Dataset Information

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. III. Quantifying the Energy Costs of Ion Transport in Salt-Stressed Roots of Arabidopsis.

ABSTRACT: Salt stress defense mechanisms in plant roots, such as active Na+ efflux and storage, require energy in the form of ATP. Understanding the energy required for these transport mechanisms is an important step toward achieving an understanding of salt tolerance. However, accurate measurements of the fluxes required to estimate these energy costs are difficult to achieve by experimental means. As a result, the magnitude of the energy costs of ion transport in salt-stressed roots relative to the available energy is unclear, as are the relative contributions of different defense mechanisms to the total cost. We used mathematical modeling to address three key questions about the energy costs of ion transport in salt-stressed Arabidopsis roots: are the energy requirements calculated on the basis of flux data feasible; which transport steps are the main contributors to the total energy costs; and which transport processes could be altered to minimize the total energy costs? Using our biophysical model of ion and water transport we calculated the energy expended in the trans-plasma membrane and trans-tonoplast transport of Na+, K+, Cl-, and H+ in different regions of a salt-stressed model Arabidopsis root. Our calculated energy costs exceeded experimental estimates of the energy supplied by root respiration for high external NaCl concentrations. We found that Na+ exclusion from, and Cl- uptake into, the outer root were the major contributors to the total energy expended. Reducing the leakage of Na+ and the active uptake of Cl- across outer root plasma membranes would lower energy costs while enhancing exclusion of these ions. The high energy cost of ion transport in roots demonstrates that the energetic consequences of altering ion transport processes should be considered when attempting to improve salt tolerance.

SUBMITTER: Foster KJ

PROVIDER: S-EPMC7348042 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Publications

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. III. Quantifying the Energy Costs of Ion Transport in Salt-Stressed Roots of <i>Arabidopsis</i>.

Foster Kylie J KJ Miklavcic Stanley J SJ

Frontiers in plant science 20200703

Salt stress defense mechanisms in plant roots, such as active Na<sup>+</sup> efflux and storage, require energy in the form of ATP. Understanding the energy required for these transport mechanisms is an important step toward achieving an understanding of salt tolerance. However, accurate measurements of the fluxes required to estimate these energy costs are difficult to achieve by experimental means. As a result, the magnitude of the energy costs of ion transport in salt-stressed roots relative ...[more]

PMID: 32719693

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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: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.

Project description:BACKGROUND: Roots are an attractive system for genomic and post-genomic studies of NaCl responses, due to their primary importance to agriculture, and because of their relative structural and biochemical simplicity. Excellent genomic resources have been established for the study of Arabidopsis roots, however, a comprehensive microarray analysis of the root transcriptome following NaCl exposure is required to further understand plant responses to abiotic stress and facilitate future, systems-based analyses of the underlying regulatory networks. RESULTS: We used microarrays of 70-mer oligonucleotide probes representing 23,686 Arabidopsis genes to identify root transcripts that changed in relative abundance following 6 h, 24 h, or 48 h of hydroponic exposure to 150 mM NaCl. Enrichment analysis identified groups of structurally or functionally related genes whose members were statistically over-represented among up- or down-regulated transcripts. Our results are consistent with generally observed stress response themes, and highlight potentially important roles for underappreciated gene families, including: several groups of transporters (e.g. MATE, LeOPT1-like); signalling molecules (e.g. PERK kinases, MLO-like receptors), carbohydrate active enzymes (e.g. XTH18), transcription factors (e.g. members of ZIM, WRKY, NAC), and other proteins (e.g. 4CL-like, COMT-like, LOB-Class 1). We verified the NaCl-inducible expression of selected transcription factors and other genes by qRT-PCR. CONCLUSION: Microarray profiling of NaCl-treated Arabidopsis roots revealed dynamic changes in transcript abundance for at least 20% of the genome, including hundreds of transcription factors, kinases/phosphatases, hormone-related genes, and effectors of homeostasis, all of which highlight the complexity of this stress response. Our identification of these transcriptional responses, and groups of evolutionarily related genes with either similar or divergent transcriptional responses to stress, will facilitate mapping of regulatory networks and extend our ability to improve salt tolerance in plants.

Dataset Information

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. III. Quantifying the Energy Costs of Ion Transport in Salt-Stressed Roots of Arabidopsis.

Publications

A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. III. Quantifying the Energy Costs of Ion Transport in Salt-Stressed Roots of <i>Arabidopsis</i>.

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