Microsensors in plant biology - in vivo visualization of inorganic analytes with high spatial and/or temporal resolution.

This Expert View provides an update on the recent development of new microsensors, and briefly summarizes some novel applications of existing microsensors, in plant biology research. Two major topics are covered, i) sensors for gaseous analytes (O2, CO2, H2S) and ii) those for measuring concentrations and fluxes of ions (macro- and micronutrients and environmental pollutants such as heavy metals). We show that application of such microsensors may significantly advance understanding of mechanisms of plant-environmental interaction and regulation of plant developmental and adaptive responses under adverse environmental conditions via non-destructive visualization of key analytes with high spatial and/or temporal resolution. Examples included cover a broad range of environmental situations including hypoxia, salinity, and heavy metal toxicity. We highlight the power of combining microsensor technology with other advanced biophysical (patch-clamp; voltage-clamp; single-cell pressure-probe), imaging (MRI; fluorescent dyes) and genetic techniques and approaches. We conclude that future progress in the field may be achieved by applying existing microsensors for important signalling molecules such as NO and H2O2, by improving selectivity of existing microsensors for some key analytes (e.g., Na, Mg and Zn) and by developing new microsensors for P.

[1]  M. Nieves‐Cordones,et al.  Doing 'business as usual' comes with a cost: evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions. , 2020, The New phytologist.

[2]  O. Pedersen,et al.  Lateral roots, in addition to the adventitious roots, form a barrier to radial oxygen loss in Zea nicaraguensis and a chromosome segment introgression line in maize. , 2020, The New phytologist.

[3]  W. Armstrong,et al.  Root O2 consumption, CO2 production and tissue concentration profiles in chickpea, as influenced by environmental hypoxia. , 2019, The New phytologist.

[4]  R. Gutiérrez,et al.  Nitrate and hormonal signaling crosstalk for plant growth and development. , 2019, Current opinion in plant biology.

[5]  H. Meinke,et al.  Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice , 2019, Front. Plant Sci..

[6]  Juan Zhu,et al.  Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance. , 2019, The Plant journal : for cell and molecular biology.

[7]  J. M. Palma,et al.  Nitric oxide (NO) and hydrogen sulfide (H2S) in plants: Which is first? , 2019, Journal of experimental botany.

[8]  S. Shabala,et al.  GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion , 2019, Journal of experimental botany.

[9]  T. Setter,et al.  Tolerance of roots to low oxygen: 'Anoxic' cores, the phytoglobin-nitric oxide cycle, and energy or oxygen sensing. , 2019, Journal of plant physiology.

[10]  G. Bassel,et al.  Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress , 2019, Nature Communications.

[11]  S. Shabala,et al.  Tissue-specific respiratory burst oxidase homolog-dependent H2O2 signaling to the plasma membrane H+-ATPase confers potassium uptake and salinity tolerance in Cucurbitaceae , 2019, Journal of experimental botany.

[12]  Xianchang Yu,et al.  24-Epibrassinolide promotes NO3− and NH4+ ion flux rate and NRT1 gene expression in cucumber under suboptimal root zone temperature , 2019, BMC Plant Biology.

[13]  J. Lohmann,et al.  An apical hypoxic niche sets the pace of shoot meristem activity , 2019, Nature.

[14]  M. Ashikari,et al.  Diel O2 Dynamics in Partially and Completely Submerged Deepwater Rice: Leaf Gas Films Enhance Internodal O2 Status, Influence Gene Expression and Accelerate Stem Elongation for 'Snorkelling' during Submergence. , 2019, Plant & cell physiology.

[15]  A. Polle,et al.  Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net , 2019, The New phytologist.

[16]  K. Gothelf,et al.  Amperometic microsensor for measurement of gaseous and dissolved CO2 , 2019, Sensors and Actuators B: Chemical.

[17]  Qing Liu,et al.  Characteristics of ammonium and nitrate fluxes along the roots of Picea asperata , 2019, Journal of Plant Nutrition.

[18]  A. Salih,et al.  The loss of RBOHD function modulates root adaptive responses to combined hypoxia and salinity stress in Arabidopsis , 2019, Environmental and Experimental Botany.

[19]  Guo-ping Zhang,et al.  Revealing mechanisms of salinity tissue tolerance in succulent halophytes: A case study for Carpobrotus rossi. , 2018, Plant, cell & environment.

[20]  P. Ralph,et al.  Seagrass rhizosphere microenvironment alters plant‐associated microbial community composition , 2018, Environmental microbiology.

[21]  Lijun Wang,et al.  Cell wall-bound silicon optimizes ammonium uptake and metabolism in rice cells , 2018, Annals of botany.

[22]  R. Hedrich,et al.  Spatio-temporal Aspects of Ca2+ Signalling: Lessons from Guard Cells and Pollen Tubes. , 2018, Journal of experimental botany.

