Water-conducting Cells Research Articles

Extreme functional specialization of fertile leaves in a widespread fern species and its implications on the evolution of reproductive dimorphism.

Resource allocation theory posits that organisms distribute limited resources across functions to maximize their overall fitness. In plants, the allocation of resources among maintenance, reproduction, and growth influences short-term economics and long-term evolutionary processes, especially during resource scarcity. The evolution of specialized structures to divide labor between reproduction and growth can create a feedback loop where selection can act on individual organs, further increasing specializaton and resource allocation. Ferns exhibit diverse reproductive strategies, including dimorphism, where leaves can either be sterile (only for photosynthesis) or fertile (for spore dispersal). This dimorphism is similar to processes in seed plants (e.g., the production of fertile flowers and sterile leaves), and presents an opportunity to investigate divergent resource allocation between reproductive and vegetative functions in specialized organs. Here, we conducted anatomical and hydraulic analyses on Onoclea sensibilis L., a widespread dimorphic fern species, to reveal significant structural and hydraulic divergences between fertile and sterile leaves. Fertile fronds invest less in hydraulic architecture, with nearly 1.5 times fewer water-conducting cells and a nearly 0.5 times less drought-resistant xylem compared to sterile fronds. This comes at the increased relative investment in structural support, which may help facilitate spore dispersal. These findings suggest that specialization in ferns-in the form of reproductive dimorphism-can enable independent selection pressures on each leaf type, potentially optimizing spore dispersal in fertile fronds and photosynthetic efficiency in sterile fronds. Overall, our study sheds light on the evolutionary implications of functional specialization and highlights the importance of reproductive strategies in shaping plant fitness and evolution.

Taxonomic Implication of Conducting Elements in the Acrocarpous Mosses

Present study deals with the structure and development of conducting elements in the nine orders of acrocarpous mosses. The significance of conducting tissues in mosses in relation to their habitat conditions, growth forms and leaf cell patterns has been discussed. Features of cells in different portions of the stem and the laminal cell patterns and costa are taken into consideration. Although water-conducting cells are unspecialized in mosses, yet the study shows that they seem to play a vital role in the conduction and provide additional criteria for the distinction of taxa. Four categories have been determined as (i) Acrocarpous mosses with a distinct thick-walled conducting strand (6-7 layered) as hydrome which is surrounded by patches of leptoids. Cortex consists of thick walled cells (6-10 layered). Costa has stereidal cells and well developed conducting elements in leaf, example Polytrichum (ii) Acrocarps with thick-walled, narrow, elongated conducting strand (4-5 layered), cells angular in the cortex (6-8 layered). Leaf cells are rectangular, irregular and porous with incrassate walls, example Dicranum (iii) Acrocarps with conducting tissue (2-5 layered) stereidal, thick walled or thin walled varying in the course of development. Leaf cells are mutipapillate, rounded-quadrate, costa is present, examples Hyophila, Philonotis and (iv) Epiphytic pleurocarps with conducting cells rudimentary, thickened, scattered (2-4 layers) and parenchymatous, cortical cells (2-3 layered) thick walled. Leaf cells are small, rounded or linear and papillate, costa may be present or absent, example Leucodon . The study would constitute a formidable task, especially if intraspecific structural variability is considered. It serves a model system in the eco-physiological aspects.

Convergent evolution of water-conducting cells in Marchantia recruited the ZHOUPI gene promoting cell wall reinforcement and programmed cell death

