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Ion Transport and Homeostasis in Plants

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 October 2020) | Viewed by 44165

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Dr. Ryoung Shin

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Guest Editor

RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan
Interests: plant nutrients; transporter; ion channels; abiotic stress; phytoremediation; marine macroalgae
Special Issues, Collections and Topics in MDPI journals

Dr. Nobuyuki Uozumi

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Guest Editor

Department of Biomolecular Engineering, Tohoku University Sendai 980-8579, Japan
Interests: membrane transport system; drought stress; salinity stress; ion channel, proton motive force
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Ion transport by ion channels and transporters is an essential mechanism in maintaining the life of all living organisms and is required for nutrient uptake, responding to external and internal stimuli, and ion homeostasis in plants. Ion homeostasis is a critical regulatory mechanism for many fundamental processes, such as maintaining electroneutrality, controlling turgor pressure, membrane potential cell volume, and ion movements across the plasma membrane and organella membrane. Understanding ion transport and homeostasis is, therefore, crucially important and gets attention as one of the major research topics today. This Special Issue will shed light on the mechanisms of ion transport activities via ion channels/transporters and of ion homeostasis in plants. We warmly welcome submissions, including original research papers and reviews, on this topic.

Dr. Ryoung Shin
Dr. Nobuyuki Uozumi
Guest Editors

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Keywords

Transporter
Ion channel
Nutrient uptake
Ion homeostasis
Membrane potential

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Published Papers (11 papers)

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Research

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17 pages, 2793 KiB

Open AccessArticle

Syringic Acid Alleviates Cesium-Induced Growth Defect in Arabidopsis

by Eri Adams, Takae Miyazaki, Ju Yeon Moon, Yuji Sawada, Muneo Sato, Kiminori Toyooka, Masami Yokota Hirai and Ryoung Shin

Int. J. Mol. Sci. 2020, 21(23), 9116; https://doi.org/10.3390/ijms21239116 - 30 Nov 2020

Cited by 8 | Viewed by 3096

Abstract

Syringic acid, a phenolic compound, serves a variety of beneficial functions in cells. Syringic acid increases in plants in response to cesium, and exogenous application of syringic acid resulted in a significant attenuation of cesium-induced growth defects in Arabidopsis. In addition, cesium or syringic acid application to plants also resulted in increased lignin deposition in interfascicular fibers. To better understand the role of lignin and syringic acid in attenuating cesium-induced growth defects, two mutants for Arabidopsis REDUCED EPIDERMAL FLUORESCENE 4 (REF4) and fourteen laccase mutants, some of which have lower levels of lignin, were evaluated for their response to cesium. These mutants responded differently to cesium stress, compared to control plants, and the application of syringic acid alleviated cesium-induced growth defects in the laccase mutants but not in the ref4 mutants. These findings imply that lignin plays a role in cesium signaling but the attenuation of cesium stress defects by syringic acid is mediated by regulatory components of lignin biosynthesis and not lignin biosynthesis itself. In contrast, syringic acid did not alleviate any low potassium-induced growth defects. Collectively, our findings provide the first established link between lignin and cesium stress via syringic acid in plants. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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16 pages, 5477 KiB

Open AccessArticle

Transcriptome Analysis of Pyrus betulaefolia Seedling Root Responses to Short-Term Potassium Deficiency

by Han Yang, Yan Li, Yumeng Jin, Liping Kan, Changwei Shen, Anish Malladi, Savithri Nambeesan, Yangchun Xu and Caixia Dong

Int. J. Mol. Sci. 2020, 21(22), 8857; https://doi.org/10.3390/ijms21228857 - 23 Nov 2020