[23]  M. Koch,et al.  Hypersalinity as a trigger of seagrass ( Thalassia testudinum ) die-off events in Florida Bay: Evidence based on shoot meristem O 2 and H 2 S dynamics , 2018, Journal of Experimental Marine Biology and Ecology.

[24]  N. Bazihizina,et al.  Na+ extrusion from the cytosol and tissue-specific Na+ sequestration in roots confer differential salt stress tolerance between durum and bread wheat , 2018, Journal of experimental botany.

[25]  N. Revsbech,et al.  CO2 and O2 dynamics in leaves of aquatic plants with C3 or CAM photosynthesis – application of a novel CO2 microsensor , 2018, Annals of botany.

[26]  P. Paira,et al.  Bipyridine bisphosphonate-based fluorescent optical sensor and optode for selective detection of Zn2+ ions and its applications , 2018 .

[27]  F. Baluška,et al.  Boron Alleviates Aluminum Toxicity by Promoting Root Alkalization in Transition Zone via Polar Auxin Transport1[OPEN] , 2018, Plant Physiology.

[28]  Alexander M. Jones,et al.  Genetically Encoded Biosensors in Plants: Pathways to Discovery. , 2018, Annual review of plant biology.

[29]  S. Shabala,et al.  Hydrogen Peroxide-Induced Root Ca2+ and K+ Fluxes Correlate with Salt Tolerance in Cereals: Towards the Cell-Based Phenotyping , 2018, International journal of molecular sciences.

[30]  S. Shabala,et al.  An Anion Conductance, the Essential Component of the Hydroxyl-Radical-Induced Ion Current in Plant Roots , 2018, International journal of molecular sciences.

[31]  Guo-ping Zhang,et al.  The ability to regulate voltage-gated K+-permeable channels in the mature root epidermis is essential for waterlogging tolerance in barley , 2017, Journal of experimental botany.

[32]  K. J. Gupta,et al.  Nitric oxide is essential for the development of aerenchyma in wheat roots under hypoxic stress. , 2017, Plant, cell & environment.

[33]  Fangsen Xu,et al.  Involvement of reactive oxygen species and Ca2+ in the differential responses to low-boron in rapeseed genotypes , 2017, Plant and Soil.

[34]  S. Shabala Signalling by potassium: another second messenger to add to the list? , 2017, Journal of experimental botany.

[35]  Xu Huang,et al.  H2S‐induced gastric fundus smooth muscle tension potentiation is mediated by the phosphoinositide 3‐kinase/Akt/endothelial nitric oxide synthase pathway , 2017, Experimental physiology.

[36]  P. Ralph,et al.  Sediment Resuspension and Deposition on Seagrass Leaves Impedes Internal Plant Aeration and Promotes Phytotoxic H2S Intrusion , 2017, Front. Plant Sci..

[37]  N. von Wirén,et al.  Ammonium as a signal for physiological and morphological responses in plants , 2017, Journal of experimental botany.

[38]  M. Bennett,et al.  Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells , 2017, Proceedings of the National Academy of Sciences.

[39]  A. Polle,et al.  Paxillus involutus-Facilitated Cd2+ Influx through Plasma Membrane Ca2+-Permeable Channels Is Stimulated by H2O2 and H+-ATPase in Ectomycorrhizal Populus × canescens under Cadmium Stress , 2017, Front. Plant Sci..

[40]  U. Roessner,et al.  Cell-Type-Specific H+-ATPase Activity in Root Tissues Enables K+ Retention and Mediates Acclimation of Barley (Hordeum vulgare) to Salinity Stress1[OPEN] , 2016, Plant Physiology.

[41]  A. Salih,et al.  Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis , 2016, Journal of experimental botany.

[42]  M. Kühl,et al.  Development of a rechargeable optical hydrogen peroxide sensor - sensor design and biological application. , 2016, The Analyst.

[43]  Ole Pedersen,et al.  Heat stress of two tropical seagrass species during low tides - impact on underwater net photosynthesis, dark respiration and diel in situ internal aeration. , 2016, The New phytologist.

[44]  Jian Sun,et al.  Extracellular ATP mediates cellular K+/Na+ homeostasis in two contrasting poplar species under NaCl stress , 2016, Trees.

[45]  J. Feijó,et al.  GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters , 2015, Nature Communications.

[46]  Ingo Klimant,et al.  LUMOS - A Sensitive and Reliable Optode System for Measuring Dissolved Oxygen in the Nanomolar Range , 2015, PloS one.

[47]  S. Baldwin,et al.  Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. , 2015, Journal of experimental botany.

[48]  P. Ralph,et al.  Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide. , 2015, The New phytologist.

[49]  G. Loake,et al.  Nitric oxide function in plant biology: a redox cue in deconvolution. , 2014, The New phytologist.

[50]  Zed Rengel,et al.  Improved measurements of Na+ fluxes in plants using calixarene-based microelectrodes. , 2011, Journal of plant physiology.

[51]  Francesco Licausi,et al.  Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. , 2011, The New phytologist.

[52]  Jessica R. Corman,et al.  Sustainability Challenges of Phosphorus and Food: Solutions from Closing the Human Phosphorus Cycle , 2011 .

