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A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response.

ABSTRACT: In this paper, we present a detailed and comprehensive mathematical model of active and passive ion and water transport in plant roots. Two key features are the explicit consideration of the separate, but interconnected, apoplastic, and symplastic transport pathways for ions and water, and the inclusion of both active and passive ion transport mechanisms. The model is used to investigate the respective roles of the endodermal Casparian strip and suberin lamellae in the salt stress response of plant roots. While it is thought that these barriers influence different transport pathways, it has proven difficult to distinguish their separate functions experimentally. In particular, the specific role of the suberin lamellae has been unclear. A key finding based on our simulations was that the Casparian strip is essential in preventing excessive uptake of Na⁺ into the plant via apoplastic bypass, with a barrier efficiency that is reflected by a sharp gradient in the steady-state radial distribution of apoplastic Na⁺ across the barrier. Even more significantly, this function cannot be replaced by the action of membrane transporters. The simulations also demonstrated that the positive effect of the Casparian strip of controlling Na⁺ uptake, was somewhat offset by its contribution to the osmotic stress component: a more effective barrier increased the detrimental osmotic stress effect. In contrast, the suberin lamellae were found to play a relatively minor, even non-essential, role in the overall response to salt stress, with the presence of the suberin lamellae resulting in only a slight reduction in Na⁺ uptake. However, perhaps more significantly, the simulations identified a possible role of suberin lamellae in reducing plant energy requirements by acting as a physical barrier to preventing the passive leakage of Na⁺ into endodermal cells. The model results suggest that more and particular experimental attention should be paid to the properties of the Casparian strip when assessing the salt tolerance of different plant varieties and species. Indeed, the Casparian strip appears to be a more promising target for plant breeding and plant genetic engineering efforts than the suberin lamellae for the goal of improving salt tolerance.

SUBMITTER: Foster KJ

PROVIDER: S-EPMC5532442 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response.

Foster Kylie J KJ Miklavcic Stanley J SJ

Frontiers in plant science 20170728

In this paper, we present a detailed and comprehensive mathematical model of active and passive ion and water transport in plant roots. Two key features are the explicit consideration of the separate, but interconnected, apoplastic, and symplastic transport pathways for ions and water, and the inclusion of both active and passive ion transport mechanisms. The model is used to investigate the respective roles of the endodermal Casparian strip and suberin lamellae in the salt stress response of pl ...[more]

PMID: 28804493

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Project description:SOS1 transporters play an essential role in plant salt tolerance. Although SOS1 is known to encode a plasma membrane Na+/H+ antiporter, the transport mechanisms by which these transporters contribute to salt tolerance at the level of the whole root are unclear. Gene expression and flux measurements have provided conflicting evidence for the location of SOS1 transporter activity, making it difficult to determine their function. Whether SOS1 transporters load or unload Na+ from the root xylem transpiration stream is also disputed. To address these areas of contention, we applied a mathematical model to answer the question: what is the function of SOS1 transporters in salt-stressed Arabidopsis roots? We used our biophysical model of ion and water transport in a salt-stressed root to simulate a wide range of SOS1 transporter locations in a model Arabidopsis root, providing a level of detail that cannot currently be achieved by experimentation. We compared our simulations with available experimental data to find reasonable parameters for the model and to determine likely locations of SOS1 transporter activity. We found that SOS1 transporters are likely to be operating in at least one tissue of the outer mature root, in the mature stele, and in the epidermis of the root apex. SOS1 transporter activity in the mature outer root cells is essential to maintain low cytosolic Na+ levels in the root and also restricts the uptake of Na+ to the shoot. SOS1 transporters in the stele actively load Na+ into the xylem transpiration stream, enhancing the transport of Na+ and water to the shoot. SOS1 transporters acting in the apex restrict cytosolic Na+ concentrations in the apex but are unable to maintain low cytosolic Na+ levels in the mature root. Our findings suggest that targeted, tissue-specific overexpression or knockout of SOS1 may lead to greater salt tolerance than has been achieved with constitutive gene changes. Tissue-specific changes to the expression of SOS1 could be used to identify the appropriate balance between limiting Na+ uptake to the shoot while maintaining water uptake, potentially leading to enhancements in salt tolerance.

