Accepted Manuscript Title: Sensing and transport of nutrients in plants Author: Guohua Xu PII: DOI: Reference:
S1084-9521(17)30501-3 http://dx.doi.org/10.1016/j.semcdb.2017.09.020 YSCDB 2386
To appear in:
Seminars in Cell & Developmental Biology
Please cite this article as: Xu Guohua.Sensing and transport of nutrients in plants.Seminars in Cell and Developmental Biology http://dx.doi.org/10.1016/j.semcdb.2017.09.020 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Special Issue: Sensing and transport of nutrients in plants
Guohua Xu Nanjing Agricultural University, State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Science, Nanjing, 210095, China. Email: [email protected]
Plants are rooted to the place where they germinate or are transplanted. As sessile organisms, plants are heavily relied on the soil where they are growing for getting nutrients and water. The nutrient concentration and buffering capacity of supply in soils with different texture and fertility are variable and affected by soil management. For example, both soluble nitrate (NO3-) and potassium ion (K+) concentrations can vary by four orders of magnitude from the micro-molar to milli-molar range in soils. Thus, plants have developed complex sensing and regulatory systems for optimizing nutrient acquisition, distribution and assimilation in order to adapt to the fluctuating environments. In addition, the majority (probably about 80%) of terrestrial plant species are capable of interacting with arbuscular mycorrhizal (AM) fungi which have coevolved with their host roots for over 450 million years in nature. The major advantage of the AM symbiosis for plants in acquiring nutrients is the extended absorption area by AM fungi hyphae in soil. In early 1960s Emanual Epestein and colleagues discovered a “biphasic pattern” of K+ uptake by barley roots and proposed the two K+ uptake mechanisms working simultaneously at the plasma membrane [1]. Since then, it has been characterized that there are both high affinity transport system (HATS) and low affinity transport system (LATS) not only for the major nutrients but also for some micro-nutrients in a number of plant species. During the past two decades, rapid progresses have been made in understanding the molecular mechanisms of sensing and transport of the major nutrients in plants. The transport proteins embedded within membranes are the key targets for improving the nutrient and water uptake and use efficiency [2]. Some plasma membrane transporters in plants like Arabidopsis NPF6.3 (NRT1.1) display dual functions as a nitrate transceptor, i.e., not only as nitrate transporter but also nitrate receptor for sensing the concentrations of nitrate in external environment [3]. 1
In this special issue of Seminars in Cell and Developmental Biology, the experts have illustrated the transport properties and sensing and/or regulatory roles of four major nutrients, nitrogen (N), phosphorus (P), K and magnesium (Mg) in plants. Nitrogen in its various inorganic and organic forms is a critical component for sustaining life on Earth. Unlike other mineral nutrients in soils which are derived from rocks, N that is being taken up by plants is certainly from atmosphere and converted via biological processes in soil. The formation of AM symbiosis is considered to be one of the most promising strategies evolved by plants for coping with limited supply of nutrients, particularly inorganic phosphate (Pi), while an increasing number of studies have revealed that plants can also take up substantial amounts of N through the mycorrhizal pathway. However, no integrated review has been published previously in international journal for the transport and regulation of N in AM symbiosis. In this special issue, Chen et al summarize the current understanding of N transport properties in both AM fungi side and plant root side of the AM association. They overview the transport systems acting putatively in transfer of N from soil to fungal cells, N assimilation and translocation in fungal hyphae, the N releasing from fungi to peri-arbuscular apoplast and further to colonized cortical cells of plant roots. They also discuss the feedback mechanisms of N status and N interplay with carbohydrates and P in modulating AM symbiosis. It has been known for a long time that inorganic N utilization by plants is finely regulated by highly sophisticated signaling pathways, activated by sensing