[53]  A. Sadanandom,et al.  Biosensors in plants. , 2010, Current opinion in plant biology.

[54]  T. Cuin,et al.  Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death , 2010, Journal of Cell Science.

[55]  H. Jensen,et al.  Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme. , 2009 .

[56]  S. Shabala,et al.  SV channels dominate the vacuolar Ca2+ release during intracellular signaling , 2009, FEBS letters.

[57]  M. Koch,et al.  Conceptual model of seagrass die-off in Florida Bay: Links to biogeochemical processes , 2007 .

[58]  T. Ross,et al.  Non-invasive microelectrode ion flux measurements to study adaptive responses of microorganisms to the environment. , 2006, FEMS microbiology reviews.

[59]  Guo-ping Zhang,et al.  Screening plants for salt tolerance by measuring K+ flux: a case study for barley , 2005 .

[60]  Calum R. Wilson,et al.  Plant cell growth and ion flux responses to the streptomycete phytotoxin thaxtomin A: calcium and hydrogen flux patterns revealed by the non-invasive MIFE technique. , 2005, Plant & cell physiology.

[61]  S. Shabala,et al.  Overcoming the Problem of Non-Ideal Liquid Ion Exchanger Selectivity in Microelectrode Ion Flux Measurements , 2004, The Journal of Membrane Biology.

[62]  T. Binzer,et al.  Sulphide intrusion in eelgrass (Zostera marina L.) , 2004 .

[63]  S. Long,et al.  Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. , 2003, Journal of experimental botany.

[64]  N. Kulagina,et al.  Monitoring hydrogen peroxide in the extracellular space of the brain with amperometric microsensors. , 2003, Analytical chemistry.

[65]  R. Lew,et al.  Turgor Regulation in Osmotically Stressed Arabidopsis Epidermal Root Cells. Direct Support for the Role of Inorganic Ion Uptake as Revealed by Concurrent Flux and Cell Turgor Measurements1 , 2002, Plant Physiology.

[66]  N. Revsbech,et al.  An oxygen insensitive microsensor for nitrous oxide , 2001 .

[67]  Sergey Shabala,et al.  Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protoplasts: MIFE meets patch-clamp , 2001 .

[68]  R. Lew,et al.  K^+ transport by Arabidopsis root hairs at low pH , 2001 .

[69]  R. Glud,et al.  Predicting the signal of O2 microsensors from physical dimensions, temperature, salinity, and O2 concentration , 1998 .

[70]  N. Revsbech,et al.  A METHOD TO IMPROVE THE SPATIAL RESOLUTION OF PHOTOSYNTHETIC RATES OBTAINED BY OXYGEN MICROSENSORS , 1998 .

[71]  D. de Beer,et al.  A fast‐responding CO2 microelectrode for profiling sediments, microbial mats, and biofilms , 1997 .

[72]  N. Revsbech,et al.  Macrophyte development and resuspension regulate the photosynthesis and production of benthic microalgae , 1997, Hydrobiologia.

[73]  N. Revsbech,et al.  A microscale biosensor for methane containing methanotrophic bacteria and an internal oxygen reservoir. , 1997, Analytical chemistry.

[74]  S. Shabala,et al.  Oscillations in H+ and Ca2+ Ion Fluxes around the Elongation Region of Corn Roots and Effects of External pH , 1997, Plant physiology.

[75]  D. R. Raman,et al.  Measurement of Net Fluxes of Ammonium and Nitrate at the Surface of Barley Roots Using Ion-Selective Microelectrodes : II. Patterns of Uptake Along the Root Axis and Evaluation of the Microelectrode Flux Estimation Technique. , 1992, Plant physiology.

[76]  B. Jørgensen,et al.  A fibre‐optic scalar irradiance microsensor: application for spectral light measurements in sediments , 1992 .

[77]  N. Revsbech,et al.  An oxygen microsensor with a guard cathode , 1989 .

[78]  J. Severinghaus,et al.  Electrodes for blood pO2 and pCO2 determination. , 1958, Journal of applied physiology.

[79]  M. Kühl,et al.  Strong leaf surface basification and CO2 limitation of seagrass induced by epiphytic biofilm microenvironments. , 2019, Plant, cell & environment.

[80]  A. Majouga,et al.  Prolonged oxygen depletion in microwounded cells of Chara corallina detected with novel O2 nanosensors. , 2019, Journal of experimental botany.

[81]  Susan J. Smith,et al.  Measuring intracellular ion concentrations with multi-barrelled microelectrodes. , 2012, Methods in molecular biology.

[82]  Jian Sun,et al.  Non-invasive flux measurements using microsensors: theory, limitations, and systems. , 2012, Methods in molecular biology.

[83]  I. Ślesak,et al.  The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. , 2007, Acta biochimica Polonica.

[84]  Ingo Klimant,et al.  Optical measurement of oxygen and temperature in microscale: strategies and biological applications , 1997 .