Intercellular Gas Spaces Research Articles

Stomatal evolution and plant adaptation to future climate.

Global climate change is affecting plant photosynthesis and transpiration processes, as well as increasing weather extremes impacting socio-political and environmental events and decisions for decades to come. One major research challenge in plant biology and ecology is the interaction of photosynthesis with the environment. Stomata control plant gas exchange and their evolution was a crucial innovation that facilitated the earliest land plants to colonize terrestrial environments. Stomata couple homoiohydry, together with cuticles, intercellular gas space, with the endohydric water-conducting system, enabling plants to adapt and diversify across the planet. Plants control stomatal movement in response to environmental change through regulating guard cell turgor mediated by membrane transporters and signaling transduction. However, the origin, evolution, and active control of stomata remain controversial topics. We first review stomatal evolution and diversity, providing fossil and phylogenetic evidence of their origins. We summarize functional evolution of guard cell membrane transporters in the context of climate changes and environmental stresses. Our analyses show that the core signaling elements of stomatal movement are more ancient than stomata, while genes involved in stomatal development co-evolved de novo with the earliest stomata. These results suggest that novel stomatal development-specific genes were acquired during plant evolution, whereas genes regulating stomatal movement, especially cell signaling pathways, were inherited ancestrally and co-opted by dynamic functional differentiation. These two processes reflect the different adaptation strategies during land plant evolution.

Carbon supply–consumption balance in plant roots: effects of carbon use efficiency and root anatomical plasticity

The growth and maintenance of the plant root system may consume more than 50% of all photosynthates, making the root system a major carbon sink (Lambers et al., 2002). Carbon is supplied to roots via sieve tubes that are located in the phloem of the root stele, and is consumed for anabolic and catabolic processes. In a recent paper, Kong et al., (2021) proposed a framework to assess the carbon supply-consumption balance in plant roots that bridges root anatomical structures and root functioning using 'structural allometric relationships'. Their framework highlights the pivotal role of root radius and associated anatomical properties such as sieve tube radius and the size and number of root cells for the carbon supply-consumption balance.

Fusoid cells in the grass family Poaceae (Poales): a developmental study reveals homologies and suggests new insights into their functional role in young leaves.

In mature grass leaf blades as seen in cross-section, oblong cell-like structures have been interpreted most recently as intercellular gas spaces delimited by successive collapsed fusoid cells. These cells have been reported in at least seven of 12 subfamilies of Poaceae and are considered a synapomorphy for the family; however, no developmental work has been performed to verify their meristematic origin or to assess possible homologies within the graminid clade (= Flagellariaceae + [(Joinvilleaceae + Ecdeiocoleaceae) + Poaceae]) or among subfamilies of Poaceae. A developmental study was therefore carried out, including 20 species in three families (Flagellariaceae, Joinvilleaceae and Poaceae), representing the earlier-diverging and derived branches within the graminid clade and Poaceae. Light microscopy was combined with scanning electron microscopy, cryoscanning electron microscopy and transmission electron microscopy to study the development of leaves taken from the shoot apex of young plants. Mature leaf blades also were taken from living or dried plants and the mid-portion was studied. Developmental results show that, in mature leaf blades as seen in cross-section, one apparent fusoid cell is typically a cavity resulting from the collapse of the initial fusoid cell and its internal divisions, which are herein interpreted as derivative cells with formation of cell plates only. Each cavity is delimited by successive collapsed fusoid cells arranged perpendicularly to the veins. Fusoid cells in all studied Poaceae members originate from the ground meristem, as do the colourless cells in Joinvillea ascendens (Joinvilleaceae). These two types of mesophyll cell have a strongly similar ontogeny, distinguished mainly by the collapse of the fusoid cells in Poaceae, which is not observed in the colourless cells in J. ascendens. Within the Poaceae, the meristematic origin of fusoid cells is the same in the early-diverging lineages, BOP clade and Panicoideae, and thus they are homologous within the family. The same topography and meristematic origin suggest that fusoid cells in Poaceae and colourless cells in Joinvilleaceae are homologous. The results also suggest that the role played by the fusoid cells in young grass leaves is related to synthesis and storage of starch granules at early stages of development.

Treatment of Plants with Gaseous Ethylene and Gaseous Inhibitors of Ethylene Action.