Cited by 17 | Viewed by 2964

Abstract

Potassium (K) plays a crucial role in multiple physiological and developmental processes in plants. Its deficiency is a common abiotic stress that inhibits plant growth and reduces crop productivity. A better understanding of the mechanisms involved in plant responses to low K could help to improve the efficiency of K use in plants. However, such responses remain poorly characterized in fruit tree species such as pears (Pyrus sp). We analyzed the physiological and transcriptome responses of a commonly used pear rootstock, Pyrus betulaefolia, to K-deficiency stress (0 mM). Potassium deprivation resulted in apparent changes in root morphology, with short-term low-K stress resulting in rapidly enhanced root growth. Transcriptome analyses indicated that the root transcriptome was coordinately altered within 6 h after K deprivation, a process that continued until 15 d after treatment. Potassium deprivation resulted in the enhanced expression (up to 5-fold) of a putative high-affinity K⁺ transporter, PbHAK5 (Pbr037826.1), suggesting the up-regulation of mechanisms associated with K⁺ acquisition. The enhanced root growth in response to K-deficiency stress was associated with a rapid and sustained decrease in the expression of a transcription factor, PbMYB44 (Pbr015309.1), potentially involved in mediating auxin responses, and the increased expression of multiple genes associated with regulating root growth. The concentrations of several phytohormones including indoleacetic acid (IAA), ABA, ETH, gibberellin (GA₃), and jasmonic acid (JA) were higher in response to K deprivation. Furthermore, genes coding for enzymes associated with carbon metabolism such as SORBITOL DEHYDROGENASE (SDH) and SUCROSE SYNTHASE (SUS) displayed greatly enhanced expression in the roots under K deprivation, presumably indicating enhanced metabolism to meet the increased energy demands for growth and K⁺ acquisition. Together, these data suggest that K deprivation in P. betulaefolia results in the rapid re-programming of the transcriptome to enhance root growth and K⁺ acquisition. These data provide key insights into the molecular basis for understanding low-K-tolerance mechanisms in pears and in other related fruit trees and identifying potential candidates that warrant further analyses. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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17 pages, 4496 KiB

Open AccessArticle

Genome-Wide Analysis of the Five Phosphate Transporter Families in Camelina sativa and Their Expressions in Response to Low-P

by Dhondup Lhamo, Qiaolin Shao, Renjie Tang and Sheng Luan

Int. J. Mol. Sci. 2020, 21(21), 8365; https://doi.org/10.3390/ijms21218365 - 7 Nov 2020

Cited by 10 | Viewed by 2781

Abstract

Phosphate transporters (PHTs) play pivotal roles in phosphate (Pi) acquisition from the soil and distribution throughout a plant. However, there is no comprehensive genomic analysis of the PHT families in Camelina sativa, an emerging oilseed crop. In this study, we identified 73 CsPHT members belonging to the five major PHT families. A whole-genome triplication event was the major driving force for CsPHT expansion, with three homoeologs for each Arabidopsis ortholog. In addition, tandem gene duplications on chromosome 11, 18 and 20 further enlarged the CsPHT1 family beyond the ploidy norm. Phylogenetic analysis showed clustering of the CsPHT1 and CsPHT4 family members into four distinct groups, while CsPHT3s and CsPHT5s were clustered into two distinct groups. Promoter analysis revealed widespread cis-elements for low-P response (P1BS) specifically in CsPHT1s, consistent with their function in Pi acquisition and translocation. In silico RNA-seq analysis revealed more ubiquitous expression of several CsPHT1 genes in various tissues, whereas CsPHT2s and CsPHT4s displayed preferential expression in leaves. While several CsPHT3s were expressed in germinating seeds, most CsPHT5s were expressed in floral and seed organs. Suneson, a popular Camelina variety, displayed better tolerance to low-P than another variety, CS-CROO, which could be attributed to the higher expression of several CsPHT1/3/4/5 family genes in shoots and roots. This study represents the first effort in characterizing CsPHT transporters in Camelina, a promising polyploid oilseed crop that is highly tolerant to abiotic stress and low-nutrient status, and may populate marginal soils for biofuel production. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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18 pages, 2096 KiB

Open AccessArticle

Calcium Plays a Double-Edged Role in Modulating Cadmium Uptake and Translocation in Rice

by Shuo Zhang, Qi Li, Muhammad Mudassir Nazir, Shafaqat Ali, Younan Ouyang, Shuzhen Ye and Fanrong Zeng

Int. J. Mol. Sci. 2020, 21(21), 8058; https://doi.org/10.3390/ijms21218058 - 29 Oct 2020