of both external N availability and internal N status of the whole plant [4]. Nitrate is the dominant form of N acquired by the plants grown in aerobic neutral and alkaline soils. In addition, nitrate also acts as an important signaling molecule in vital physiological processes for optimum growth and development. Surya Kant illustrates the current understanding of NO3- uptake, transport, relocation and remobilization of its assimilates, regulation of root growth and their relationship with plant nitrogen use efficiency (NUE). Plett et al summarize the key transporters and regulators mediating NO3- uptake in plant roots at both mature tissue and tip regions. Both papers highlight the plant responses to altered NO3- supply at transcriptional and translational levels, in particular, the involvement of microRNAs in NO3- signaling. Plett et al have also identified three major gaps in the knowledge discovered in Arabidopsis plant for the development of high NUE cereal crops. Amino acids are the constituents of proteins and precursors of important secondary metabolites. Besides nitrate, amino acids are the main form of N transported between the plant organs and the transport process is mediated by membrane amino acid transporters. Dinkeloo et al describe the updated functions of amino acid transporters in facilitating amino acids across intracellular membranes and movement from source leaves to sink organs, particularly during seed filling and fruit development. They show the amino 2
acid transporters as targets for crop improvement and resistance to pathogen. In addition, they have discussed and proposed the potential receptors and transceptors as amino acids sensors in plants. Phosphorus is a structural component of nucleic acids and phospholipids and plays critical roles in energy transfer, signal transduction, and enzymatic activation. Plant roots are commonly experiencing limited supply of soluble Pi due to both chemical and biological fixation and extremely low mobility of Pi in natural soil environment. Thus, plants have evolved complex mechanisms of Pi transport and signaling to cope with low Pi availability [5]. Taking the data mainly from both dicot Arabidopsis and monocot rice crop, Wang et al summarize the latest advances in the understanding of the molecular mechanisms of Pi sensing, uptake and allocation, as well as Pi signaling in plants. They illustrate the key members of Pi transporters (i.e. PHT families, SPX-EXS and SPX-MFS families and SULTR-like transporters), the basic mechanism of sensing both external and internal Pi status, the regulation of Pi signaling in transcriptional, post-transcriptional and post-translational levels. They propose the potential biotechnological applications of known genes including Pi-related transcription factors, Pi transporters, and their interacting proteins to develop Pi use efficient cultivars. SIZ1 is a small ubiquitin-like modifier E3 ligase and plays a broad role in the post-translational sumoylation of proteins. Datta et al review the progresses made so far regarding the regulatory influences of SIZ1 on Pi deficiency-mediated responses, namely possible change of Pi distribution and concentration, and several morphophysiological and molecular traits that govern Pi homeostasis in plants. Authors have also analyzed the potential sumoylation sites by bioinformatics and proposed applications of high throughput state-of-the-art technologies for identifying the sumoylation targets involved in plant Pi homeostasis. Potassium is the most abundant cation in plant cells to maintain electrical charge balance. It is involved in transport of nitrate and sugar in addition to act as an important osmoticum. To maintain a high and stable K+ concentration (about 100-150 mM) in the cytosol, plants have developed at least five K + transporter families (i.e., Shaker-like and tandem-pore K+ channels, HAK/KUP/KT K+ transporters, HKT transporters, cation-proton antiporters) and a delicate regulatory mechanism fine-tuning the maintenance of K+ homeostasis in different plant tissues. The HAK/KUP/KT transporters were first identified in plants 20 years ago and have been widely associated with K+ transport across membranes in bacteria, fungi and plants. However, there was no comprehensive review on these plant K+ transporters during the past decade. Li et al summarize the common and specific roles of the transporters from different plant species in K+ acquisition, translocation, salt tolerance and osmotic regulation, in particular, the K+ independent regulation of root morphology and shoot phenotype. They illustrate the expression regulation of 3