The gaseous nature of ethylene affects not only its role in plant biology but also how you treat plants with the hormone. In many ways, it simplifies the treatment problem. Other hormones have to be made up in solution and applied to some part of the plant hoping the hormone will be taken up into the plant and translocated throughout the plant at the desired concentration. Because all plant cells are connected by an intercellular gas space the ethylene concentration you treat with is relatively quickly reached throughout the plant. In some instances, like mature fruit, treatment with ethylene initiates autocatalytic synthesis of ethylene. However, in most experiments, the exogenous ethylene concentration is saturating, usually >1 μL L-1, and the synthesis of additional ethylene is inconsequential. Also facilitating ethylene research compared with other hormones is that there are inhibitors of ethylene action 1-MCP (1-methylcyclopropene) and 2,5-NBD (2,5-norbornadiene) that are also gases wherein you can achieve nearly 100% inhibition of ethylene action quickly and with few side effects. Inhibitors for other plant hormones are applied as a solution and their transport and concentration at the desired site is not always known and difficult to measure. Here, our focus is on how to treat plants and plant parts with the ethylene gas and the gaseous inhibitors of ethylene action.

Ontogeny of fusoid cells in Guadua species (Poaceae, Bambusoideae, Bambuseae): evidence for transdifferentiation and possible functions

Fusoid cells have been interpreted as cells or intercellular spaces, according to different authors. Here, structural and ultrastructural evidence is provided relative to the origin and changes experimented by chlorenchyma cells (“arm cells”) to differentiate into fusoid cells with large intercellular spaces between them. Performed studies and observations were made using Light and Transmission Electron Microscopy. Fusoid cells in Guadua species die but do not remain intact; instead, they uniformly collapse, delimiting conspicuous intercellular spaces which are bigger and different in shape from these cells. In transverse sections of mature and expanded bamboo leaf blades, usually seen in anatomical descriptions, the so-called “fusoid cells” are actually conspicuous intercellular gas spaces delimited by successive collapsed (and rarely not collapsed) fusoid cells. Also, we hypothesize possible relations or links between fusoid cell shape, structural function and apoplastic transport in bamboo leaves.

Evolution of tree nutrition

Using a broad definition of trees, the evolutionary origins of trees in a nutritional context is considered using data from the fossil record and molecular phylogeny. Trees are first known from the Late Devonian about 380 million years ago, originated polyphyletically at the pteridophyte grade of organization; the earliest gymnosperms were trees, and trees are polyphyletic in the angiosperms. Nutrient transporters, assimilatory pathways, homoiohydry (cuticle, intercellular gas spaces, stomata, endohydric water transport systems including xylem and phloem-like tissue) and arbuscular mycorrhizas preceded the origin of trees. Nutritional innovations that began uniquely in trees were the seed habit and, certainly (but not necessarily uniquely) in trees, ectomycorrhizas, cyanobacterial, actinorhizal and rhizobial (Parasponia, some legumes) diazotrophic symbioses and cluster roots.

Horsetails get the wind up

Horsetails get the wind up

Formation of intercellular gas space in the diaphragm during the development of aerenchyma in the leaf petiole of Sagittaria trifolia

The development of aerenchyma in the petiole of Sagittaria trifolia L. was studied by means of light-microscopy, scanning electron microscope, transmission electron microscope and immunofluorescence, focusing on the formation of intercellular spaces in diaphragms and its relationship with the organization of cortical microtubule arrays. A complex and organized honeycomb-like schizogenous aerenchyma formed by cylinders and vascular diaphragms was observed in the petiole of S. trifolia at different developmental stages. Cell division was the primary factor contributing to the increased volume of air spaces at early stages, while cell enlargement became the primary factor at later stages. The cortical microtubules localize at the sites where intercellular spaces and the secondary cell walls will be formed or deposited during the formation of intercellular spaces by the separation of diaphragm cells. Cortical microtubules were observed at the boundary of diaphragm cells and the fringes of intercellular spaces at later developmental stages where cell expansion occurs rapidly. These observations support the hypothesis that reorganization of cortical microtubule arrays might be related to the formation of air spaces in diaphragms and are involved in the deposition of secondary cell walls.

