Sensitive To Proton Rhizotoxicity1 Regulates Salt and Drought Tolerance of Arabidopsis thaliana Through Transcriptional Regulation of CIPK23.

The transcription factor sensitive to proton rhizotoxicity 1 (STOP1) regulates multiple stress tolerances. In this study, we confirmed its involvement in NaCl and drought tolerance. The root growth of the T-DNA insertion mutant of STOP1 (stop1) was sensitive to NaCl-containing solidified MS media. Transcriptome analysis of stop1 under NaCl stress revealed that STOP1 regulates several genes related to salt tolerance, including CIPK23. Among all available homozygous T-DNA insertion mutants of the genes suppressed in stop1, only cipk23 showed a NaCl-sensitive root growth phenotype comparable to stop1. The CIPK23 promoter had a functional STOP1-binding site, suggesting a strong CIPK23 suppression led to NaCl sensitivity of stop1. This possibility was supported by in planta complementation of CIPK23 in the stop1 background, which rescued the short root phenotype under NaCl. Both stop1 and cipk23 exhibited a drought tolerant phenotype and increased ABA-regulated stomatal closure, while the complementation of CIPK23 in stop1 reversed these traits. Our findings uncover additional pleiotropic roles of STOP1 mediated by CIPK23 which regulates various ion transporters including those regulating K+-homeostasis, which may induce a trade-off between drought tolerance and other traits.

[1]  J. Lynch.  Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. , 2019, The New phytologist.

[2]  S. Iuchi,et al.  STOP1 regulates the expression of HsfA2 and GDH genes critical for low-oxygen tolerance in Arabidopsis. , 2019, Journal of experimental botany.

[3]  Yoshiharu Y. Yamamoto,et al.  Characterization of NtSTOP1-regulating genes in tobacco under aluminum stress , 2019, Soil Science and Plant Nutrition.

[4]  J. Wasaki,et al.  Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminum tolerance, and recruiting beneficial rhizobacteria , 2018, Soil Science and Plant Nutrition.

[5]  M. Bemer,et al.  The SAUR gene family: the plant's toolbox for adaptation of growth and development. , 2018, Journal of experimental botany.

[6]  Jian-Min Zhou,et al.  Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. , 2018, Journal of integrative plant biology.

[7]  G. Vert,et al.  Metal Sensing by the IRT1 Transporter-Receptor Orchestrates Its Own Degradation and Plant Metal Nutrition. , 2018, Molecular cell.

[8]  Zaib-un-Nisa,et al.  Genome-wide analysis and expression profiling of PP2C clade D under saline and alkali stresses in wild soybean and Arabidopsis , 2017, Protoplasma.

[9]  L. Kochian,et al.  Identification and characterization of suppressor mutants of stop1 , 2017, BMC Plant Biology.

[10]  J. Pellequer,et al.  Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation , 2017, Nature Communications.

[11]  U. Ludewig,et al.  The Kinase CIPK23 Inhibits Ammonium Transport in Arabidopsis thaliana , 2017, Plant Cell.

[12]  J. Botto,et al.  The Multifaceted Roles of HY5 in Plant Growth and Development. , 2016, Molecular plant.

[13]  Mathew G. Lewsey,et al.  Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape , 2016, Cell.

[14]  Y. Bao,et al.  Role of Arabidopsis NHL family in ABA and stress response , 2016, Plant signaling & behavior.

[15]  Ziding Zhang,et al.  AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis1[OPEN] , 2016, Plant Physiology.

[16]  M. Osaki,et al.  Application of ionomics to plant and soil in fields under long-term fertilizer trials , 2015, SpringerPlus.

[17]  Paula Ragel,et al.  The CBL-Interacting Protein Kinase CIPK23 Regulates HAK5-Mediated High-Affinity K+ Uptake in Arabidopsis Roots1[OPEN] , 2015, Plant Physiology.

