Vascular architecture in shoots of early divergent vascular plants, Lycopodium clavatum and Lycopodium annotinum

Abstract

Summary• Lycopodium represents a phylogenetically distinct clade of basal vascular plants with anatomical characters that have no parallel in other lineages. Thus, knowledge of lycopod structure and development may reveal important information about the common ancestors of all vascular plants. Here we report the unique architecture of the conducting system in Lycopodium annotinum and Lycopodium clavatum .• Based on multiple series of anatomical sections, we reconstructed spatial relationships between microphylls and the stelar system.• Analysis revealed that protoxylem ribs (PXR) were vertical, regardless of type of phyllotaxis, and their numbers were variable. Microphyll traces (MTr) were randomly distributed between ribs, resulting in the absence of defined sympodia and varied lengths of MTr. Dichotomous branching contributed to additional features, for example occurrence of mesarch protoxylem, affecting stele structure and PXR numbers.• Our data showed limited interrelationships between lycopod vasculature and microphyll phyllotaxis. This may suggest that both systems developed independently, then evolved together to form the integrated supply system. Thus vasculature in extant lycophytes may be less functionally efficient than in seed plants, where consistent leaf-trace lengths guarantee predictable energy utilization during ontogeny. Differences may result from the phylogenetically different origin of microphylls, and the level of vascular complexity.

The Stele - A Developmental Perspective on the Diversity and Evolution of Primary Vascular Architecture

“…This is consistent with evidence for independent evolution of leaves in ferns and seed plants (Tomescu 2009), whose stelar architectures illustrate peripheral and radial concentration, respectively (see Sections 8.2.2 and 8.2.3 below). In contrast to these euphyllophyte lineages, leaves seem to have little influence on auxin distribution and the structure of the protostele of lycophytes Gola et al 2007), consistent with their independent evolution in this lineage. These observations point to the importance of the relationships between lateral appendages, with their influence on concentrations of auxin and other putative morphogens in the shoot apical meristem, and stelar architecture.…”

Diversity of phyllotaxis in land plants in reference to the shoot apical meristem structure

“…As a consequence, phyllotaxis is established de novo at the SAM, at every change of the type of initiated organs (scales vs. leaves) [63]. Similarly, the relationship between microphylls and the internal (stelar) vascular system is relatively unstable in lycopods, which display a high diversity of phyllotactic patterns and possibly independence of the SAM in pattern formation [133]. Moreover, extremely diversified phyllotactic arrangements in the carpels of Michelia fuscata may be related to the instability and flexibility of vascular system structure during carpel initiation [88].…”

What can lycophytes teach us about plant evolution and development? Modern perspectives on an ancient lineage

“…In extinct and extant tracheophytes, the arrangement of the xylem tissue within the stem can be diverse. Lycophytes are typically protostelic (Gola, Jernstedt, & Zagórska‐Marek, 2007), having a core of xylem surrounded by phloem and an endodermis, and tissues can be arranged in a lobed central xylem pole (actinostele), numerous xylem poles (plectostele) or a combination of these arrangements (actino‐plectostelic, e.g. Lycopodium clavatum and Lycopodium annotinum ; Figure 3; Gola et al, 2007).…”

“…(b) Phylogeny showing relationships between extant (in bold; Euphyllophytes, Lycopodiales, Selaginellales, and Isoëtales) and extinct (†; Partitatheca, Aglaophyton, Rhynia, Horneophyton , Zosterophyllopsida, Drepanophycales, Protolepidodendrales, and Lepidodendrales) land plant clades (Cascales‐Miñana et al, 2019; Gensel & Berry, 2001; Schuettpelz et al, 2016). The last shared common ancestor of vascular plants had branching sporophytes (1; Boyce, 2008; Edwards & Kenrick, 2015), and fossils show a stepwise acquisition of higher order branching (2; Kenrick & Crane, 1997), specialised vascular cells (3; Cascales‐Miñana et al, 2019), annular and/or spiral xylem tracheid thickening (4; Cascales‐Miñana et al, 2019), shoot meristem indeterminacy (5; Harrison, 2017b), sporangia on short lateral branches (6; Gensel & Berry, 2001), vegetative leaves with a single vascular trace (7; Gifford & Foster, 1989; Gola et al, 2007), and sporangia with a subtending leaf (sporophyll) (8; Sporne, 1962). Lycopodiales and Protolepidodendrales have/had spores that are all the same size (homospory) and no ligule at the base of the growing leaf.…”