The causes of sinking and floating in turions of Myriophyllum verticillatum

The sinking and floating (density) of the special winter buds (turions) produced by many aquatic plants play important roles in their life cycles, yet there has been little experimental study of these phenomena. However, it has been postulated that starch determines the density of turions. In order to test this hypothesis, turions of Myriophyllum verticillatum L. were collected from October through April and analyzed for density, dry-to-fresh-weight ratio and starch content. Density did not correlate closely ( R 2 = 0.37) with the dry-to-fresh-weight ratios. Density strongly correlated ( R 2 = 0.99) with starch only in the January collections, but not at several other times, so starch content alone is not always the major determinant of turion density. Intracellular lacunae (potentially gas spaces) also occur within the axes of these turions, and the lacunal volumes increased ca. 20-fold as they resumed growth, at which time the turions started to float. Significantly, turions, which were near the density of water, could be sunk or floated by changing the ambient pressure (which would alter their internal gas volume). Thus, starch has a role in determining the density of M. verticillatum turions, but the amount of intercellular gas space may be more important, especially when they resume growth in the spring.

Photoacoustic analysis indicates that chloroplast movement does not alter liquid-phase CO2 diffusion in leaves of Alocasia brisbanensis.

Light-mediated chloroplast movements are common in plants. When leaves of Alocasia brisbanensis (F.M. Bailey) Domin are exposed to dim light, mesophyll chloroplasts spread along the periclinal walls normal to the light, maximizing absorbance. Under high light, the chloroplasts move to anticlinal walls. It has been proposed that movement to the high-light position shortens the diffusion path for CO(2) from the intercellular air spaces to the chloroplasts, thus reducing CO(2) limitation of photosynthesis. To test this hypothesis, we used pulsed photoacoustics to measure oxygen diffusion times as a proxy for CO(2) diffusion in leaf cells. We found no evidence that chloroplast movement to the high-light position enhanced gas diffusion. Times for oxygen diffusion were not shorter in leaves pretreated with white light, which induced chloroplast movement to the high-light position, compared with leaves pretreated with 500 to 700 nm light, which did not induce movement. From the oxygen diffusion time and the diffusion distance from chloroplasts to the intercellular gas space, we calculated an oxygen permeability of 2.25 x 10(-)(6) cm(2) s(-)(1) for leaf cells at 20 degrees C. When leaf temperature was varied from 5 degrees C to 40 degrees C, the permeability for oxygen increased between 5 degrees C and 20 degrees C but changed little between 20 degrees C and 40 degrees C, indicating changes in viscosity or other physical parameters of leaf cells above 20 degrees C. Resistance for CO(2) estimated from oxygen permeability was in good agreement with published values, validating photoacoustics as another way of assessing internal resistances to CO(2) diffusion.

Selection pressures on stomatal evolution.

Fossil evidence shows that stomata have occurred in sporophytes and (briefly) gametophytes of embryophytes during the last 400myr. Cladistic analyses with hornworts basal are consistent with a unique origin of stomata, although cladograms with hornworts as the deepest branching embryophytes require loss of stomata early in the evolution of liverworts. Functional considerations suggest that stomata evolved from pores in the epidermis of plant organs which were at least three cell layers thick and had intercellular gas spaces and a cuticle; an endohydric conducting system would not have been necessary for low-growing rhizophytes, especially in early Palaeozoic CO2 -rich atmospheres. The 'prestomatal state' (pores) would have permitted higher photosynthetic rates per unit ground area. Functional stomata, and endohydry, permit the evolution of homoiohydry and the loss of vegetative desiccation tolerance and plants >1m tall. Stomatal functioning would then have involved maintenance of hydration, and restricting the occurrence of xylem embolism, under relatively desiccating conditions at the expense of limiting carbon acquisition. The time scale of environmental fluctuations over which stomatal responses can maximize carbon gain per unit water loss varies among taxa and life forms. Contents Summary 371 I. Introduction 371 II. Monophyly of stomata? 372 III. Roles of stomata in extant plants 373 IV. Ecophysiology of ancestrally astomatous terrestrial plants 375 V. Evolution of stomata 379 VI. Ecophysiological implications of losses of stomata 382 VII. Conclusions 384 Acknowledgements 384 References 384.

