Osmotic Stress Responses and Plant Growth Controlled by Potassium Transporters in Arabidopsis
TL;DR: It is proposed that the KUP6 subfamily transporters act as key factors in osmotic adjustment by balancing potassium homeostasis in cell growth and drought stress responses.
Abstract: Osmotic adjustment plays a fundamental role in water stress responses and growth in plants; however, the molecular mechanisms governing this process are not fully understood. Here, we demonstrated that the KUP potassium transporter family plays important roles in this process, under the control of abscisic acid (ABA) and auxin. We generated Arabidopsis thaliana multiple mutants for K+ uptake transporter 6 (KUP6), KUP8, KUP2/SHORT HYPOCOTYL3, and an ABA-responsive potassium efflux channel, guard cell outward rectifying K+ channel (GORK). The triple mutants, kup268 and kup68 gork, exhibited enhanced cell expansion, suggesting that these KUPs negatively regulate turgor-dependent growth. Potassium uptake experiments using 86radioactive rubidium ion (86Rb+) in the mutants indicated that these KUPs might be involved in potassium efflux in Arabidopsis roots. The mutants showed increased auxin responses and decreased sensitivity to an auxin inhibitor (1-N-naphthylphthalamic acid) and ABA in lateral root growth. During water deficit stress, kup68 gork impaired ABA-mediated stomatal closing, and kup268 and kup68 gork decreased survival of drought stress. The protein kinase SNF1-related protein kinases 2E (SRK2E), a key component of ABA signaling, interacted with and phosphorylated KUP6, suggesting that KUP functions are regulated directly via an ABA signaling complex. We propose that the KUP6 subfamily transporters act as key factors in osmotic adjustment by balancing potassium homeostasis in cell growth and drought stress responses.
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TL;DR: The systems that regulate plant adaptation to water stress through a sophisticated regulatory network are the subject of the current review and molecular mechanisms that plants use to increase stress tolerance, maintain appropriate hormone homeostasis and responses and prevent excess light damage are discussed.
Abstract: Water stress adversely impacts many aspects of the physiology of plants, especially photosynthetic capacity. If the stress is prolonged, plant growth and productivity are severely diminished. Plants have evolved complex physiological and biochemical adaptations to adjust and adapt to a variety of environmental stresses. The molecular and physiological mechanisms associated with water-stress tolerance and water-use efficiency have been extensively studied. The systems that regulate plant adaptation to water stress through a sophisticated regulatory network are the subject of the current review. Molecular mechanisms that plants use to increase stress tolerance, maintain appropriate hormone homeostasis and responses and prevent excess light damage, are also discussed. An understanding of how these systems are regulated and ameliorate the impact of water stress on plant productivity will provide the information needed to improve plant stress tolerance using biotechnology, while maintaining the yield and quality of crops.
1,083 citations
TL;DR: This review analyzes the physiological, biochemical, and molecular aspects of Na+ and Cl− uptake, sequestration, and transport associated with salinity, and discusses the role and importance of symplastic versus apoplastic pathways for ion uptake and the multiple roles of K+ in plant salinity stress.
Abstract: Salinity is a major threat to modern agriculture causing inhibition and impairment of crop growth and development. Here, we not only review recent advances in salinity stress research in plants but also revisit some basic perennial questions that still remain unanswered. In this review, we analyze the physiological, biochemical, and molecular aspects of Na+ and Cl- uptake, sequestration, and transport associated with salinity. We discuss the role and importance of symplastic versus apoplastic pathways for ion uptake and critically evaluate the role of different types of membrane transporters in Na+ and Cl- uptake and intercellular and intracellular ion distribution. Our incomplete knowledge regarding possible mechanisms of salinity sensing by plants is evaluated. Furthermore, a critical evaluation of the mechanisms of ion toxicity leads us to believe that, in contrast to currently held ideas, toxicity only plays a minor role in the cytosol and may be more prevalent in the vacuole. Lastly, the multiple roles of K+ in plant salinity stress are discussed.
619 citations
TL;DR: The dynamics of ABA metabolic pools and signaling that affects many of its physiological functions are reviewed.
Abstract: Abscisic acid (ABA) is an important phytohormone regulating plant growth, development, and stress responses. It has an essential role in multiple physiological processes of plants, such as stomatal closure, cuticular wax accumulation, leaf senescence, bud dormancy, seed germination, osmotic regulation, and growth inhibition among many others. Abscisic acid controls downstream responses to abiotic and biotic environmental changes through both transcriptional and posttranscriptional mechanisms. During the past 20 years, ABA biosynthesis and many of its signaling pathways have been well characterized. Here we review the dynamics of ABA metabolic pools and signaling that affects many of its physiological functions.
589 citations
Cites background from "Osmotic Stress Responses and Plant ..."