HAK/KUP/KT transporters at both transcriptional and post-translational levels and their implications in K+ sensing and signaling. Finally, they highlight the potential involvement of HAK/KUP/KT K+ transporters in the complex K+ signaling pathways, K+ compartmentation to vacuolar and other intracellular organs, balancing the transport of counter-anions, particularly nitrate, and the re-distribution of K+ into specific tissues at late plant developmental stages. Magnesium is the second most abundant cation in plant cytosol and plays critical roles in a number of physiological and biochemical process, particularly the leaf photosynthesis. Plants grown in acidic soils are easily subjected to Mg deficiency due to leaching of Mg2+ by intensive rainfall and saturation of H+, Al3+ and Mn2+. Relative to the frequent and excellent review of the progresses in dissecting the physiological and molecular mechanisms in efficient use of N, P and K nutrients, few reviews on plant Mg nutritional biology can be found in literature. Chen et al have summarized the advances in understanding of the transport systems for Mg2+ uptake, storage and translocation in relation to Mg functions in phytosynthesis, carbon allocation, protein synthesis and energy metabolism, as well as in responses to the stresses of Al3+ toxicity, salinity, and Mg2+ toxicity. Current studies are commonly focusing on the specific responses of plants to the deficiency or excess of individual nutrients. However, the nutrient sensing has been shown to be affected by multiple external factors which act as local signals to trigger systemic signaling coordinated by long-distance mobile signals [4]. To maximize nutrient acquisition and use efficiency, plants may trigger a single signaling event governing the transport of several nutrients. One common plant response to severe nutrient stresses is the increased production of reactive oxygen species (ROS) in various intracellular compartments which operates upstream of the key transporters for maintaining the homeostasis of the nutrients in different plant cells. In Arabidopsis, CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE23 (CIPK23) has been identified as a nutrient regulatory hub involved in K +, NO3- and NH4+ nutrition. CIPK23 can activate the K+ channel AKT1 [6] and a high affinity K+ transporter HAK5 [7], but inhibit NH4+ transporters (AMT1.1 and AMT1.2) [8]. CIPK23 can also phosphorylate nitrate transporter NPF6.3 (NRT1.1 or CHL1) for shifting the transporter affinity with nitrate [3]. These findings highlight the key roles of such central regulator(s) in sensing nutrient availability and controlling nutrient homeostasis, which may determine the nutrient use efficiency in plants. We thank all of the authors and reviewers for their contributions toward this issue, and we hope that readers will find the articles to be informative and stimulating.
References 4
[1] E. Epstein, D.W. Rains, O.E. Elzam, Resolution of dual mechanisms of potassium absorption by barley roots, Proc. Natl. Acad. Sci. USA, 49(1963) 684-692. [2] J.I. Schroeder, E. Delhaize, W.B. Frommer, M. Guerinot, M.J. Harrison, et al. Using membrane transporters to improve crops for sustainable food production, Nature 497 (2013) 60–66 [3] C.H. Ho, S.H. Lin, H.C. Hu, Y.F. Tsay, CHL1 functions as a nitrate sensor in plants, Cell, 138(2009) 1184-1194 [4] W. Xuan, T. Beeckman, G.H. Xu, Plan nitrogen nutrition: sensing and signaling, Curr. Opin. Plant Biol. 39(2017) 57-65. [5] M. Gu, A.Q. Chen, S.B. Sun, G.H. Xu, Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: What Is missing? Mol. Plant, 9(2016) 396-416. [6] J. Xu, H. Li, L. Chen, Y. Wang, L. Liu, L. He, W. Wu, A protein kinase, interacting with two Calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis, Cell, 125 (2006) 1347-1360. [7] P. Ragel, R. Ródenas, E. García-Martín, Z. Andrés, I. Villalta, M. Nieves-Cordones, R.M. Rivero, V. Martínez, J.M. Pardo, F.J. Quintero, F. Rubio, The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K+ Uptake in Arabidopsis Roots. Plant Physiol. 169(2015) 2863-73. [8] T. Straub, U. Ludewig, B. Neuhäuser, The kinase CIPK23 inhibits ammonium transport in Arabidopsis thaliana. Plant Cell, 29(2017) 409-422.
