Xylem of early angiosperms: Nuphar (Nymphaeaceae) has novel tracheid microstructure¹

Abstract

SEM studies of xylem of stems of Nuphar reveal a novel feature, not previously reported for any angiosperm. Pit membranes of tracheid end walls are composed of coarse fibrils, densest on the distal (outside surface, facing the pit of an adjacent cell) surface of the pit membrane of a tracheid, thinner, and disposed at various levels on the lumen side of a pit membrane. The fibrils tend to be randomly oriented on the distal face of the pit membrane; the innermost fibrils facing the lumen take the form of longitudinally oriented strands. Where most abundantly present, the fibrils tend to be disposed in a spongiform, three-dimensional pattern. Pores that interconnect tracheids are present within the fibrillar meshwork. Pit membranes on lateral walls of stem tracheids bear variously diminished versions of this pattern. Pits of root tracheids are unlike those of stems in that the lumen side of pit membranes bears a reticulum revealed on the outer surface of the tracheid after most of the thickness of a pit membrane is shaved away by the sectioning process. No fibrillar texturing is visible on the root tracheid pits when they are viewed from the inside of a tracheid. Tracheid end walls of roots do contain pores of various sizes in pit membranes. These root and stem patterns were seen in six species representing the two sections of Nuphar, plus one intersectional hybrid, as well as in one collection of Nymphaea, included for purposes of comparison. Differences between root and stem tracheids with respect to microstructure are consistent in all species studied. Microstructural patterns reported here for stem tracheid pits of Nymphaeaceae are not like those of Chloranthaceae, Illiciaceae, or other basal angiosperms. They are not referable to any of the patterns reported for early vascular plants. The adaptational nature of the pit membrane structure in these tracheids is not apparent; microstructure of pit membranes in basal angiosperms is more diverse than thought prior to study with SEM.

Do tracheid microstructure and the presence of minute crystals link Nymphaeaceae, Cabombaceae and Hydatellaceae?

“…We have demonstrated the occurrence of a peculiar microstructure in stem tracheid end walls of all genera of Nymphaeaceae (Carlquist & Schneider, 2009; Carlquist et al. , 2009; Schneider & Carlquist, in press; Schneider et al.…”

“…(Carlquist & Schneider, 2009); Nuphar Sm. (Carlquist, Schneider & Hellquist, 2009); Barclaya Wall. (Schneider & Carlquist, in press); and Nymphaea L., including Ondinea Hartog, (Schneider, Carlquist & Hellquist, in press).…”

Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications

“…All Nymphaeaceae could easily be considered to be vesselless. They could just as easily be considered to have tracheids in stems but tracheids somewhat transitional to vessel elements in roots (Carlquist & Schneider, 2009; Carlquist, Schneider & Hellquist, 2009; Schneider, Carlquist & Hellquist, 2009).…”

Origins and nature of vessels in Monocotyledons. 14. Vessellessness in Orontioideae (Araceae): adaptation or relictualism?

“…Acoraceae, the family that is sister to the remainder of the monocots, have what must be called tracheids in roots as well as stems (Carlquist and Schneider , Carlquist ). This, like similar conditions in Nymphaeales (Carlquist and Schneider , , Carlquist et al , Schneider and Carlquist , Schneider et al ), can be considered retention of a primitively vesselless condition that seems to have been shared by primitive angiosperms, judging from recent phylogenies (Soltis et al ). However, secondary vessellessness in roots of monocotyledons is conceivable in the case of submersed aquatics such as submersed Alismatales (Carlquist ).…”

“…Fibrillar meshwork‐like texture is characteristic of pit membranes in end walls of tracheids in stems, but not roots, in the Orontioideae. These characteristics are somewhat reminiscent of the end wall pit membranes in tracheids of Nymphaeaceae and Cabombaceae (Carlquist and Schneider , , Carlquist et al , Schneider and Carlquist , Schneider et al ). However, the stem tracheid pit membranes in Nymphaeaceae and Cabombaceae are much more three‐dimensional, and feature strands and layers superimposed over the pit membrane and some parts of the secondary walls.…”