Project description:Growth- and health-promoting bacteria can boost crop productivity in a sustainable way. Pseudomonas simiae WCS417 is such a bacterium that efficiently colonizes roots, modifies the architecture of the root system to increase its size, and induces systemic resistance to make plants more resistant to pests and pathogens. Our previous work suggested that WCS417-induced phenotypes are controlled by root cell-type-specific mechanisms. However, it remains unclear how WCS417 affects these mechanisms. In this study, we transcriptionally profiled five Arabidopsis thaliana root cell types following WCS417 colonization. We found that the cortex and endodermis have the most differentially expressed genes, even though they are not in direct contact with this epiphytic bacterium. Many of these genes are associated with reduced cell wall biogenesis, and mutant analysis suggests that this downregulation facilitates WCS417-driven root architectural changes. Furthermore, we observed elevated expression of suberin biosynthesis genes and increased deposition of suberin in the endodermis of WCS417-colonized roots. Using an endodermal barrier mutant, we showed the importance of endodermal barrier integrity for optimal plant-beneficial bacterium association. Comparison of the transcriptome profiles in the two epidermal cell types that are in direct contact with WCS417-trichoblasts that form root hairs and atrichoblasts that do not-implies a difference in potential for defense gene activation. While both cell types respond to WCS417, trichoblasts displayed both higher basal and WCS417-dependent activation of defense-related genes compared with atrichoblasts. This suggests that root hairs may activate root immunity, a hypothesis that is supported by differential immune responses in root hair mutants. Taken together, these results highlight the strength of cell-type-specific transcriptional profiling to uncover "masked" biological mechanisms underlying beneficial plant-microbe associations.

Project description:Background and aimsRoots have complex anatomical structures, and certain localized cell layers develop suberized apoplastic barriers. The size and tightness of these barriers depend on the growth conditions and on the age of the root. Such complex anatomical structures result in a composite water and solute transport in roots.MethodsDevelopment of apoplastic barriers along barley seminal roots was detected using various staining methods, and the suberin amounts in the apical and basal zones were analysed using gas chromatography-mass spectometry (GC-MS). The hydraulic conductivity of roots ( Lp r ) and of cortical cells ( Lp c ) was measured using root and cell pressure probes.Key resultsWhen grown in hydroponics, barley roots did not form an exodermis, even at their basal zones. However, they developed an endodermis. Endodermal Casparian bands first appeared as 'dots' as early as at 20 mm from the apex, whereas a patchy suberin lamellae appeared at 60 mm. The endodermal suberin accounted for the total suberin of the roots. The absolute amount in the basal zone was significantly higher than in the apical zone, which was inversely proportional to the Lp r . Comparison of Lp r and Lp c suggested that cell to cell pathways dominate for water transport in roots. However, the calculation of Lp r from Lp c showed that at least 26 % of water transport occurs through the apoplast. Roots had different solute permeabilities ( P sr ) and reflection coefficients ( σ sr ) for the solutes used. The σ sr was below unity for the solutes, which have virtually zero permeability for semi-permeable membranes.ConclusionsSuberized endodermis significantly reduces Lp r of seminal roots. The water and solute transport across barley roots is composite in nature and they do not behave like ideal osmometers. The composite transport model should be extended by adding components arranged in series (cortex, endodermis) in addition to the currently included components arranged in parallel (apoplastic, cell to cell pathways).

Project description:BackgroundSalt tolerance in grapevine is associated with chloride (Cl-) exclusion from shoots; the rate-limiting step being the passage of Cl- between the root symplast and xylem apoplast. Despite an understanding of the physiological mechanism of Cl- exclusion in grapevine, the molecular identity of membrane proteins that control this process have remained elusive. To elucidate candidate genes likely to control Cl- exclusion, we compared the root transcriptomes of three Vitis spp. with contrasting shoot Cl- exclusion capacities using a custom microarray.ResultsWhen challenged with 50 mM Cl-, transcriptional changes of genotypes 140 Ruggeri (shoot Cl- excluding rootstock), K51-40 (shoot Cl- including rootstock) and Cabernet Sauvignon (intermediate shoot Cl- excluder) differed. The magnitude of salt-induced transcriptional changes in roots correlated with the amount of Cl- accumulated in shoots. Abiotic-stress responsive transcripts (e.g. heat shock proteins) were induced in 140 Ruggeri, respiratory transcripts were repressed in Cabernet Sauvignon, and the expression of hypersensitive response and ROS scavenging transcripts was altered in K51-40. Despite these differences, no obvious Cl- transporters were identified. However, under control conditions where differences in shoot Cl- exclusion between rootstocks were still significant, genes encoding putative ion channels SLAH3, ALMT1 and putative kinases SnRK2.6 and CPKs were differentially expressed between rootstocks, as were members of the NRT1 (NAXT1 and NRT1.4), and CLC families.ConclusionsThese results suggest that transcriptional events contributing to the Cl- exclusion mechanism in grapevine are not stress-inducible, but constitutively different between contrasting varieties. We have identified individual genes from large families known to have members with roles in anion transport in other plants, as likely candidates for controlling anion homeostasis and Cl- exclusion in Vitis species. We propose these genes as priority candidates for functional characterisation to determine their role in chloride transport in grapevine and other plants.

Dataset Information

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response.

Publications

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response.

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