[18]  L. Xiong,et al.  General mechanisms of drought response and their application in drought resistance improvement in plants , 2015, Cellular and Molecular Life Sciences.

[19]  S. Iuchi,et al.  SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and Other Transcription Factors Are Involved in ALUMINUM-ACTIVATED MALATE TRANSPORTER1 Expression1[OPEN] , 2015, Plant Physiology.

[20]  Miguel González-Guzmán,et al.  A mechanism of growth inhibition by abscisic acid in germinating seeds of Arabidopsis thaliana based on inhibition of plasma membrane H+-ATPase and decreased cytosolic pH, K+, and anions , 2014, Journal of experimental botany.

[21]  K. Nam,et al.  A subset of Arabidopsis RAV transcription factors modulates drought and salt stress responses independent of ABA. , 2014, Plant & cell physiology.

[22]  S. Iuchi,et al.  VuDREB2A, a novel DREB2-type transcription factor in the drought-tolerant legume cowpea, mediates DRE-dependent expression of stress-responsive genes and confers enhanced drought resistance in transgenic Arabidopsis , 2014, Planta.

[23]  S. Iuchi,et al.  STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. , 2014, Molecular plant.

[24]  H. Ohta,et al.  Molecular and Physiological Analysis of Al3+ and H+ Rhizotoxicities at Moderately Acidic Conditions1[W][OPEN] , 2013, Plant Physiology.

[25]  Rainer Hedrich,et al.  Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs). , 2013, Molecular plant.

[26]  I. Szarejko,et al.  Towards the Identification of New Genes Involved in ABA-Dependent Abiotic Stresses Using Arabidopsis Suppressor Mutants of abh1 Hypersensitivity to ABA during Seed Germination , 2013, International journal of molecular sciences.

[27]  S. Iuchi,et al.  Characterization of AtSTOP1 Orthologous Genes in Tobacco and Other Plant Species1[W][OPEN] , 2013, Plant Physiology.

[28]  Shiwei Guo,et al.  The Critical Role of Potassium in Plant Stress Response , 2013, International journal of molecular sciences.

[29]  K. Shinozaki,et al.  Osmotic Stress Responses and Plant Growth Controlled by Potassium Transporters in Arabidopsis[C][W] , 2013, Plant Cell.

[30]  Yanming Zhu,et al.  AtPP2CG1, a protein phosphatase 2C, positively regulates salt tolerance of Arabidopsis in abscisic acid-dependent manner. , 2012, Biochemical and biophysical research communications.

[31]  D. Yun,et al.  Phosphorylation by AtMPK6 is required for the biological function of AtMYB41 in Arabidopsis. , 2012, Biochemical and biophysical research communications.

[32]  K. Shinozaki,et al.  AP2/ERF family transcription factors in plant abiotic stress responses. , 2012, Biochimica et biophysica acta.

[33]  M. Nieves‐Cordones,et al.  Disruption of the Arabidopsis thaliana inward-rectifier K+ channel AKT1 improves plant responses to water stress. , 2012, Plant & cell physiology.

[34]  N. Yamaji,et al.  Identification of a Cis-Acting Element of ART1, a C2H2-Type Zinc-Finger Transcription Factor for Aluminum Tolerance in Rice1[OA] , 2011, Plant Physiology.

[35]  Hiroyuki Koyama,et al.  Prediction of transcriptional regulatory elements for plant hormone responses based on microarray data , 2011, BMC Plant Biology.

[36]  J. M. Pardo,et al.  How do vacuolar NHX exchangers function in plant salt tolerance? , 2010, Plant signaling & behavior.

[37]  Peng-ling Wang,et al.  The surface charge density of plant cell membranes (σ): an attempt to resolve conflicting values for intrinsic σ , 2010, Journal of experimental botany.

[38]  J. Schroeder,et al.  High-Affinity K+ Transport in Arabidopsis: AtHAK5 and AKT1 Are Vital for Seedling Establishment and Postgermination Growth under Low-Potassium Conditions1[C][W][OA] , 2010, Plant Physiology.