Cited by 45 | Viewed by 3338

Abstract

Cadmium (Cd) contamination in soils poses great risks to both agricultural production and human health. Calcium (Ca) is an essential element playing a significant role in protecting plants against Cd toxicity. However, how Ca affects Cd uptake and translocation in rice is still not fully elucidated. In this study, the regulatory role of Ca in Cd uptake and upward translocation was investigated in rice at different growth stages. Our results showed that the supplement of 5 mM Ca significantly reduced Cd uptake by rice roots, because of their competition for Ca-permeable channels as an absorption site and Ca-induced downregulation of OsNRAMP1 and OsNRAMP5. However, Ca application facilitated the upward translocation of Cd by both upregulating OsHMA2 to induce xylem loading of Cd and downregulating OsHMA3 to reduce vacuolar sequestration of Cd. Such contrary results suggested a double-edged role of Ca in regulating root Cd uptake and root-to-shoot Cd translocation in rice. Although it increased Cd content in the aboveground vegetative tissues during the whole growth period, the addition of 5 mM Ca eventually decreased Cd content in rice grains at the ripening stage. All these results suggest that Ca-based amendments possess great potential for the production of low-Cd rice grains. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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15 pages, 2942 KiB

Open AccessArticle

Histone Deacetylase Inhibitor SAHA Improves High Salinity Tolerance Associated with Hyperacetylation-Enhancing Expression of Ion Homeostasis-Related Genes in Cotton

by Shibin He, Yunfei Hao, Qi Zhang, Penghui Zhang, Fengfeng Ji, Hui Cheng, Dong Lv, Yanfeng Sun, Fushun Hao and Chen Miao

Int. J. Mol. Sci. 2020, 21(19), 7105; https://doi.org/10.3390/ijms21197105 - 26 Sep 2020

Cited by 9 | Viewed by 2729

Abstract

Histone acetylation plays an important role in regulation of chromatin structure and gene expression in terms of responding to abiotic stresses. Histone acetylation is modulated by histone deacetylases (HDACs) and histone acetyltransferases. Recently, the effectiveness of HDAC inhibitors (HDACis) for conferring plant salt tolerance has been reported. However, the role of HDACis in cotton has not been elucidated. In the present study, we assessed the effects of the HDACi suberoylanilide hydroxamic acid (SAHA) during high salinity stress in cotton. We demonstrated that 10 μM SAHA pretreatment could rescue of cotton from 250 mM NaCl stress, accompanied with reduced Na⁺ accumulation and a strong expression of the ion homeostasis-related genes. Western blotting and immunostaining results revealed that SAHA pretreatment could induce global hyperacetylation of histone H3 at lysine 9 (H3K9) and histone H4 at lysine 5 (H4K5) under 250 mM NaCl stress, indicating that SAHA could act as the HDACi in cotton. Chromatin immunoprecipitation and chromatin accessibility coupled with real time quantitative PCR analyses showed that the upregulation of the ion homeostasis-related genes was associated with the elevated acetylation levels of H3K9 and H4K5 and increased chromatin accessibility on the promoter regions of these genes. Our results could provide a theoretical basis for analyzing the mechanism of HDACi application on salt tolerance in plants. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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15 pages, 6464 KiB

Open AccessArticle

Halophytic Hordeum brevisubulatum HbHAK1 Facilitates Potassium Retention and Contributes to Salt Tolerance

by Haiwen Zhang, Wen Xiao, Wenwen Yu, Ying Jiang and Ruifen Li

Int. J. Mol. Sci. 2020, 21(15), 5292; https://doi.org/10.3390/ijms21155292 - 25 Jul 2020

Cited by 15 | Viewed by 2610

Abstract

Potassium retention under saline conditions has emerged as an important determinant for salt tolerance in plants. Halophytic Hordeum brevisubulatum evolves better strategies to retain K⁺ to improve high-salt tolerance. Hence, uncovering K⁺-efficient uptake under salt stress is vital for understanding K⁺ homeostasis. HAK/KUP/KT transporters play important roles in promoting K⁺ uptake during multiple stresses. Here, we obtained nine salt-induced HAK/KUP/KT members in H. brevisubulatum with different expression patterns compared with H. vulgare through transcriptomic analysis. One member HbHAK1 showed high-affinity K⁺ transporter activity in athak5 to cope with low-K⁺ or salt stresses. The expression of HbHAK1 in yeast Cy162 strains exhibited strong activities in K⁺ uptake under extremely low external K⁺ conditions and reducing Na⁺ toxicity to maintain the survival of yeast cells under high-salt-stress. Comparing with the sequence of barley HvHAK1, we found that C170 and R342 in a conserved domain played pivotal roles in K⁺ selectivity under extremely low-K⁺ conditions (10 μM) and that A13 was responsible for the salt tolerance. Our findings revealed the mechanism of HbHAK1 for K⁺ accumulation and the significant natural adaptive sites for HAK1 activity, highlighting the potential value for crops to promote K⁺-uptake under stresses. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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15 pages, 2934 KiB