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S1084-9521(17)30501-3 http://dx.doi.org/10.1016/j.semcdb.2017.09.020 YSCDB 2386
To appear in:
Seminars in Cell & Developmental Biology
Please cite this article as: Xu Guohua.Sensing and transport of nutrients in plants.Seminars in Cell and Developmental Biology http://dx.doi.org/10.1016/j.semcdb.2017.09.020 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Special Issue: Sensing and transport of nutrients in plants
Guohua Xu Nanjing Agricultural University, State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Science, Nanjing, 210095, China. Email: [email protected]
Plants are rooted to the place where they germinate or are transplanted. As sessile organisms, plants are heavily relied on the soil where they are growing for getting nutrients and water. The nutrient concentration and buffering capacity of supply in soils with different texture and fertility are variable and affected by soil management. For example, both soluble nitrate (NO3-) and potassium ion (K+) concentrations can vary by four orders of magnitude from the micro-molar to milli-molar range in soils. Thus, plants have developed complex sensing and regulatory systems for optimizing nutrient acquisition, distribution and assimilation in order to adapt to the fluctuating environments. In addition, the majority (probably about 80%) of terrestrial plant species are capable of interacting with arbuscular mycorrhizal (AM) fungi which have coevolved with their host roots for over 450 million years in nature. The major advantage of the AM symbiosis for plants in acquiring nutrients is the extended absorption area by AM fungi hyphae in soil. In early 1960s Emanual Epestein and colleagues discovered a “biphasic pattern” of K+ uptake by barley roots and proposed the two K+ uptake mechanisms working simultaneously at the plasma membrane [1]. Since then, it has been characterized that there are both high affinity transport system (HATS) and low affinity transport system (LATS) not only for the major nutrients but also for some micro-nutrients in a number of plant species. During the past two decades, rapid progresses have been made in understanding the molecular mechanisms of sensing and transport of the major nutrients in plants. The transport proteins embedded within membranes are the key targets for improving the nutrient and water uptake and use efficiency [2]. Some plasma membrane transporters in plants like Arabidopsis NPF6.3 (NRT1.1) display dual functions as a nitrate transceptor, i.e., not only as nitrate transporter but also nitrate receptor for sensing the concentrations of nitrate in external environment [3]. 1
In this special issue of Seminars in Cell and Developmental Biology, the experts have illustrated the transport properties and sensing and/or regulatory roles of four major nutrients, nitrogen (N), phosphorus (P), K and magnesium (Mg) in plants. Nitrogen in its various inorganic and organic forms is a critical component for sustaining life on Earth. Unlike other mineral nutrients in soils which are derived from rocks, N that is being taken up by plants is certainly from atmosphere and converted via biological processes in soil. The formation of AM symbiosis is considered to be one of the most promising strategies evolved by plants for coping with limited supply of nutrients, particularly inorganic phosphate (Pi), while an increasing number of studies have revealed that plants can also take up substantial amounts of N through the mycorrhizal pathway. However, no integrated review has been published previously in international journal for the transport and regulation of N in AM symbiosis. In this special issue, Chen et al summarize the current understanding of N transport properties in both AM fungi side and plant root side of the AM association. They overview the transport systems acting putatively in transfer of N from soil to fungal cells, N assimilation and translocation in fungal hyphae, the N releasing from fungi to peri-arbuscular apoplast and further to colonized cortical cells of plant roots. They also discuss the feedback mechanisms of N status and N interplay with carbohydrates and P in modulating AM symbiosis. It has been known for a long time that inorganic N utilization by plants is finely regulated by highly sophisticated signaling pathways, activated by sensing of both external N availability and internal N status of