A key adaptation of plants to life on land is the formation of water-conducting cells (WCCs) for efficient long-distance water transport. Based on morphological analyses it is thought that WCCs have evolved independently on multiple occasions. For example, WCCs have been lost in all but a few lineages of bryophytes but, strikingly, within the liverworts a derived group, the complex thalloids, has evolved a novel externalized water-conducting tissue composed of reinforced, hollow cells termed pegged rhizoids. Here, we show that pegged rhizoid differentiation in Marchantia polymorpha is controlled by orthologs of the ZHOUPI and ICE bHLH transcription factors required for endosperm cell death in Arabidopsis seeds. By contrast, pegged rhizoid development was not affected by disruption of MpNAC5, the Marchantia ortholog of the VND genes that control WCC formation in flowering plants. We characterize the rapid, genetically controlled programmed cell death process that pegged rhizoids undergo to terminate cellular differentiation and identify a corresponding upregulation of conserved putative plant cell death effector genes. Lastly, we show that ectopic expression of MpZOU1 increases production of pegged rhizoids and enhances drought tolerance. Our results support that pegged rhizoids evolved independently of other WCCs. We suggest that elements of the genetic control of developmental cell death are conserved throughout land plants and that the ZHOUPI/ICE regulatory module has been independently recruited to promote cell wall modification and programmed cell death in liverwort rhizoids and in the endosperm of flowering plant seed.

Fossil evidence of tylosis formation in Late Devonian plants.

Tyloses are swellings of parenchyma cells into adjacent water-conducting cells that develop in vascular plants as part of heartwood formation or specifically in response to embolism and pathogen infection. Here we document tyloses in Late Devonian (approximately 360 Myr ago) Callixylon wood. This discovery suggests that some of the earliest woody trees were already capable of protecting their vascular system by occluding individual conducting cells.

Deep origin and gradual evolution of transporting tissues: Perspectives from across the land plants.

The evolution of transporting tissues was an important innovation in terrestrial plants that allowed them to adapt to almost all nonaquatic environments. These tissues consist of water-conducting cells and food-conducting cells and bridge plant-soil and plant-air interfaces over long distances. The largest group of land plants, representing about 95% of all known plant species, is associated with morphologically complex transporting tissue in plants with a range of additional traits. Therefore, this entire clade was named tracheophytes, or vascular plants. However, some nonvascular plants possess conductive tissues that closely resemble vascular tissue in their organization, structure, and function. Recent molecular studies also point to a highly conserved toolbox of molecular regulators for transporting tissues. Here, we reflect on the distinguishing features of conductive and vascular tissues and their evolutionary history. Rather than sudden emergence of complex, vascular tissues, plant transporting tissues likely evolved gradually, building on pre-existing developmental mechanisms and genetic components. Improved knowledge of the intimate structure and developmental regulation of transporting tissues across the entire taxonomic breadth of extant plant lineages, combined with more comprehensive documentation of the fossil record of transporting tissues, is required for a full understanding of the evolutionary trajectory of transporting tissues.

Highlighted articles for February 2022

Highlighted articles for February 2022

Mysteries of the bryophyte-tracheophyte transition revealed: enter the eophytes.

This article is a Commentary on Edwards et al. (2022a,b), 233: 1440–1455 and 1456–1465.

Subcellular coordination of plant cell wall synthesis.

Organelles of the plant cell cooperate to synthesize and secrete a strong yet flexible polysaccharide-based extracellular matrix: the cell wall. Cell wall composition varies among plant species, across cell types within a plant, within different regions of a single cell wall, and in response to intrinsic or extrinsic signals. This diversity in cell wall makeup is underpinned by common cellular mechanisms for cell wall production. Cellulose synthase complexes function at the plasma membrane and deposit their product into the cell wall. Matrix polysaccharides are synthesized by a multitude of glycosyltransferases in hundreds of mobile Golgi stacks, and an extensive set of vesicle trafficking proteins govern secretion to the cell wall. In this review, we discuss the different subcellular locations at which cell wall synthesis occurs, review the molecular mechanisms that control cell wall biosynthesis, and examine how these are regulated in response to different perturbations to maintain cell wall homeostasis.

Stomata: the holey grail of plant evolution

Stomata: the holey grail of plant evolution

Involvement of VNS NAC-domain transcription factors in tracheid formation in Pinus taeda.