A novel approach to the in situ measurement of oxygen concentrations in the sapwood of woody plants

AbstractA novel technique for the physico‐chemical analysis of xylem sap by underwater access to the sapwood of trees is described. In situ measurements of dissolved oxygen in the sapwood are performed by combining this technique with a novel optical method for oxygen detection. In early spring, the oxygen concentration of the sapwood of Betula pendula was in the range of 80–230 µmol O2 L−1, corresponding to an oxygen deficit of 40–75% of air saturation. Oxygen concentration maxima and minima occurred early in the morning and in the afternoon, respectively, whereas xylem sap temperatures showed the reverse pattern. In the sapwood, hypoxia increased from the beginning of bud break until frondescence, when a deficit of 86% of air saturation marked the upper limit of oxygen depletion. There seemed to be no relationship between daily variations of oxygen concentration and xylem sap pressure. In summer, sap flow was a major determinant for the diurnal variation of dissolved oxygen concentration. Oxygen supply to the sapwood was determined by both radial influx into the trunk through intercellular gas spaces and transport of dissolved oxygen via xylem sap flow. Radial influx seemed to be favoured during night‐time, when the trunk was warmer than ambient air. During daytime, the hypoxia of the sapwood rose and increased sharply in the evening, when sap flow velocity approximated zero. High temperature in the sapwood enhanced the respiratory oxygen consumption of the wood parenchyma while the supply of dissolved oxygen via the transpiration stream became ineffective.

Methane flux in grassy marshlands near Kolyma River, north-eastern Siberia

The relationships between vegetation types and methane flux were evaluated in north-eastern Siberia in the summer of 1995. Based on 71 50×50-cm plots, the vegetation was divided into three types by TWINSPAN cluster analysis: (1) Eriophorum grassland where species richness was high and moss well-established ( Eriophorum grassland), (2) horsetail grassland with moss cover and (3) Carex grassland without moss. Vascular plant cover in all vegetation types was less than 50%. The methane flux was measured by a static chamber method. Horsetail grassland emitted the highest amount of methane, 165.5 mg CH 4/m 2/d, while diverse-sedge grassland emitted less methane, i.e., −1.9 mg CH 4/m 2/d. Methane flux positively increased with electric conductivity (EC), water depth, thaw depth, and soil humidity. Of those, EC was strongly correlated to methane emission (Spearman's rank correlation, r 2=0.630). The difference in methane flux between horsetail grassland and sedge-dominated grassland suggested that the morphological characteristics of vascular plants were important on methane transport, probably because vascular plants, such as horsetail, that developed aerenchyma and intercellular gas space promoted methane transport from soil to air while mosses do not.

Diffusion and reaction of oxygen in the central tissue of ureide‐producing legume nodules

ABSTRACTPrevious simulation models for the diffusion and reaction of oxygen in legume nodules were based on infected cells and neglected adjacent uninfected cells. This study uses a three‐dimensional model of the central zone of legume nodules made up of the two cell types represented by a geometrically defined, space‐filling, binary combination of polyhedra, each with bevelled edges to allow for a network of intercellular gas spaces. The model predicted a distinctively compartmentalized distribution of [O2] between uninfected and infected cells; with high O2 concentrations for an uninfected cell being consistent with, and necessary for, efficient operation of uricase and ureide synthesis and low O2 concentrations across most of the infected cell providing a suitable environment for N2‐fixation. Compartmentalization of O2 also predicted significant O2 fluxes between cell types, compromising maintenance of low [O2] in infected cells, as well as high [O2] in uninfected cells. The results predict that there might be significant resistance to O2 diffusion across the cell : cell interface due to the plasmalemma and cell walls.

The minimum size of seeds and spores in relation to the ontogeny of homoiohydric plants