the whole plant [4]. Nitrate is the dominant form of N acquired by the plants grown in aerobic neutral and alkaline soils. In addition, nitrate also acts as an important signaling molecule in vital physiological processes for optimum growth and development. Surya Kant illustrates the current understanding of NO3- uptake, transport, relocation and remobilization of its assimilates, regulation of root growth and their relationship with plant nitrogen use efficiency (NUE). Plett et al summarize the key transporters and regulators mediating NO3- uptake in plant roots at both mature tissue and tip regions. Both papers highlight the plant responses to altered NO3- supply at transcriptional and translational levels, in particular, the involvement of microRNAs in NO3- signaling. Plett et al have also identified three major gaps in the knowledge discovered in Arabidopsis plant for the development of high NUE cereal crops. Amino acids are the constituents of proteins and precursors of important secondary metabolites. Besides nitrate, amino acids are the main form of N transported between the plant organs and the transport process is mediated by membrane amino acid transporters. Dinkeloo et al describe the updated functions of amino acid transporters in facilitating amino acids across intracellular membranes and movement from source leaves to sink organs, particularly during seed filling and fruit development. They show the amino 2
acid transporters as targets for crop improvement and resistance to pathogen. In addition, they have discussed and proposed the potential receptors and transceptors as amino acids sensors in plants. Phosphorus is a structural component of nucleic acids and phospholipids and plays critical roles in energy transfer, signal transduction, and enzymatic activation. Plant roots are commonly experiencing limited supply of soluble Pi due to both chemical and biological fixation and extremely low mobility of Pi in natural soil environment. Thus, plants have evolved complex mechanisms of Pi transport and signaling to cope with low Pi availability [5]. Taking the data mainly from both dicot Arabidopsis and monocot rice crop, Wang et al summarize the latest advances in the understanding of the molecular mechanisms of Pi sensing, uptake and allocation, as well as Pi signaling in plants. They illustrate the key members of Pi transporters (i.e. PHT families, SPX-EXS and SPX-MFS families and SULTR-like transporters), the basic mechanism of sensing both external and internal Pi status, the regulation of Pi signaling in transcriptional, post-transcriptional and post-translational levels. They propose the potential biotechnological applications of known genes including Pi-related transcription factors, Pi transporters, and their interacting proteins to develop Pi use efficient cultivars. SIZ1 is a small ubiquitin-like modifier E3 ligase and plays a broad role in the post-translational sumoylation of proteins. Datta et al review the progresses made so far regarding the regulatory influences of SIZ1 on Pi deficiency-mediated responses, namely possible change of Pi distribution and concentration, and several morphophysiological and molecular traits that govern Pi homeostasis in plants. Authors have also analyzed the potential sumoylation sites by bioinformatics and proposed applications of high throughput state-of-the-art technologies for identifying the sumoylation targets involved in plant Pi homeostasis. Potassium is the most abundant cation in plant cells to maintain electrical charge balance. It is involved in transport of nitrate and sugar in addition to act as an important osmoticum. To maintain a high and stable K+ concentration (about 100-150 mM) in the cytosol, plants have developed at least five K + transporter families (i.e., Shaker-like and tandem-pore K+ channels, HAK/KUP/KT K+ transporters, HKT transporters, cation-proton antiporters) and a delicate regulatory mechanism fine-tuning the maintenance of K+ homeostasis in different plant tissues. The HAK/KUP/KT transporters were first identified in plants 20 years ago and have been widely associated with K+ transport across membranes in bacteria, fungi and plants. However, there was no comprehensive review on these plant K+ transporters during the past decade. Li et al summarize the common and specific roles of the transporters from different plant species in K+ acquisition, translocation, salt tolerance and osmotic regulation, in particular, the K+ independent regulation of root morphology and shoot phenotype. They illustrate the expression regulation of 3
