall structure in tracheary elements of extant vascular plants have been confined to highly derived seed plants (Esau et al. 1963, 1966a, 1966b; Wooding and Northcote 1964; Cron- shaw and Bouck 1965; O’Brien and Thimann 1967; Hepler et al. 1970; Esau 1978; Daniel and Nilsson 1984; Uehara and Hogetsu 1993; Fineran 1997), and it is evident that basic fea- tures of cell wall structure in tracheary elements of seed plants do not correspond well to those of S-, G-, and P-type tracheids of the Late Silurian and Early Devonian. Electron micrographs of tracheary elements in conifers and angiosperms depict cell wall thickenings with a three-layered secondary cell wall (S1, S2, and S3 layers), and these layers of secondary wall are all heavily lignified, differing mostly in the orientation (angle) of Fig. 1 Hypothesis of phylogenetic relationships among the three microfibril deposition (Boudet et al. 1995). Thus, tracheary major vascular plant lineages (Kenrick and Crane 1997a). Rhyniopsida elements of extant seed plants do not exhibit the prominent is sister to the eutracheophytes. Lycophytina, including the extant ly- copsids, is the sister group to Euphyllophytina, which includes all other degradation-prone (possibly unlignified) layer of cell wall ma- extant vascular plants. Huperzia is a basal extant member of the terial that is characteristic of tracheids in early tracheophytes. Lycophytina. A connection between the hollow wall thickenings of early fossil tracheids and a possibly unlignified core in the secondary wall thickenings of basal extant vascular plants (Bierhorst two main lineages have been recognized: the Lycophytina (ly- 1958, 1960) has previously been suggested by several paleo- copsids and their extinct ancestors or close relatives, the zos- botanists (Brauer 1980; Taylor 1986; Kenrick and Edwards terophylls; Niklas and Banks 1990; Gensel 1992), whose ear- 1988; Kenrick and Crane 1991, 1997a; Kenrick et al. 1991). liest members have G-type tracheids, and the Euphyllophytina On the basis of a series of light microscope level studies of (the extinct trimerophytes, ferns, sphenopsids, psilophytes, mature tracheids, Bierhorst (1958, 1960) reported an “unlig- progymnosperms, and seed plants), whose earliest (trimero- nified or very faintly lignified” core in the interior of annular phyte) members have P-type tracheids (Kenrick and Crane or helical thickenings in Lycopodium and other basal extant vascular plants (Equisetum and Osmunda). Bierhorst (1958, 1997a). 1960) was uncertain as to whether these putatively unlignified G-type tracheids, named after the zosterophyll genus Gos- or faintly lignified wall layers consisted of primary or second- slingia, have annular or helical wall thickenings that exhibit ary walls. No photomicrographs of the reported unlignified two layers: a carbonaceous dark layer closest to the cell lumen core in the tracheid walls of primitive vascular plants were and a light layer that appears to represent a mineralized hollow published (Bierhorst 1958, 1960), so it is impossible to eval- core of each thickening (fig. 2; Kenrick and Edwards 1988; uate the specific nature of these observations. Studies of tra- Kenrick and Crane 1991; Kenrick et al. 1991). Between the cheid wall development among seedless vascular plants have spiral thickenings is a degradation-resistant layer of wall ma- not been undertaken in modern times. terial with irregularly shaped holes

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