[39]  M. Nieves‐Cordones,et al.  The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. , 2010, Molecular plant.

[40]  Y. Tsay,et al.  CHL1 Functions as a Nitrate Sensor in Plants , 2009, Cell.

[41]  M. Nieves‐Cordones,et al.  Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions , 2009 .

[42]  N. Sakurai,et al.  STOP1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities1[C][W][OA] , 2009, Plant Physiology.

[43]  W. Scheible,et al.  AtMyb41 Regulates Transcriptional and Metabolic Responses to Osmotic Stress in Arabidopsis[W][OA] , 2009, Plant Physiology.

[44]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[45]  S. Iuchi,et al.  Amino Acid Polymorphisms in Strictly Conserved Domains of a P-Type ATPase HMA5 Are Involved in the Mechanism of Copper Tolerance Variation in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[46]  T. Cuin,et al.  Potassium transport and plant salt tolerance. , 2008, Physiologia plantarum.

[47]  J. Schroeder,et al.  Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool , 2008, Plant Methods.

[48]  Yong Hwa Cheong,et al.  Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[49]  Rongmin Zhao,et al.  Expression of a Constitutively Activated Plasma Membrane H+-ATPase Alters Plant Development and Increases Salt Tolerance1[C][OA] , 2007, Plant Physiology.

[50]  K. Shinozaki,et al.  Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance , 2007, Proceedings of the National Academy of Sciences.

[51]  Yong Hwa Cheong,et al.  CIPK9: a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis , 2007, Cell Research.

[52]  Wei-Hua Wu,et al.  A Protein Kinase, Interacting with Two Calcineurin B-like Proteins, Regulates K+ Transporter AKT1 in Arabidopsis , 2006, Cell.

[53]  L. Kochian,et al.  AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[54]  R. Bressan,et al.  Uncoupling the Effects of Abscisic Acid on Plant Growth and Water Relations. Analysis of sto1/nced3, an Abscisic Acid-Deficient but Salt Stress-Tolerant Mutant in Arabidopsis1 , 2004, Plant Physiology.

[55]  E. Spalding,et al.  Protection of Plasma Membrane K+ Transport by the Salt Overly Sensitive1 Na+-H+ Antiporter during Salinity Stress1 , 2004, Plant Physiology.

[56]  Heribert Hirt,et al.  Plant PP2C phosphatases: emerging functions in stress signaling. , 2004, Trends in plant science.

[57]  Jian-Kang Zhu,et al.  Regulation of Ion Homeostasis under Salt Stress , 2015 .

[58]  T. Mitchell-Olds,et al.  Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits , 2003, Molecular ecology.

[59]  K. Shinozaki,et al.  Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. , 2001, The Plant journal : for cell and molecular biology.

[60]  R. Hedrich,et al.  KAT1 is not essential for stomatal opening , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[61]  H. Shi,et al.  The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[62]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[63]  E. Macrobbie,et al.  Signal transduction and ion channels in guard cells. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[64]  K. Shinozaki,et al.  Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis , 1998, Plant Cell.

[65]  K. Sakano.  Revision of Biochemical pH-Stat: Involvement of Alternative Pathway Metabolisms , 1998 .

[66]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .

[67]  S. Ok,et al.  CML10, a variant of calmodulin, modulates ascorbic acid synthesis. , 2016, The New phytologist.

[68]  A. Rodríguez-Navarro,et al.  Salt intolerance in Arabidopsis: shoot and root sodium toxicity, and inhibition by sodium-plus-potassium overaccumulation , 2015, Planta.

[69]  Paula Ragel,et al.  CIPK23 regulates HAK5-mediated high-affinity K + uptake in 1 Arabidopsis roots 2 , 2015 .

[70]  C. Tonelli,et al.  Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. , 2008, The Plant journal : for cell and molecular biology.