Open AccessArticle

Changes in Expression Level of OsHKT1;5 Alters Activity of Membrane Transporters Involved in K⁺ and Ca²⁺ Acquisition and Homeostasis in Salinized Rice Roots

by Mohammad Alnayef, Celymar Solis, Lana Shabala, Takaaki Ogura, Zhonghua Chen, Jayakumar Bose, Frans J. M. Maathuis, Gayatri Venkataraman, Keitaro Tanoi, Min Yu, Meixue Zhou, Tomoaki Horie and Sergey Shabala

Int. J. Mol. Sci. 2020, 21(14), 4882; https://doi.org/10.3390/ijms21144882 - 10 Jul 2020

Cited by 28 | Viewed by 4310

Abstract

In rice, the OsHKT1;5 gene has been reported to be a critical determinant of salt tolerance. This gene is harbored by the SKC1 locus, and its role was attributed to Na⁺ unloading from the xylem. No direct evidence, however, was provided in previous studies. Also, the reported function of SKC1 on the loading and delivery of K⁺ to the shoot remains to be explained. In this work, we used an electrophysiological approach to compare the kinetics of Na⁺ uptake by root xylem parenchyma cells using wild type (WT) and NIL(SKC1) plants. Our data showed that Na⁺ reabsorption was observed in WT, but not NIL(SKC1) plants, thus questioning the functional role of HKT1;5 as a transporter operating in the direct Na⁺ removal from the xylem. Instead, changes in the expression level of HKT1;5 altered the activity of membrane transporters involved in K⁺ and Ca²⁺ acquisition and homeostasis in the rice epidermis and stele, explaining the observed phenotype. We conclude that the role of HKT1;5 in plant salinity tolerance cannot be attributed to merely reducing Na⁺ concentration in the xylem sap but triggers a complex feedback regulation of activities of other transporters involved in the maintenance of plant ionic homeostasis and signaling under stress conditions. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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25 pages, 4112 KiB

Open AccessArticle

Genome-Wide Identification of Metal Tolerance Protein Genes in Populus trichocarpa and Their Roles in Response to Various Heavy Metal Stresses

by Yongfeng Gao, Fengming Yang, Jikai Liu, Wang Xie, Lin Zhang, Zihao Chen, Zhuoxi Peng, Yongbin Ou and Yinan Yao

Int. J. Mol. Sci. 2020, 21(5), 1680; https://doi.org/10.3390/ijms21051680 - 29 Feb 2020

Cited by 52 | Viewed by 4316

Abstract

Metal tolerance proteins (MTPs) are plant divalent cation transporters that play important roles in plant metal tolerance and homeostasis. Poplar is an ideal candidate for the phytoremediation of heavy metals because of its numerous beneficial attributes. However, the definitive phylogeny and heavy metal transport mechanisms of the MTP family in poplar remain unknown. Here, 22 MTP genes in P. trichocarpa were identified and classified into three major clusters and seven groups according to phylogenetic relationships. An evolutionary analysis suggested that PtrMTP genes had undergone gene expansion through tandem or segmental duplication events. Moreover, all PtrMTPs were predicted to localize in the vacuole and/or cell membrane, and contained typical structural features of the MTP family, cation efflux domain. The temporal and spatial expression pattern analysis results indicated the involvement of PtrMTP genes in poplar developmental control. Under heavy metal stress, most of PtrMTP genes were induced by at least two metal ions in roots, stems or leaves. In addition, PtrMTP8.1, PtrMTP9 and PtrMTP10.4 displayed the ability of Mn transport in yeast cells, and PtrMTP6 could transport Co, Fe and Mn. These findings will provide an important foundation to elucidate the biological functions of PtrMTP genes, and especially their role in regulating heavy metal tolerance in poplar. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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Review

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14 pages, 1089 KiB

Open AccessReview

Diverse Physiological Functions of Cation Proton Antiporters across Bacteria and Plant Cells

by Masaru Tsujii, Ellen Tanudjaja and Nobuyuki Uozumi

Int. J. Mol. Sci. 2020, 21(12), 4566; https://doi.org/10.3390/ijms21124566 - 26 Jun 2020

