•Suberized apoplastic barriers are known to impede water and solute transport in roots.•Different complex anatomical structures are evident for Arabidopsis, barley and rice roots.•A simple view that ...transfer of knowledge on root water transport from Arabidopsis to crop plants may not always be straightforward.•Caution is required when correlating amounts of suberin in roots with water uptake.•Not only suberin amounts, but also monomer arrangements and its microstructure may play an important role.
Water is the most important prerequisite for life and plays a major role during uptake and transport of nutrients. Roots are the plant organs that take up the major part of water, from the surrounding soil. Water uptake is related to the root system architecture, root growth, age and species dependent complex developmental changes in the anatomical structures. The latter is mainly attributed to the deposition of suberized barriers in certain layers of cell walls, such as endo- and exodermis. With respect to water permeability, changes in the suberization of roots are most relevant. Water transport or hydraulic conductivity of roots (Lpr) can be described by the composite transport model and is known to be very variable between plant species and growth conditions and root developmental states. In this review, we summarize how anatomical structures and apoplastic barriers of roots can diversely affect water transport, comparing the model plant Arabidopsis with crop plants, such as barley and rice. Results comparing the suberin amounts and water transport properties indicate that the common assumption that suberin amount negatively correlates with water and solute transport through roots may not always be true. The composition, microstructure and localization of suberin may also have a great impact on the formation of efficient barriers to water and solutes.
BACKGROUND: The plant cuticle is an extracellular lipophilic biopolymer covering leaf and fruit surfaces. Its main function is the protection of land-living plants from uncontrolled water loss. In ...the past, the permeability of the cuticle to water and to non-ionic lipophilic molecules (pesticides, herbicides and other xenobiotics) was studied intensively, whereas cuticular penetration of polar ionic compounds was rarely investigated. RECENT PROGRESS: Recent work measuring cuticular penetration of inorganic and organic ions is presented; the effects of molecular size of ions, temperature, wax extraction, humidity and plasticizers strongly support the conclusion that ions penetrate cuticles via water-filled pores. The cuticle covering stomata and trichomes forms the preferential site of ion penetration. This indicates that cuticles possess a pronounced lateral heterogeneity: the largest fraction of the cuticle surface is covered by the lipophilic domains of cutin and wax, but to a certain extent polar domains are also present in the cuticle, which form preferential sites of penetration for polar compounds. THE FUTURE: The chemical nature of these polar domains awaits detailed characterization, which will be of major importance in agriculture and green biotechnology, since polar paths of diffusion represent the most important transport routes for foliar-applied nutrients. Furthermore, many compounds acting as inducers of gene expression in transgenic plants are ionic and need to penetrate the cuticle via polar paths in order to be active.
Although it is implied that suberized apoplastic barriers of roots negatively correlate with water and solute permeabilities, direct transport measurements across roots with altered amounts and ...compositions of aliphatic suberin are scarce. In the present study, hydroponically grown Arabidopsis wild types (Co18 and Co10) and different suberin mutants with altered amounts and/or compositions (horst, esb1-1, and esb1-2) were used to test this hypothesis. Detailed histochemical studies revealed late development of Casparian bands and suberin lamellae in the horst mutant compared with wild types and esb mutants. Suberin analysis with gas chromatography and mass spectrometry (GC-MS) showed that the horst mutant had ~33% lower amounts of aliphatic monomers than Co18 and Co10. In contrast, enhanced suberin mutants (esb1-1 and esb1-2) had twice the amount of suberin as the wild types. Correlative permeability measurements, which were carried out for the first time with a root pressure probe for Arabidopsis, revealed that the hydraulic conductivity (Lp r ) and NaCI permeability (P sr ) of the whole root system of the horst mutant were markedly greater than in the respective wild types. This was reflected by the total amounts of aliphatic suberin determined in the roots. However, increased levels of aliphatic suberin in esb mutants failed to reduce either water or NaCI permeabilities below those of the wild types. It was concluded that the simple view and the conventional assumption that the amount of root suberin negatively correlates with permeability may not always be true. The aliphatic monomer arrangement in the suberin biopolymer and its microstructure also play a role in apoplastic barrier formation.
▶ The first genes involved in suberin formation have been identified. ▶ Mutant analysis challenges models about biosynthesis and structure of suberin. ▶ Genetic evidence has established a crucial ...role for suberin in controlling water and ion transport.
