Structurally complex, yet anatomically plesiomorphic: permineralized plants from the Emsian of Gaspé (Quebec, Canada) expand the diversity of Early Devonian euphyllophytes

2019

IAWA J.

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Studies of anatomically preserved fossils provide a wealth of information on the evolution of plant vascular systems through time, from the oldest evidence of vascular plants more than 400 million years ago to the rise of the modern angiosperm-dominated flora. In reviewing the key contributions of the fossil record, we discuss knowledge gaps and major outstanding questions about the processes attending the evolution of vascular systems. The appearance and diversification of early vascular plants in the late Silurian-Devonian was accompanied by the evolution of different types of tracheids, which initially improved the hydraulics of conduction but had less of an effect on mechanical support. This was followed in the Devonian and Carboniferous by an increase in complexity of the organization of primary vascular tissues, with different types of steles evolving in response to mechanical, hydraulic, and developmental regulatory constraints. Concurrently, secondary vascular tissues, such as wood, produced by unifacial or bifacial cambia are documented in a wide array of plant groups, including some that do not undergo secondary growth today. While wood production has traditionally been thought to have evolved independently in different lineages, accumulating evidence suggests that this taxonomic breadth reflects mosaic deployment of basic developmental mechanisms, some of which are derived by common ancestry. For most of vascular plant history, wood contained a single type of conducting element: tracheids (homoxyly). However, quantitative (e.g. diameter and length) and qualitative (e.g. pitting type) diversity of these tracheids allowed various taxa to cover a broad range of hydraulic properties. A second type of conducting elements, vessels, is first documented in an extinct late Permian (c. 260 Ma) group. While the putative hydraulic advantages of vessels are still debated, wood characterized by presence of vessels (heteroxyly) would become the dominant type, following the diversification of angiosperms during the Cretaceous.

Section: The First Vascular Plantsmentioning

confidence: 98%

Plant hydraulic architecture through time: lessons and questions on the evolution of vascular systems

Decombeix

Boura

2019

IAWA J.

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“…7h). Records of Early Devonian plants with a ribbed column of central xylem (Gensel 1984;Remy & Hass 1986;Bickner & Tomescu 2019) place the origin of actinosteles as far back in time as 400 million years. Higher in the stratigraphic column, actinosteles are present in multiple lineages: cladoxylopsids (iridopterids and some pseudosporochnaleans), stenokolealeans, progymnosperms (aneurophytes and archaeopterids), and early seed plants.…”

Section: Radial Concentration and Eustelesmentioning

confidence: 99%

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

2020

Preprint

The stele concept is one of the oldest enduring concepts in plant biology. This paper reviews the concept and its foundations, and builds an argument for an updated view of steles and their evolution. The history of studies of stelar organization has generated a widely ranging array of definitions of the stele that determine the way we classify steles and construct scenarios about the evolution of stelar architecture. Because at the level of the organism biological evolution proceeds by, and is reflected in, changes in development, concepts of structure need to be grounded in development in order to be relevant in an evolutionary perspective. For the stele, most of the traditional definitions that incorporate development have viewed it as the totality of tissues that either originate from procambium – currently the prevailing view – or are bordered by a boundary layer (e.g., endodermis). A definition of the stele that would bring consensus between these perspectives recasts the stele as a structural entity of dual nature. Here, I review briefly the history of the stele concept, basic terminology related to stelar organization, and traditional classifications of the steles. I then revisit boundary layers from the perspective of histogenesis as a dynamic mosaic of developmental domains. I use classic and recent anatomical and molecular data to reaffirm and explore the importance of boundary layers for stelar organization. Drawing on data from comparative anatomy, developmental regulation, and the fossil record, I offer a model for a stele concept that integrates both the boundary layer and the procambial perspective, consistent with a dual nature of the stele. The dual stele model posits that stelar architecture is determined in the apical meristem by two major cell fate specification events: a first one that specifies a provascular domain and its boundaries, and a second event that specifies a procambial domain (which will mature into conducting tissues) from cell subpopulations of the provascular domain. If the position and extent of the developmental domains defined by the two events are determined by different concentrations of the same morphogen (most likely auxin), then the distribution of this organizer factor in the shoot apical meristem, as modulated by changes in axis size and the effect of lateral organs, can explain the different stelar configurations documented among tracheophytes. This model provides a set of working hypotheses that incorporate assumptions and generate implications that can be tested empirically. The model also offers criteria for an updated classification of steles that is in line with current understanding of plant development. In this classification, steles fall into two major categories determined by the configuration of boundary layers – boundary protosteles and boundary siphonosteles, each with subtypes defined by the architecture of the vascular tissues. Validation the dual stele model and, more generally, in-depth understanding of the regulation of stelar architecture, will necessitate targeted efforts in two areas: (i) the regulation of procambium, vascular tissue, and boundary layer specification in all extant vascular plants, considering that most of the diversity in stelar architecture is hosted by seed-free plants, which are the least explored in terms of developmental regulation; (ii) the configuration of vascular tissues and, especially, boundary layers, in as many extinct species and lineages as possible.