Vascular plants have two types of water-conducting cells, xylem vessel cells (in angiosperms) and tracheid cells (in ferns and gymnosperms). These cells are commonly characterized by secondary cell wall (SCW) formation and programmed cell death (PCD), which increase the efficiency of water conduction. The differentiation of xylem vessel cells is regulated by a set of NAC (NAM, ATAF1/2 and CUC2) transcription factors, called the VASCULAR-RELATED NAC-DOMAIN (VND) family, in Arabidopsis thaliana Linne. The VNDs regulate the transcriptional induction of genes required for SCW formation and PCD. However, information on the transcriptional regulation of tracheid cell differentiation is still limited. Here, we performed functional analysis of loblolly pine (Pinus taeda Linne) VND homologs (PtaVNS, for VND, NST/SND, SMB-related protein). We identified five PtaVNS genes in the loblolly pine genome, and four of these PtaVNS genes were highly expressed in tissues with tracheid cells, such as shoot apices and developing xylem. Transient overexpression of PtaVNS genes induced xylem vessel cell-like patterning of SCW deposition in tobacco (Nicotiana benthamiana Domin) leaves, and up-regulated the promoter activities of loblolly pine genes homologous to SCW-related MYB transcription factor genes and cellulose synthase genes, as well as to cysteine protease genes for PCD. Collectively, our data indicated that PtaVNS proteins possess transcriptional activity to induce the molecular programs required for tracheid formation, i.e., SCW formation and PCD. Moreover, these findings suggest that the VNS-MYB-based transcriptional network regulating water-conducting cell differentiation in angiosperm and moss plants is conserved in gymnosperms.

Similar hydraulic efficiency and safety across vesselless angiosperms and vessel-bearing species with scalariform perforation plates.

The evolution of xylem vessels from tracheids is put forward as a key innovation that boosted hydraulic conductivity and photosynthetic capacities in angiosperms. Yet, the role of xylem anatomy and interconduit pits in hydraulic performance across vesselless and vessel-bearing angiosperms is incompletely known, and there is a lack of functional comparisons of ultrastructural pits between species with different conduit types. We assessed xylem hydraulic conductivity and vulnerability to drought-induced embolism in 12 rain forest species from New Caledonia, including five vesselless species, and seven vessel-bearing species with scalariform perforation plates. We measured xylem conduit traits, along with ultrastructural features of the interconduit pits, to assess the relationships between conduit traits and hydraulic efficiency and safety. In spite of major differences in conduit diameter, conduit density, and the presence/absence of perforation plates, the species studied showed similar hydraulic conductivity and vulnerability to drought-induced embolism, indicating functional similarity between both types of conduits. Interconduit pit membrane thickness (Tm) was the only measured anatomical feature that showed a relationship to significant vulnerability to embolism. Our results suggest that the incidence of drought in rain forest ecosystems can have similar effects on species bearing water-conducting cells with different morphologies.

The effects of intervessel pit characteristics on xylem hydraulic efficiency and photosynthesis in hemiepiphytic and non-hemiepiphytic Ficus species.

Xylem vulnerability to cavitation and hydraulic efficiency are directly linked to fine-scale bordered pit features in water-conducting cells of vascular plants. However, it is unclear how pit characteristics influence water transport and carbon economy in tropical species. The primary aim of this study was to evaluate functional implications of changes in pit characteristics for water relations and photosynthetic traits in tropical Ficus species with different growth forms (i.e. hemiepiphytic and non-hemiepiphytic) grown under common conditions. Intervessel pit characteristics were measured using scanning electron microscopy in five hemiepiphytic and five non-hemiepiphytic Ficus species to determine whether these traits were related to hydraulics, leaf photosynthesis, stomatal conductance and wood density. Ficus species varied greatly in intervessel pit structure, hydraulic conductivity and leaf physiology, and clear differences were observed between the two growth forms. The area and diameter of pit aperture were negatively correlated with sapwood-specific hydraulic conductivity, mass-based net assimilation rate, stomatal conductance (gs ), intercellular CO2 concentration (Ci ) and the petiole vessel lumen diameters (Dv ), but positively correlated with wood density. Pit morphology was only negatively correlated with sapwood- and leaf-specific hydraulic conductivity and Dv . Pit density was positively correlated with gs , Ci and Dv , but negatively with intrinsic leaf water-use efficiency. Pit and pit aperture shape were not significantly correlated with any of the physiological traits. These findings indicate a significant role of pit characteristics in xylem water transport, carbon assimilation and ecophysiological adaptation of Ficus species in tropical rain forests.