...OST1 can also up-regulate the activity of SLAC1 and KUP6, a KUP/HAK/KT family potassium efflux transporter, and inhibit KAT1 through phosphorylation, also affecting stomatal movement (Kwak et al. 2001; Geiger et al. 2009; Sato et al. 2009; Osakabe et al. 2013)....
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TL;DR: The role of multi-omics approaches in generating multi-pronged information to provide a better understanding of plant–microbe interactions that modulate cellular mechanisms in plants under extreme external conditions and help to optimize abiotic stresses is described.
Abstract: Abiotic stresses are the foremost limiting factors for agricultural productivity. Crop plants need to cope up adverse external pressure created by environmental and edaphic conditions with their intrinsic biological mechanisms, failing which their growth, development, and productivity suffer. Microorganisms, the most natural inhabitants of diverse environments exhibit enormous metabolic capabilities to mitigate abiotic stresses. Since microbial interactions with plants are an integral part of the living ecosystem, they are believed to be the natural partners that modulate local and systemic mechanisms in plants to offer defence under adverse external conditions. Plant-microbe interactions comprise complex mechanisms within the plant cellular system. Biochemical, molecular and physiological studies are paving the way in understanding the complex but integrated cellular processes. Under the continuous pressure of increasing climatic alterations, it now becomes more imperative to define and interpret plant-microbe relationships in terms of protection against abiotic stresses. At the same time, it also becomes essential to generate deeper insights into the stress-mitigating mechanisms in crop plants for their translation in higher productivity. Multi-omics approaches comprising genomics, transcriptomics, proteomics, metabolomics and phenomics integrate studies on the interaction of plants with microbes and their external environment and generate multi-layered information that can answer what is happening in real-time within the cells. Integration, analysis and decipherization of the big-data can lead to a massive outcome that has significant chance for implementation in the fields. This review summarizes abiotic stresses responses in plants in-terms of biochemical and molecular mechanisms followed by the microbe-mediated stress mitigation phenomenon. We describe the role of multi-omics approaches in generating multi-pronged information to provide a better understanding of plant-microbe interactions that modulate cellular mechanisms in plants under extreme external conditions and help to optimize abiotic stresses. Vigilant amalgamation of these high-throughput approaches supports a higher level of knowledge generation about root-level mechanisms involved in the alleviation of abiotic stresses in organisms.
515 citations
Cites background from "Osmotic Stress Responses and Plant ..."
...Therefore, plants have smartly evolved different mechanisms to minimize consumption of optimal water resources and manage their growth till they face adverse conditions (Osakabe et al., 2013)....
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TL;DR: It is argued that cytosolic K(+) content may be considered as one of the 'master switches' enabling plant transition from the normal metabolism to 'hibernated state' during first hours after the stress exposure and then to a recovery phase.
Abstract: Intracellular potassium homeostasis is a prerequisite for the optimal operation of plant metabolic machinery and plant's overall performance. It is controlled by K(+) uptake, efflux and intracellular and long-distance relocation, mediated by a large number of K(+) -selective and non-selective channels and transporters located at both plasma and vacuolar membranes. All abiotic and biotic stresses result in a significant disturbance to intracellular potassium homeostasis. In this work, we discuss molecular mechanisms and messengers mediating potassium transport and homeostasis focusing on four major environmental stresses: salinity, drought, flooding and biotic factors. We argue that cytosolic K(+) content may be considered as one of the 'master switches' enabling plant transition from the normal metabolism to 'hibernated state' during first hours after the stress exposure and then to a recovery phase. We show that all these stresses trigger substantial disturbance to K(+) homeostasis and provoke a feedback control on K(+) channels and transporters expression and post-translational regulation of their activity, optimizing K(+) absorption and usage, and, at the extreme end, assisting the programmed cell death. We discuss specific modes of regulation of the activity of K(+) channels and transporters by membrane voltage, intracellular Ca(2+) , reactive oxygen species, polyamines, phytohormones and gasotransmitters, and link this regulation with plant-adaptive responses to hostile environments.
501 citations
Cites background from "Osmotic Stress Responses and Plant ..."
...KUP6, a high-affinity K+ transporter from the KUP/HAK/KT family, was recently shown to be responsive to the drought stress (Osakabe et al. 2013)....
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...KUP6, a high-affinity K+ transporter from the KUP/HAK/KT family, was recently shown to be responsive to the drought stress (Osakabe et al. 2013)....
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...The protein kinase SNF1related protein kinases 2E (SRK2E), a key component of ABA signaling, interacted with and phosphorylated KUP6, suggesting that KUP functions are regulated directly via an ABA signaling complex (Osakabe et al. 2013)....
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References
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TL;DR: The role of turgor and sensitivity to stress, as well as growth adjustments during and after stress, are studied.