“…Aside from Gmujij tetraxylopteroides , other Early Devonian plants with lobed primary xylem include Gothanophyton zimmermanni (Remy & Hass 1986), Leptocentroxyla tetrarcha (Bickner & Tomescu 2019), an unnamed euphyllophyte described by (Gensel 1984) from the Battery Point Formation, and another plant described from the same unit by Toledo (2018); see also Kenrick & Crane (1997, fig. 4.24.a).…”

Section: Discussionmentioning

confidence: 99%

“…To further complicate matters, many Early Devonian plants, including Gmujij , possess P‐type tracheid thickening, which is considered plesiomorphic in euphyllophytes. Despite the fact that these plants have clear anatomical similarities to younger Devonian euphyllophytes, their P‐type thickening separates them from those younger groups, precluding conclusive taxonomic placement (Bickner & Tomescu 2019). Currently, it is not known whether the evolutionary transition from P‐type thickening to tracheids with bordered pits involved simple or complex changes in the regulatory mechanisms for secondary wall patterning.…”

Section: Discussionmentioning

confidence: 99%

An Early Devonian actinostelic euphyllophyte with secondary growth from the Emsian of Gaspé (Canada) and the importance of tracheid wall thickening patterns in early euphyllophyte systematics

Pfeiler

Papers in Palaeontology

2020

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Secondary growth is a tracheophyte structural feature whose earliest known occurrence dates to the late Pragianearly Emsian. Armoricaphyton, Franhueberia and an unnamed plant from eastern Canada represent the only instances of secondary growth documented to date for the Early Devonian. Here, we describe a new Early Devonian euphyllophyte exhibiting secondary growth, from the Emsian (c. 400-395 Ma) Battery Point Formation (Qu ebec, Canada): Gmujij tetraxylopteroides gen. et sp. nov., which is characterized by a mesarch actinostele with Psilophyton-type (P-type) tracheid wall thickening, and which exhibits a new type of anatomical organization in Early Devonian wood-producing euphyllophytes. Gmujij differs from coeval euphyllophytes, but lack of data on branching patterns, reproductive structures and other traditional diagnostic features precludes classification in previously recognized euphyllophyte groups. We experiment with a numerical approach to tracheid size distributions, to compare Gmujij with younger euphyllophytes exhibiting secondary growth. Comparisons indicate similarity between Gmujij and aneurophytalean progymnosperms, such as Tetraxylopteris. However, its plesiomorphic P-type tracheids set Gmujij apart from younger actinostelic euphyllophytes, questioning the importance of tracheid thickening patterns as diagnostic characters separating major lineages. Answers to this question hinge on whether transitions between wall thickening patterns require simple or complex changes in developmental regulation, a matter that requires improved understanding of regulatory programs that determine tracheid thickening patterns. Irrespective of these, Gmujij adds a new component to the diversity of anatomically preserved plants known in the Early Devonian, an incompletely explored interval of tracheophyte anatomical diversification, contributing information that will facilitate understanding of the evolutionary origins of secondary growth.