Homoiohydry may be defined as the capacity of nondormant terrestrial plants to remain hydrated, albeit without the capacity for net CO2 fixation, when the soil can supply water to the plant less rapidly than the atmosphere can potentially remove water in transpiration. Homoiohydry is an attribute of the sporophytes of most extant vascular plants and involves significant differentiation with roots (or functionally analogous structures), xylem, cuticle, stomata and intercellular gas spaces (Raven 1977; Edwards, Abbott & Raven 1996; Bell & Mooers 1997). Homoiohydry was a major physiological innovation in the evolution of embryophytes and has enabled plants 1-100 m high to grow in terrestrial habitats with fluctuating soil water availability and evaporative demand of the atmosphere (Raven 1977, 1984a, 1993, 1997a, 1998). The possession of homoiohydric characteristics permits non-dormant sporophytic structures to be desiccation-intolerant, i.e. unable to survive equilibration with an atmospheric relative humidity of less than c. 50% (i.e. a water potential of c. -100 MPa). Whatever the mechanistic basis for this height restriction of desiccation-tolerant growing vegetative structures of land plants to less than 1 m, it appears that the occurrence of terrestrial plants in the 1-100 m height range requires desiccation-intolerance in the growing sporophyte combined with homoiohydry. It must be remembered that desiccation-tolerance (as defined above) is common in dormant structures (e.g. seeds) of those plants which are desiccation-intolerant when growing and apparently relates to the widespread occurrence in vascular plants of a number of closely related genes encoding 'late-embryogenesisabundant' proteins, one group of which is termed the dehydrins (Ingrams & Bartels 1996). Major reproductive innovations in the evolution of embryophytes were the polyphyletic evolution of heterospory and, in a few of these parallel heterosporous lines of evolution, the seed habit, and culminated in the plant supplying all of the water needed to its reproductive structures, so that above-ground sexual reproductive processes relied only on soil water supply to the

The development of blackcurrant fruit from flower to maturity: a comparative study by 3D nuclear magnetic resonance (NMR) micro‐imaging and conventional histology

The development of fruits of blackcurrant (Ribes nigrum) cv. Ben Alder from flower to maturity was studied non‐invasively by nuclear magnetic resonance (NMR) microscopy, using attached and detached fruits, and the images were compared with those from low temperature scanning electron microscopy (LTSEM) and conventional resin histology. The NMR images derived from 2‐D and 3‐D datasets showed the previously unreported growth of arillar tissues to the extent that they almost completely occlude the locular cavity, but LTSEM and resin histology revealed that no fusion occurs between the arillar tissues and the gelatinous sheath surrounding each seed, or between the arillar tissues and the endocarp. The discontinuities between these tissues cause magnetic inhomogenities which result in these structures being clearly resolved by gradient echo imaging sequences. During seed maturation the endosperm changed from high (bright) to low (dark) signal intensity as lipid reserves formed and solidified, whereas the gelatinous sheath had high signal intensity throughout maturation. The high lipid concentration in the seed was manifested by chemical shift effects in the images and the increasing viscosity of the endosperm was reflected in the decrease in spin–lattice (T1) relaxation times. The funiculi, throughout development of seeds, appeared in NMR images with low signal intensity and 3‐D surface‐rendered reconstructions illustrated the complexity of the spatial array of seeds and funiculi arising from parietal placentas within the loculus. All other vascular tissues in the pericarp and placentas were resolved as a small bright core surrounded by a dark region, within a matrix of moderate signal intensity. Conventional microscopical studies then showed that the bright core discernible by NMR imaging encompassed an entire vascular bundle whereas the darker surrounding region represented small parenchyma cells with pronounced intercellular gas spaces. Other regions of the pericarp which included extremely large parenchyma cells, however, had few intercellular spaces and consequently gave rise to brighter regions of the image.

Flooding tolerance of Carex species. I. Root structure

Young Carex extensa Good., C. remota L. and C. pseudocyperus L. plants were subjected to aerobic or anaerobic growth conditions in nutrient solution for 40 d. Root anatomy was studied by serial transsections and longitudinal sections of the root tip. Under both growth conditions, the flooding-intolerant C. extensa developed the typical Carex root pattern, i.e. an intact cortex in the youngest part of the root, but lysogenous aerenchyma in maturing parts. In contrast, flooding-tolerant C. remota from periodically flooded habitats showed a similar root anatomy to C. extensa under aerobic conditions, but a cortex with fine intercellular spaces throughout most of the root under anaerobic conditions. The flooding-tolerant C. pseudocyperus from permanently flooded stands developed an intact cortex over most of the root length under both growth conditions. Fine intercellular spaces on four sides of each cortical cell penetrated into the very tip of the root in this species, connecting the whole root with the lacunae of the leaves and the atmosphere. In both flooding-tolerant species, morphometry showed that even under anaerobic growth conditions and despite the maintenance of a juvenile growth habit, i.e. intact cortical cells, the average root porosities were more than 20% and there was an increase in the contact area between intercellular gas spaces and the surface of cortical cells. While C. remota showed radial oxygen loss along the whole root length, C. pseudocyperus released oxygen to an oxygen-free medium only at the root tip. It is concluded that the maintenance of a juvenile root structure in combination with a system of fine intercellular spaces allows efficient nutrient uptake and plant growth during anaerobiosis in flooding-tolerant Carex species, in contrast to those species which may tolerate periods of anaerobiosis by forming aerenchyma at the cost of decreased nutrient uptake and growth.