Evolution of phytolith deposition in modern bryophytes, and implications for the fossil record and influence on silica cycle in early land plant evolution.

Anecdotal evidence indicating substantial silica accumulation in tissues of bryophytes suggests that silica (phytolith) deposition evolved early on in embryophytes. To test this hypothesis, we conducted the first survey of phytolith content representing the major liverwort, moss and hornwort clades. We also assessed the diagnostic value of bryophyte phytoliths. Silica extracted from bryophyte material through wet-ashing was described, focusing on abundance, classifying taxa as nonproducers, light producers and higher producers; and phytolith morphotypes. Ancestral state reconstruction of these characters was performed for mosses and liverworts using published phylogenies. Phytoliths are present in multiple subclades within liverworts, mosses and hornworts, but these phyla were not ancestrally high silica-producers. Higher deposition occurs in liverworts and mosses with specialized water-conducting cells. We hypothesize that active, high silica accumulation was not ancestral for embryophytes, but became possible in clades with increased water conductance. Phytoliths of diagnostic structures (e.g. pegged rhizoids) could help track bryophyte clades or water conductance evolution in the fossil record.

Infrared Nanospectroscopy Reveals the Chemical Nature of Pit Membranes in Water-Conducting Cells of the Plant Xylem.

In the xylem of angiosperm plants, microscopic pits through the secondary cell walls connect the water-conducting vessels. Cellulosic meshes originated from primary walls, and middle lamella between adjacent vessels, called the pit membrane, separates one conduit from another. The intricate structure of the nano-sized pores in pit membranes enables the passage of water under negative pressure without hydraulic failure due to obstruction by gas bubbles (i.e. embolism) under normal conditions or mild drought stress. Since the chemical composition of pit membranes affects embolism formation and bubble behavior, we directly measured pit membrane composition in Populus nigra wood. Here, we characterized the chemical composition of cell wall structures by synchrotron infrared nanospectroscopy and atomic force microscopy-infrared nanospectroscopy with high spatial resolution. Characteristic peaks of cellulose, phenolic compounds, and proteins were found in the intervessel pit membranes of P. nigra wood. In addition, the vessel to parenchyma pit membranes and developing cell walls of the vascular cambium showed clear signals of cellulose, proteins, and pectin. We did not find a distinct peak of lignin and other compounds in these structures. Our investigation of the complex chemical composition of intervessel pit membranes furthers our understanding of the flow of water and bubbles between neighboring conduits. The advances presented here pave the way for further label-free studies related to the nanochemistry of plant cell components.

Organs and tissues of Rhynie chert plants.

The Early Devonian Rhynie chert and the nearby Windyfield chert contain the oldest in situ preserved terrestrial ecosystem. Two of the seven species of anatomically preserved land plants had naked axes, one an axis with a more or less regular pattern of short-longitudinal ribs, two species had spiny axes and one species had small leaf-like appendages. All plants mainly consist of parenchymatous tissues. In some species, conducting elements comprise uniformly thickened thick-walled cells resembling hydroids of larger bryophytes, whereas others have real tracheids with annular and/or spiral secondary wall thickenings. True phloem has never been demonstrated but in all species the thick-walled water-conducting cells are encircled by a zone of thin-walled cells without intercellular spaces. The cortex is differentiated into two or three zones and forms the major part of the axes; in one species the cells of the middle cortex are sclerified. Some species have a hypodermis. In all species the epidermis is covered by a well-developed cuticle. Sporangia are known from all species. Sporangia are spindle-shaped, lobed or kidney-shaped and attached terminally or laterally with a short stalk. Gametophytes of four species have been described. Gametophytes are unisexual, isomorphic but much smaller than the sporophytes.This article is part of a discussion meeting issue 'The Rhynie cherts: our earliest terrestrial ecosystem revisited'.