HAK/KUP/KT transporters at both transcriptional and post-translational levels and their implications in K+ sensing and signaling. Finally, they highlight the potential involvement of HAK/KUP/KT K+ transporters in the complex K+ signaling pathways, K+ compartmentation to vacuolar and other intracellular organs, balancing the transport of counter-anions, particularly nitrate, and the re-distribution of K+ into specific tissues at late plant developmental stages. Magnesium is the second most abundant cation in plant cytosol and plays critical roles in a number of physiological and biochemical process, particularly the leaf photosynthesis. Plants grown in acidic soils are easily subjected to Mg deficiency due to leaching of Mg2+ by intensive rainfall and saturation of H+, Al3+ and Mn2+. Relative to the frequent and excellent review of the progresses in dissecting the physiological and molecular mechanisms in efficient use of N, P and K nutrients, few reviews on plant Mg nutritional biology can be found in literature. Chen et al have summarized the advances in understanding of the transport systems for Mg2+ uptake, storage and translocation in relation to Mg functions in phytosynthesis, carbon allocation, protein synthesis and energy metabolism, as well as in responses to the stresses of Al3+ toxicity, salinity, and Mg2+ toxicity. Current studies are commonly focusing on the specific responses of plants to the deficiency or excess of individual nutrients. However, the nutrient sensing has been shown to be affected by multiple external factors which act as local signals to trigger systemic signaling coordinated by long-distance mobile signals [4]. To maximize nutrient acquisition and use efficiency, plants may trigger a single signaling event governing the transport of several nutrients. One common plant response to severe nutrient stresses is the increased production of reactive oxygen species (ROS) in various intracellular compartments which operates upstream of the key transporters for maintaining the homeostasis of the nutrients in different plant cells. In Arabidopsis, CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE23 (CIPK23) has been identified as a nutrient regulatory hub involved in K +, NO3- and NH4+ nutrition. CIPK23 can activate the K+ channel AKT1 [6] and a high affinity K+ transporter HAK5 [7], but inhibit NH4+ transporters (AMT1.1 and AMT1.2) [8]. CIPK23 can also phosphorylate nitrate transporter NPF6.3 (NRT1.1 or CHL1) for shifting the transporter affinity with nitrate [3]. These findings highlight the key roles of such central regulator(s) in sensing nutrient availability and controlling nutrient homeostasis, which may determine the nutrient use efficiency in plants. We thank all of the authors and reviewers for their contributions toward this issue, and we hope that readers will find the articles to be informative and stimulating.
References 4
[1] E. Epstein, D.W. Rains, O.E. Elzam, Resolution of dual mechanisms of potassium absorption by barley roots, Proc. Natl. Acad. Sci. USA, 49(1963) 684-692. [2] J.I. Schroeder, E. Delhaize, W.B. Frommer, M. Guerinot, M.J. Harrison, et al. Using membrane transporters to improve crops for sustainable food production, Nature 497 (2013) 60–66 [3] C.H. Ho, S.H. Lin, H.C. Hu, Y.F. Tsay, CHL1 functions as a nitrate sensor in plants, Cell, 138(2009) 1184-1194 [4] W. Xuan, T. Beeckman, G.H. Xu, Plan nitrogen nutrition: sensing and signaling, Curr. Opin. Plant Biol. 39(2017) 57-65. [5] M. Gu, A.Q. Chen, S.B. Sun, G.H. Xu, Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: What Is missing? Mol. Plant, 9(2016) 396-416. [6] J. Xu, H. Li, L. Chen, Y. Wang, L. Liu, L. He, W. Wu, A protein kinase, interacting with two Calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis, Cell, 125 (2006) 1347-1360. [7] P. Ragel, R. Ródenas, E. García-Martín, Z. Andrés, I. Villalta, M. Nieves-Cordones, R.M. Rivero, V. Martínez, J.M. Pardo, F.J. Quintero, F. Rubio, The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K+ Uptake in Arabidopsis Roots. Plant Physiol. 169(2015) 2863-73. [8] T. Straub, U. Ludewig, B. Neuhäuser, The kinase CIPK23 inhibits ammonium transport in Arabidopsis thaliana. Plant Cell, 29(2017) 409-422.
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