CAM photosynthesis in submerged aquatic plants

Crassulacean acid metabolism (CAM) is a CO2-concentrating mechanism selected in response to aridity in terrestrial habitats, and, in aquatic environments, to ambient limitations of carbon. Evidence is reviewed for its presence in five genera of aquatic vascular plants, includingIsoetes, Sagittaria, Vallisneria, Crassula, andLittorella. Initially, aquatic CAM was considered by some to be an oxymoron, but some aquatic species have been studied in sufficient detail to say definitively that they possess CAM photosynthesis. CO2-concentrating mechanisms in photosynthetic organs require a barrier to leakage; e.g., terrestrial C4 plants have suberized bundle sheath cells and terrestrial CAM plants high stomatal resistance. In aquatic CAM plants the primary barrier to CO2 leakage is the extremely high difrusional resistance of water. This, coupled with the sink provided by extensive intercellular gas space, generates daytime CO2(pi) comparable to terrestrial CAM plants. CAM contributes to the carbon budget by both net carbon gain and carbon recycling, and the magnitude of each is environmentally influenced. Aquatic CAM plants inhabit sites where photosynthesis is potentially limited by carbon. Many occupy moderately fertile shallow temporary pools that experience extreme diel fluctuations in carbon availability. CAM plants are able to take advantage of elevated nighttime CO2 levels in these habitats. This gives them a competitive advantage over non-CAM species that are carbon starved during the day and an advantage over species that expend energy in membrane transport of bicarbonate. Some aquatic CAM plants are distributed in highly infertile lakes, where extreme carbon limitation and light are important selective factors.

Three-dimensional study of the intercellular gas space inVigna radiata hypocotyl

Infiltration of the intercellular gas space is often used in physiological experimentation either to reach internal targets with various biochemical probes or to extract molecules from the apoplast. Such investigations require a good understanding of the organization and structure of the gas space system. This system was studied in the mung bean hypocotyl using different approaches, in particular internal microcasting of seedlings. Results show the presence of two continuous, more or less independent, networks, one in the cortical parenchyma, the other in the pith. The narrow tubules of one or the other network connect all cells within a tissue. Infiltration with physiological solutions does not significantly disturb living cells, at least in the short term, but opens a large field for experimental applications.

Flood‐induced leaf elongation in Rumex species: effects of water depth and water movements

SUMMARYSeveral species from the genus Rumex are found in Dutch river forelands. Species such as R. palustris Sm. From the low, frequently flooded areas are well adapted to wet conditions, Rumex species from higher and less frequently flooded sites are poorly adapted and therefore sensitive to flooding. One of the adaptations to flooding is enhanced shoot elongation upon complete submergence, enabling plants to restore leaf‐air contact, provided that the water is not too deep. This paper demonstrates the strong variation in the absolute extent of flood‐induced leaf elongation among species of the genus Rumex. The effects of flooding on shoot dry and fresh weight and internal gas volumes of an elongating and a non‐elongating species, R. palustris and R. acetosella L., were compared. Net water uptake in response to complete submergence was observed in the shoots of both species. Based on results presented here, we conclude that in plants of R. palustris water enters the cells and is used for cell expansion leading to petiole elongation, whereas in plants of R. acetosella at least part of the water taken up fills the intercellular gas spaces. Elongation of completely submerged Rumex plants does not vary with different depths of submergence, This was concluded from the observation that there is little effect of either hydrostatic pressure or irradiance on leaf elongation during complete submergence. However, when R. palustris plants were subjected to a changing water depth, i.e. alternate periods of complete submergence and waterlogging, they elongated less strongly than under permanent complete submergence. Water movements did not affect leaf elongation induced by submergence.