Unique growth strategy in the Earth’s first trees revealed in silicified fossil trunks from China

Cladoxylopsida included the earliest large trees that formed critical components of globally transformative pioneering forest ecosystems in the Mid- and early Late Devonian (ca. 393-372 Ma). Well-known cladoxylopsid fossils include the up to ∼1-m-diameter sandstone casts known as Eospermatopteris from Middle Devonian strata of New York State. Cladoxylopsid trunk structure comprised a more-or-less distinct cylinder of numerous separate cauline xylem strands connected internally with a network of medullary xylem strands and, near the base, externally with downward-growing roots, all embedded within parenchyma. However, the means by which this complex vascular system was able to grow to a large diameter is unknown. We demonstrate-based on exceptional, up to ∼70-cm-diameter silicified fossil trunks with extensive preservation of cellular anatomy from the early Late Devonian (Frasnian, ca. 374 Ma) of Xinjiang, China-that trunk expansion is associated with a cylindrical zone of diffuse secondary growth within ground and cortical parenchyma and with production of a large amount of wood containing both rays and growth increments concentrically around individual xylem strands by normal cambia. The xylem system accommodates expansion by tearing of individual strand interconnections during secondary development. This mode of growth seems indeterminate, capable of producing trees of large size and, despite some unique features, invites comparison with secondary development in some living monocots. Understanding the structure and growth of cladoxylopsids informs analysis of canopy competition within early forests with the potential to drive global processes.

New research perspectives from a novel approach to quantify tracheid wall thickness.

The analysis of xylem cell anatomical features in dated tree rings provides insights into xylem functional responses and past growth conditions at intra-annual resolution. So far, special focus has been given to the lumen of the water-conducting cells, whereas the equally relevant cell wall thickness (CWT) has been less investigated due to methodological limitations. Here we present a novel approach to measure tracheid CWT in high-resolution images of wood cross-sections that is implemented within the specialized image-analysis tool 'ROXAS'. Compared with the traditional manual line measurements along a selection of few radial files, this novel image-analysis tool can: (i) measure CWT of all tracheids in a tree-ring cross-section, thus increasing the number of individual tracheid measurements by a factor of ~10-20; (ii) measure the tangential and radial walls separately; and (iii) laterally integrate the measurements in a customizable way from only the thinnest central part of the cell walls up to the thickest part of the tracheids at the corners. Cell wall thickness measurements performed with our novel approach and the traditional manual approach showed comparable accuracy for several image resolutions, with an optimal accuracy-efficiency balance at 100× magnification. The configurable settings intended to underscore different cell wall properties indeed changed the absolute levels and intra- and inter-annual patterns of CWT. This versatility, together with the high data production capacity, allows to tailor the measurements of CWT to the specific goal of each study, which opens new research perspectives, e.g., for investigating structure-function relationships, tree stress responses and carbon allocation patterns, and for reconstructing climate based on intra- and inter-annual variability of anatomical wood density.

Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation.

One crucial problem that plants faced during their evolution, particularly during the transition to growth on land, was how to transport water, nutrients, metabolites, and small signaling molecules within a large, multicellular body. As a solution to this problem, land plants developed specific tissues for conducting molecules, called water-conducting cells (WCCs) and food-conducting cells (FCCs). The well-developed WCCs and FCCs in extant plants are the tracheary elements and sieve elements, respectively, which are found in vascular plants. Recent molecular genetic studies revealed that transcriptional networks regulate the differentiation of tracheary and sieve elements, and that the networks governing WCC differentiation are largely conserved among land plant species. In this review, we discuss the molecular evolution of plant conducting cells. By focusing on the evolution of the key transcription factors that regulate vascular cell differentiation, the NAC transcription factor VASCULAR-RELATED NAC-DOMAIN for WCCs and the MYB-coiled-coil (CC)-type transcription factor ALTERED PHLOEM DEVELOPMENT for sieve elements, we describe how land plants evolved molecular systems to produce the specialized cells that function as WCCs and FCCs.