Abstract: OBSERVED RESPONSES TO WATER STRESS....... . . • . • • . . • . . . . • • . • • • • . . . . . • • • • • • • 523 Transpiration and Stomata. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 523 Transpiration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523 Leaf temperature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 524 "Wall" resistance to transpiration.. . . ....... ......... .... . ...... 524 Sensitivity of stomata to stress. .. . . . . . . .. . . . . . . . . . . . . . . . . . . . . . .. 525 Mechanisms of stomatal response..... . . . . . . . . . . . . . . .. . . . . . . . . . .. 526 Aftereffect on stomata . . . . " . . . . .. . . . . . . . . . . . . . . . . . . . . .. . . . . . .. 528 CO, Assimilation in Light.. . . .. .. .. . . . .. .. . . .. . .. . . . . . .. .. . . . . ... 528 At the leaf level. . . . . .. .. . . . . . . .. .. .. .. . . . .. . .. .. .. .. .. .. . .... 528 At the subcellular level. . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 532 Lichens, bryophytes, and ferns. . . . . .. . . .. . . . . . . . . . . . . . . . . . . . . . .. 533 Respiration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 534 Cell Growth and Cell Wal/ Synthesis..... . . .. . . . . . . . . . . . . . . . . . . . . . .. 535 Role of turgor and sensitivity to stress. . . . . . . . . . . . . . . . . . . . . . . . . .. 535 Growth adjustments during and after stress.... . . . . . . . . . . . . . . . . . . .. 537 Root growth and soil mechanical impedance.. . . . . .. . . . . . . . . . . . . . .. 539 Cel/ wall synthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 540 Cel/ Division. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 540 Hormones and Ethylene.. . . . . . . . . . . .. . . .... . ... .... .. . ..... .... ... 541 Cytokinin activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 542 Abscissic acid. . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 542 Ethylene and abscission. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 543 Nitrogen Metabolism...... ........ .. ... . ... . .. .. .... . . .. ..... . . .. 544 Protein synthesis in vegetative tissue. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 544 Protein synthesis in seeds and mosses . . . . . . . . . . . . . . '. . . . . . . . . . . . .. 546 Nucleic acids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 547 Proline and other amino acids.... . . . . . . .. . . . . . . . . . . . . . . . . . . . . . .. 548 Nitrogen fixation. . . . .. . .. .. . .. .. . . . . .. . .. . . . . . .. .. . . . .. .. . . .. 548 Enzyme Levels. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 548
2,923 citations
TL;DR: This review article highlights transcriptional regulation of gene expression in response to drought and cold stresses, with particular emphasis on the role of transcription factors and cis-acting elements in stress-inducible promoters.
Abstract: Plant growth and productivity are greatly affected by environmental stresses such as drought, high salinity, and low temperature. Expression of a variety of genes is induced by these stresses in various plants. The products of these genes function not only in stress tolerance but also in stress response. In the signal transduction network from perception of stress signals to stress-responsive gene expression, various transcription factors and cis-acting elements in the stress-responsive promoters function for plant adaptation to environmental stresses. Recent progress has been made in analyzing the complex cascades of gene expression in drought and cold stress responses, especially in identifying specificity and cross talk in stress signaling. In this review article, we highlight transcriptional regulation of gene expression in response to drought and cold stresses, with particular emphasis on the role of transcription factors and cis-acting elements in stress-inducible promoters.
2,616 citations
"Osmotic Stress Responses and Plant ..." refers background in this paper
...During water deficit stress, osmotic stress sensing and signaling are pivotal to plant water status and lead to rapid changes in gene expression (Yamaguchi-Shinozaki and Shinozaki, 2006; Osakabe et al., 2011) and turgor-dependent stomatal closing, which responds to hydraulic properties in the xylem…...
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...During water deficit stress, osmotic stress sensing and signaling are pivotal to plant water status and lead to rapid changes in gene expression (Yamaguchi-Shinozaki and Shinozaki, 2006; Osakabe et al., 2011) and turgor-dependent stomatal closing, which responds to hydraulic properties in the xylem (Maggio et al....
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Book•
31 Jul 1995
TL;DR: This book is a useful introduction for students, teachers, and investigators in both basic and applied plant science, including botanists, crop scientists, foresters, horticulturists, soil scientists, and even gardeners and farmers who desire a better understanding of how their plants grow.