Suberin is an apoplastic biopolymer with tissue-specific deposition in the cell walls of the endo- and exodermis of roots, of periderms including wound periderm and other border tissues. Suberised cell walls contain both polyaliphatic and polyaromatic domains which are supposedly cross-linked. The predominant aliphatic components are ω-hydroxyacids, α,ω-diacids, fatty acids and primary alcohols, whereas hydroxycinnamic acids, especially ferulic acid, are the main components of the polyaromatic domain. Although the monomeric composition of suberin has been known for decades, its biosynthesis and deposition has mainly been a subject of speculation. Only recently, significant progress elucidating suberin biosynthesis has been achieved using molecular genetic approaches, especially in the model species Arabidopsis. In parallel, the long-standing hypothesis that suberin functions as an apoplastic barrier has been corroborated by sophisticated, quantitative physiological studies in the past decade. These studies demonstrated that suberised cell walls could act as barriers, minimising the movement of water and nutrients, restricting pathogen invasion and impeding toxic gas diffusion. In addition, suberised cell walls provide a barrier to radial oxygen loss from roots to the anaerobic root substrate in wetland plants. The recent onset of multidisciplinary approaches combining genetic, analytical and physiological studies has begun to deliver further insights into the physiological importance of suberin depositions in plants.
Most of the aerial organs of vascular plants are covered by a protective layer known as the cuticle, the main purpose of which is to limit transpirational water loss. Cuticles consist of an ...amphiphilic polyester matrix, polar polysaccharides that extend from the underlying epidermal cell wall and become less prominent towards the exterior, and hydrophobic waxes that dominate the surface. Here we report that the polarity gradient caused by this architecture renders the transport of water through astomatous olive and ivy leaf cuticles directional and that the permeation is regulated by the hydration level of the cutin-rich outer cuticular layer. We further report artificial nanocomposite membranes that are inspired by the cuticles' compositionally graded architecture and consist of hydrophilic cellulose nanocrystals and a hydrophobic polymer. The structure and composition of these cuticle-inspired membranes can easily be varied and this enables a systematic investigation of the water transport mechanism.
Key message
We identified two poplar clones of the same species as highly comparable, yet clones of two further species of the same genus to be distinctly different regarding multiple morphological ...and ecophysiological traits.
Leaf morphology, wax composition, and residual (cuticular) transpiration of four poplar clones (two clones of the hybrid species
P.
×
canescens
,
P. trichocarpa
, and
P. euphratica
) were monitored from the beginning to end of the growing season 2020. A pronounced epicuticular wax coverage was found only with
P. euphratica
. As the most prominent substance classes of cuticular wax primary alcohols, alkanes and esters were identified with
P.
×
canescens
and
P. trichocarpa
, whereas esters and alkanes were completely lacking in
P. euphratica
. Wax amounts were slightly decreasing during the season and significantly lower wax amounts were found for newly formed leaves in summer compared to leaves of the same age formed in spring. Residual (cuticular) transpiration was about five to tenfold lower for
P.
×
canescens
compared with the two other poplar species. Interestingly, with three of the four investigated species, newly formed leaves in summer had lower wax coverages and lower rates of residual (cuticular) transpiration compared to leaves of exactly the same age formed in spring. Our findings were especially surprising with
P. euphratica
, representing the only one of the four investigated poplar species naturally growing in very dry and hot climates in Central Asia. Instead of developing very low rates of residual (cuticular) transpiration, it seems to be of major advantage for
P. euphratica
to develop a pronounced epicuticular wax bloom efficiently reflecting light.
Suberin, a polymer composed of both aliphatic and aromatic domains, is deposited as a rough matrix upon plant surface damage and during normal growth in the root endodermis, bark, specialized organs ...(e.g., potato Solanum tuberosum tubers), and seed coats. To identify genes associated with the developmental control of suberin deposition, we investigated the chemical composition and transcriptomes of suberized tomato (Solanum lycopersicum) and russet apple (Malus x domestica) fruit surfaces. Consequently, a gene expression signature for suberin polymer assembly was revealed that is highly conserved in angiosperms. Seed permeability assays of knockout mutants corresponding to signature genes revealed regulatory proteins (i.e., AtMYB9 and AtMYB107) required for suberin assembly in the Arabidopsis thaliana seed coat. Seeds of myb107 and myb9 Arabidopsis mutants displayed a significant reduction in suberin monomers and altered levels of other seed coat-associated metabolites. They also exhibited increased permeability, and lower germination capacities under osmotic and salt stress. AtMYB9 and AtMYB107 appear to synchronize the transcriptional induction of aliphatic and aromatic monomer biosynthesis and transport and suberin polymerization in the seed outer integument layer. Collectively, our findings establish a regulatory system controlling developmentally deposited suberin, which likely differs from the one of stress-induced polymer assembly recognized to date.
