Growth, development, and systematics of ferns: Does Botrychium s.l. (Ophioglossales) really produce secondary xylem?¹

Abstract

Developmental morphology and anatomy of Botrychium s.l. were studied to clarify rhizome ontogeny and patterns of tissue maturation that can be used to test the hypothesis that ferns of the Ophioglossales may represent living progymnosperms. Serial anatomical sections of the rhizomes of B. virginianum and B. dissectum reveal that apical meristematic activity and vascular tissue maturation occur over an extended period of several years and then stop. Most of the xylem consists of radial rows of tracheids and interspersed ray-like xylem parenchyma cells that are similar in these respects to secondary xylem, but pits occur on all tracheid walls as is characteristic of primary xylem. No vascular cambium is initiated in mature primary tissues, nor is there secondary phloem. Radial rows of xylem cells are produced by the direct continuation of divisions that begin at the shoot apical meristem, forming a cylinder of radially aligned procambial cells before the differentiation of protoxylem. Continuing divisions over a period of several years increase the number of thin-walled cells and tracheids in each radial row back to about one internode behind where the current year's frond trace diverges from the rhizome stele. At more proximal levels of the rhizome, procambial cell divisions cease and there is no additional tracheid differentiation. These data reveal that the rhizome matures over an exceedingly long period of several years, but that growth is ultimately determinate, thus supporting hypotheses that the Ophioglossales is more closely related to other groups of living ferns than to progymnosperms and seed plants.

Evolution of development of vascular cambia and secondary growth

“…Lycopodium and Equisetum ) lack secondary growth entirely. Similarly, although no modern ferns produce secondary growth (but see Rothwell & Karrfalt, 2008), evidence of a vascular cambium has been found in several extinct pre‐fern lineages, most notably in Rhacophyton (Cichan & Taylor, 1990; Taylor et al. , 2009).…”

“…, 2004; Judd et al. , 2008; Rothwell & Karrfalt, 2008), implying that this origin of secondary growth predates the seed. The earliest extant angiosperms share both a bifacial cambium and tracheid‐based wood structure with the gymnosperms.…”

“…The cambium of Sphenophyllales was bifacial and produced both secondary xylem and phloem, suggesting an origin distinct from the Calamitales (although note that relationships among these groups are not clear). The bifacial cambium of extant seed plants is thought to be homologous with that of the spore-bearing progymnosperms (Friedman et al, 2004;Judd et al, 2008;Rothwell & Karrfalt, 2008), implying that this origin of secondary growth predates the seed. The earliest extant angiosperms share both a bifacial cambium and tracheid-based wood structure with the gymnosperms.…”

The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage

“…In angiosperms, a combination of thin pit membranes and a large pit membrane area increases species' vulnerability to cavitation (Christman et al, 2009; Lens et al, 2011), so given the resemblance in pit membrane structure between angiosperms and ferns, we suspect that the mechanism of cavitation resistance operates under similar constraints in ferns. Interestingly, members of the basal fern genus Botrychium exhibit torus-margo pit membranes and developmental patterns that superficially resemble those of conifers (Figure 1E), but the functional significance of these traits is unknown (Morrow and Dute, 1998; Rothwell and Karrfalt, 2008). …”

The Structure and Function of Xylem in Seed-Free Vascular Plants: An Evolutionary Perspective

“…Similar pit membrane arrangements have been observed in seed-free vascular plants since the Early Devonian (Kenrick and Crane 1997 ;Taylor et al 2009 ). Interestingly, torus-margo pit membranes are present in ferns, but only in the anomalous secondary growth in rhizomes in the genus Botrychium (Ophioglossaceae; Morrow and Dute 1998 ;Rothwell and Karrfalt 2008 ). The presence of conifer-like pit membranes in Botrychium as well as bordered pits in Psilotum indicates that ferns have the genetic potential to evolve xylem that is functionally comparable to higher plants, but either selection acted on attributes of fern physiology or life history that override the importance of pit membranes, or the genetic or developmental capacity to capitalize on these traits is absent.…”