Primary Metabolism during Biosynthesis of Secondary Wall Polymers of Protoxylem Vessel Elements.

Xylem vessels, the water-conducting cells in vascular plants, undergo characteristic secondary wall deposition and programmed cell death. These processes are regulated by the VASCULAR-RELATED NAC-DOMAIN (VND) transcription factors. Here, to identify changes in metabolism that occur during protoxylem vessel element differentiation, we subjected tobacco (Nicotiana tabacum) BY-2 suspension culture cells carrying an inducible VND7 system to liquid chromatography-mass spectrometry-based wide-target metabolome analysis and transcriptome analysis. Time-course data for 128 metabolites showed dynamic changes in metabolites related to amino acid biosynthesis. The concentration of glyceraldehyde 3-phosphate, an important intermediate of the glycolysis pathway, immediately decreased in the initial stages of cell differentiation. As cell differentiation progressed, specific amino acids accumulated, including the shikimate-related amino acids and the translocatable nitrogen-rich amino acid arginine. Transcriptome data indicated that cell differentiation involved the active up-regulation of genes encoding the enzymes catalyzing fructose 6-phosphate biosynthesis from glyceraldehyde 3-phosphate, phosphoenolpyruvate biosynthesis from oxaloacetate, and phenylalanine biosynthesis, which includes shikimate pathway enzymes. Concomitantly, active changes in the amount of fructose 6-phosphate and phosphoenolpyruvate were detected during cell differentiation. Taken together, our results show that protoxylem vessel element differentiation is associated with changes in primary metabolism, which could facilitate the production of polysaccharides and lignin monomers and, thus, promote the formation of the secondary cell wall. Also, these metabolic shifts correlate with the active transcriptional regulation of specific enzyme genes. Therefore, our observations indicate that primary metabolism is actively regulated during protoxylem vessel element differentiation to alter the cell's metabolic activity for the biosynthesis of secondary wall polymers.

Response of tree growth and wood structure of Larix kaempferi, Kalopanax septemlobus and Betula platyphylla saplings to elevated CO2 concentration for 5 years exposure in a FACE system

Elevated CO 2 concentration affected biomass partitioning in above-ground biomass, but size and number of water-conducting cells were unchanged in Larix kaempferi, Kalopanax septemlobus and Betula platyphylla. Using a Free-Air CO2 Enrichment (FACE) system, we studied the effect of elevated CO2 on the growth, leaf gas exchange and xylem anatomy of a conifer, Larix kaempferi, and two angiospermous tree species, Kalopanax septemlobus and Betula platyphylla. Two-year-old seedlings were grown at control sites (ambient; 370 ppm) and FACE sites (elevated; 500 ppm) for 5 years. We measured the lumen area and number of water-conducting cells, as well as biomass and leaf gas exchange, and visualized the functional region of water transport using a dye injection experiment. Elevated CO2 did not induce any significant changes in growth or in leaf gas exchange or lumen area of earlywood tracheids in L. kaempferi relative to ambient CO2. In two other tree species, elevated CO2 was found to enhance tree height and total leaf area (LA), with no change in stomatal conductance. In K. septemlobus, there were no changes in lumen area or number of earlywood vessels, or in the functional region of water transport. B. platyphylla also underwent no changes in lumen area or number of vessels, although there was a yearly variation in the size of the vessels. Our results show that 5 years of CO2 exposure did not notably affect the anatomical features of water-conducting cells. This finding suggests that, under elevated CO2, trees respond to changes in water balance due to changes in LA by extending the hydraulically active area of xylem.