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

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.

Section: Evolution Of the Pith -Siphonosteles And Eustelesmentioning

confidence: 99%

Section: Radial Concentration and Eustelesmentioning

confidence: 99%

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

2020

Preprint

“…In all the cases discussed above, the development of a central parenchymatous area of the stele is associated with an increase in axis diameter. This, as well as the evolution of specialized lateral appendages (leaves), are thought to have imposed physiological constraints – underpinned by efficiency of water and photosynthate transfer and by economy in the production of energy‐demanding specialized conducting tissues – that drove the evolution of siphonosteles and eusteles (reviewed by Decombeix, Boura & Tomescu, 2019). Below, I propose a model informed by current understanding of developmental regulation and incorporating axis size variation, to provide a unifying explanation for the nature of the stele and its evolution that is consistent with both the procambial and the boundary layer views of the stele discussed above.…”

Section: Evolutionary Considerationsmentioning

confidence: 99%

“…The seed plant eustele, the dissected stele of some cladoxylopsids (referred to as a eustele by some; Decombeix et al ., 2019), and the stele with discrete vascular bundles present in many sphenopsids, may have arisen along a path similar to that seen in archaeopterids – combining radial concentration and peripheral concentration – as implied by transformational series and evolutionary scenarios based on fossils (Stewart & Rothwell, 1993). However, in contrast to the archaeopterid pathway, the scenarios proposed for seed plants (Namboodiri & Beck, 1968; Beck, 1970) and cladoxylopsids involve initial fragmentation (dissection) of the actinostele – corresponding to more severe radial concentration – followed by development of a central parenchymatous area due to subsequent peripheral concentration (h, k and l in Fig.…”

Section: A Unifying Perspective On Stelar Architecture: the Dual Stele Modelmentioning

confidence: 99%

The stele – a developmental perspective on the diversity and evolution of primary vascular architecture

2021

Biological Reviews

The stele concept is one of the oldest enduring concepts in plant biology. Here, I review the history of the concept and build an argument for an updated view of steles and their evolution. Studies of stelar organization have generated a widely ranging array of definitions that determine the way we classify steles and construct scenarios about the evolution of stelar architecture. Because at the organismal level biological evolution proceeds by changes in development, concepts of structure need to be grounded in development to be relevant in an evolutionary perspective. For the stele, most 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). Consensus between these two perspectives can be reached by recasting the stele as a structural entity of dual nature. Following a brief review of the history of the stele concept, basic terminology related to stelar organization, and traditional classifications of the steles, I revisit boundary layers from the perspective of histogenesis as a dynamic mosaic of developmental domains. I review anatomical and molecular data to explore and reaffirm the importance of boundary layers for stelar organization. Drawing on information from comparative anatomy, developmental regulation, and the fossil record, I propose a stele concept that integrates both the boundary layer and the procambial perspectives, consistent with a dual nature of the stele. This dual stele model posits that stelar architecture is determined at 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 working hypotheses that incorporate assumptions and generate implications that can be tested empirically. The model also offers criteria for an updated classification of steles 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 of 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...

“…Today, secondary growth is present in the two major tracheophyte clades: in euphyllophytes (seed plants) and lycophytes (isoetaleans; Decombeix et al . 2019). In contrast to the extant flora, the fossil record shows a high diversity of lineages with secondary vascular tissue, which is recorded in both of the major tracheophyte clades by the Carboniferous ( c .…”

mentioning

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

Self Cite

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.