Radial oxygen loss (ROL) and root porosity of rice (Oryza sativa L.) plants grown in either aerated or deoxygenated (stagnant) conditions were combined for the first time with extensive histochemical ...and biochemical studies of the apoplastic barriers in the roots' peripheral cell layers. Growth in stagnant solution significantly affected structural and, consequently, the physiological features of rice roots. It increased adventitious root porosity by about 20% and decreased the ROL towards the base to zero at a distance of 40 mm from the apex. By contrast, roots of plants grown in aerated solutions revealed the highest rates of ROL at 30 mm from the apex. Differences in the ROL pattern along the root were related to histochemical studies, which showed an early development of Casparian bands and suberin lamellae in the exodermis, and lignified sclerenchyma cells in roots of plants grown in deoxygenated solution. In agreement with anatomical studies, absolute contents of suberin and lignin in the outer part of the roots (OPR) were higher in plants grown in deoxygenated solution. Regardless of growth conditions, the levels of suberin and lignin increased along the roots towards the base. It is concluded that radial oxygen loss can be effectively restricted by the formation of a suberized exodermis and/or lignified sclerenchyma in the OPR. However, the relative contribution of suberin and lignin in the formation of a tight barrier is unclear. Knowing the permeability coefficient across OPR for roots of plants grown in both conditions will allow a more precise understanding of the mechanisms controlling ROL.
Barley (Hordeum vulgare) is more drought tolerant than other cereals, thus making it an excellent model for the study of the chemical, transcriptomic and physiological effects of water deficit. Roots ...are the first organ to sense soil water deficit. Therefore, we studied the response of barley seminal roots to different water potentials induced by polyethylene glycol (PEG) 8000.
We investigated changes in anatomical parameters by histochemistry and microscopy, quantitative and qualitative changes in suberin composition by analytical chemistry, transcript changes by RNA-sequencing (RNA-Seq), and the radial water and solute movement of roots using a root pressure probe.
In response to osmotic stress, genes in the suberin biosynthesis pathway were upregulated that correlated with increased suberin amounts in the endodermis and an overall reduction in hydraulic conductivity (Lpr). In parallel, transcriptomic data indicated no or only weak effects of osmotic stress on aquaporin expression.
These results indicate that osmotic stress enhances cell wall suberization and markedly reduces Lpr of the apoplastic pathway, whereas Lpr of the cell-to-cell pathway is not altered. Thus, the sealed apoplast markedly reduces the uncontrolled backflow of water from the root to the medium, whilst keeping constant water flow through the highly regulated cell-to-cell path.
Main conclusion
Time-dependent contact angle measurements of pure water on barley leaf surfaces allow quantifying the kinetics of surfactant diffusion into the leaf.
Barley leaf surfaces were sprayed ...with three different aqueous concentrations (0.1, 1.0 and 10%) of a monodisperse (tetraethylene glycol monododecyl ether) and a polydisperse alcohol ethoxylate (BrijL4). After 10 min, the surfactant solutions on the leaf surfaces were dry leading to surfactant coverages of 1, 10 and 63 µg cm
−2
, respectively. The highest surfactant coverage (63 µg cm
−2
) affected leaf physiology (photosynthesis and water loss) rapidly and irreversibly and leaves were dying within 2–6 h. These effects on leaf physiology did not occur with the lower surfactant coverages (1 and 10 µg cm
−2
). Directly after spraying of 0.1 and 1.0% surfactant solution and complete drying (10 min), leaf surfaces were fully wettable for pure water and contact angles were 0°. Within 60 min (0.1% surfactant) and 6 h (1.0% surfactant), leaf surfaces were non-wettable again and contact angles of pure water were identical to control leaves. Scanning electron microscopy investigations directly performed after surfactant spraying and drying indicated that leaf surface wax crystallites were partially or fully covered by surfactants. Wax platelets with unaltered microstructure were fully visible again within 2 to 6 h after treatment with 0.1% surfactant solutions. Gas chromatographic analysis showed that surfactant amounts on leaf surfaces continuously disappeared over time. Our results indicate that surfactants, applied at realistic coverages between 1 and 10 µg cm
−2
to barley leaf surfaces, leading to total wetting (contact angles of 0°) of leaf surfaces, are rapidly taken up by the leaves. As a consequence, leaf surface non-wettability is fully reappearing. An irreversible damage of the leaf surface fine structure leading to enhanced wetting and increased foliar transpiration seems highly unlikely at low surfactant coverages of 1 µg cm
−2
.
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