Abstract: Everyone who grows plants, whether a single geranium in a flower pot or hundreds of acres of corn or cotton, is aware of the importance of water for successful growth. Water supply not only affects the yield of gardens and field crops, but also controls the distribution of plants over the earth's surface, ranging from deserts and grasslands to rain forests, depending on the amount and seasonal distribution of precipitation. However, few people understand 'fully why water is so important for plant growth. This book attempts to explain its importance by showing how water affects the physiological processes that control the quantity and quality of growth. It is a useful introduction for students, teachers, and investigators in both basic and applied plant science, including botanists, crop scientists, foresters, horticulturists, soil scientists, and even gardeners and farmers who desire a better understanding of how their plants grow. An attempt has been made to present the information in terms intelligible to readers with various backgrounds. If the treatment of some topics seems inadequate to specialists in certain fields, they are reminded that the book was not written for specialists, but as an introduction to the broad field of plant water relations. As an aid in this respect, a laboratory manual is available with detailed instructions for some of the more complex methods (J. S. Boyer in "Measuring the Water Status of Plants and Soils," Academic Press, San Diego, 1995).
1,954 citations
"Osmotic Stress Responses and Plant ..." refers background in this paper
...Stomatal aperture is controlled by the water potential in the waterconducting system, and stomatal closing has been suggested to directly respond to the hydraulic properties within the xylem during stress (Kramer and Boyer, 1995; Ache et al., 2010)....
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TL;DR: The implementation of a bimolecular fluorescence complementation technique for visualization of protein-protein interactions in plant cells revealed a remarkable signal fluorescence intensity of interacting protein complexes as well as a high reproducibility and technical simplicity of the method in different plant systems.
Abstract: Dynamic networks of protein-protein interactions regulate numerous cellular processes and determine the ability to respond appropriately to environmental stimuli. However, the investigation of protein complex formation in living plant cells by methods such as fluorescence resonance energy transfer has remained experimentally difficult, time consuming and requires sophisticated technical equipment. Here, we report the implementation of a bimolecular fluorescence complementation (BiFC) technique for visualization of protein-protein interactions in plant cells. This approach relies on the formation of a fluorescent complex by two non-fluorescent fragments of the yellow fluorescent protein brought together by association of interacting proteins fused to these fragments (Hu et al., 2002). To enable BiFC analyses in plant cells, we generated different complementary sets of expression vectors, which enable protein interaction studies in transiently or stably transformed cells. These vectors were used to investigate and visualize homodimerization of the basic leucine zipper (bZIP) transcription factor bZIP63 and the zinc finger protein lesion simulating disease 1 (LSD1) from Arabidopsis as well as the dimer formation of the tobacco 14-3-3 protein T14-3c. The interaction analyses of these model proteins established the feasibility of BiFC analyses for efficient visualization of structurally distinct proteins in different cellular compartments. Our investigations revealed a remarkable signal fluorescence intensity of interacting protein complexes as well as a high reproducibility and technical simplicity of the method in different plant systems. Consequently, the BiFC approach should significantly facilitate the visualization of the subcellular sites of protein interactions under conditions that closely reflect the normal physiological environment.
1,498 citations
"Osmotic Stress Responses and Plant ..." refers methods in this paper
...Agrobacterium was used for infiltration of Nicotiana benthamiana leaves as described previously (Walter et al., 2004)....
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...The full-length cDNAs of KUP6 and SRK2E/OST1 were cloned into 35S-SPYNE and 35S-SPYCE vectors to generate BiFC constructs (Walter et al., 2004)....
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TL;DR: Progress in identification of early stomatal signaling components are reviewed, including ABA receptors and CO(2)-binding response proteins, as well as systems approaches that advance the understanding of guard cell-signaling mechanisms.
Abstract: Stomatal pores are formed by pairs of specialized epidermal guard cells and serve as major gateways for both CO(2) influx into plants from the atmosphere and transpirational water loss of plants. Because they regulate stomatal pore apertures via integration of both endogenous hormonal stimuli and environmental signals, guard cells have been highly developed as a model system to dissect the dynamics and mechanisms of plant-cell signaling. The stress hormone ABA and elevated levels of CO(2) activate complex signaling pathways in guard cells that are mediated by kinases/phosphatases, secondary messengers, and ion channel regulation. Recent research in guard cells has led to a new hypothesis for how plants achieve specificity in intracellular calcium signaling: CO(2) and ABA enhance (prime) the calcium sensitivity of downstream calcium-signaling mechanisms. Recent progress in identification of early stomatal signaling components are reviewed here, including ABA receptors and CO(2)-binding response proteins, as well as systems approaches that advance our understanding of guard cell-signaling mechanisms.
1,169 citations
"Osmotic Stress Responses and Plant ..." refers background in this paper
...ABA induces the activation of outward K+ channels (GORK), resulting in K+ efflux from guard cells, which leads to loss of guard cell turgor and stomatal closing (Hosy et al., 2003; Kim et al., 2010)....
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...Anion and K+ efflux from guard cells leads to loss of guard cell turgor and causes stomatal closing (Schroeder and Hagiwara, 1989; Pei et al., 1997; Ache et al., 2000; Hosy et al., 2003; Kim et al., 2010)....
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