Cited by 25 | Viewed by 5667

Abstract

Membrane intrinsic transport systems play an important role in maintaining ion and pH homeostasis and forming the proton motive force in the cytoplasm and cell organelles. In most organisms, cation/proton antiporters (CPAs) mediate the exchange of K⁺, Na⁺ and Ca²⁺ for H⁺ across the membrane in response to a variety of environmental stimuli. The tertiary structure of the ion selective filter and the regulatory domains of Escherichia coli CPAs have been determined and a molecular mechanism of cation exchange has been proposed. Due to symbiogenesis, CPAs localized in mitochondria and chloroplasts of eukaryotic cells resemble prokaryotic CPAs. CPAs primarily contribute to keeping cytoplasmic Na⁺ concentrations low and controlling pH, which promotes the detoxification of electrophiles and formation of proton motive force across the membrane. CPAs in cyanobacteria and chloroplasts are regulators of photosynthesis and are essential for adaptation to high light or osmotic stress. CPAs in organellar membranes and in the plasma membrane also participate in various intracellular signal transduction pathways. This review discusses recent advances in our understanding of the role of CPAs in cyanobacteria and plant cells. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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21 pages, 480 KiB

Open AccessReview

Function and Regulation of Ammonium Transporters in Plants

by Dong-Li Hao, Jin-Yan Zhou, Shun-Ying Yang, Wei Qi, Ke-Jun Yang and Yan-Hua Su

Int. J. Mol. Sci. 2020, 21(10), 3557; https://doi.org/10.3390/ijms21103557 - 18 May 2020

Cited by 71 | Viewed by 6173

Abstract

Ammonium transporter (AMT)-mediated acquisition of ammonium nitrogen from soils is essential for the nitrogen demand of plants, especially for those plants growing in flooded or acidic soils where ammonium is dominant. Recent advances show that AMTs additionally participate in many other physiological processes such as transporting ammonium from symbiotic fungi to plants, transporting ammonium from roots to shoots, transferring ammonium in leaves and reproductive organs, or facilitating resistance to plant diseases via ammonium transport. Besides being a transporter, several AMTs are required for the root development upon ammonium exposure. To avoid the adverse effects of inadequate or excessive intake of ammonium nitrogen on plant growth and development, activities of AMTs are fine-tuned not only at the transcriptional level by the participation of at least four transcription factors, but also at protein level by phosphorylation, pH, endocytosis, and heterotrimerization. Despite these progresses, it is worth noting that stronger growth inhibition, not facilitation, unfortunately occurs when AMT overexpression lines are exposed to optimal or slightly excessive ammonium. This implies that a long road remains towards overcoming potential limiting factors and achieving AMT-facilitated yield increase to accomplish the goal of persistent yield increase under the present high nitrogen input mode in agriculture. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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16 pages, 2422 KiB

Open AccessReview

The Molecular Mechanisms Underlying Iron Deficiency Responses in Rice

by Qian Li, Lei Chen and An Yang

Int. J. Mol. Sci. 2020, 21(1), 43; https://doi.org/10.3390/ijms21010043 - 19 Dec 2019

Cited by 41 | Viewed by 5363

Abstract

Iron (Fe) is an essential element required for plant growth and development. Under Fe-deficientconditions, plants have developed two distinct strategies (designated as strategy I and II) to acquire Fe from soil. As a graminaceous species, rice is not a typical strategy II plant, as it not only synthesizes DMA (2’-deoxymugineic acid) in roots to chelate Fe³⁺ but also acquires Fe²⁺ through transporters OsIRT1 and OsIRT2. During the synthesis of DMA in rice, there are three sequential enzymatic reactions catalyzed by enzymes NAS (nicotianamine synthase), NAAT (nicotianamine aminotransferase), and DMAS (deoxymugineic acid synthase). Many transporters required for Fe uptake from the rhizosphere and internal translocation have also been identified in rice. In addition, the signaling networks composed of various transcription factors (such as IDEF1, IDEF2, and members of the bHLH (basic helix-loop-helix) family), phytohormones, and signaling molecules are demonstrated to regulate Fe uptake and translocation. This knowledge greatly contributes to our understanding of the molecular mechanisms underlying iron deficiency responses in rice. Full article

(This article belongs to the Special Issue Ion Transport and Homeostasis in Plants)

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