Root hair growth from the pH point of view

Root hairs are tubular outgrowths of epidermal cells that increase the root surface area and thereby make the root more efficient at absorbing water and nutrients. Their expansion is limited to the root hair apex, where growth is reported to take place in a pulsating manner. These growth pulses coincide with oscillations of the apoplastic and cytosolic pH in a similar way as has been reported for pollen tubes. Likewise, the concentrations of apoplastic reactive oxygen species (ROS) and cytoplasmic Ca2+ oscillate with the same periodicity as growth. Whereas ROS appear to control cell wall extensibility and opening of Ca2+ channels, the role of protons as a growth signal in root hairs is less clear and may differ from that in pollen tubes where plasma membrane H+-ATPases have been shown to sustain growth. In this review, we outline our current understanding of how pH contributes to root hair development.

[1]  Hironaka Tsukagoshi,et al.  Reactive Oxygen Species Link Gene Regulatory Networks During Arabidopsis Root Development , 2021, Frontiers in Plant Science.

[2]  J. Bahk,et al.  A temperature-sensitive FERONIA mutant allele that alters root hair growth. , 2021, Plant physiology.

[3]  T. Dandekar,et al.  An optimized genetically encoded dual reporter for simultaneous ratio imaging of Ca2+ and H+ reveals new insights into ion signaling in plants , 2021, The New phytologist.

[4]  D. Becher,et al.  A conserved cysteine near the P-site is accessible to cysteine modifications and increases ROS stability in P-type plasma membrane H+-ATPase. , 2021, The Biochemical journal.

[5]  J. Estevez,et al.  Highlighting reactive oxygen species as multitaskers in root development , 2020, iScience.

[6]  F. Baluška,et al.  Root-Apex Proton Fluxes at the Centre of Soil-Stress Acclimation. , 2020, Trends in plant science.

[7]  J. Feijó,et al.  Plasma membrane H+-ATPases sustain pollen tube growth and fertilization , 2020, Nature Communications.

[8]  G. Muday,et al.  Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis , 2020, Development.

[9]  J. Estevez,et al.  The RALF1-FERONIA complex phosphorylates eIF4E1 to promote protein synthesis and polar root hair growth. , 2020, Molecular plant.

[10]  Y. Xiang,et al.  Actin Cytoskeleton as Actor in Upstream and Downstream of Calcium Signaling in Plant Cells , 2019, International journal of molecular sciences.

[11]  G. Muday,et al.  RBOH-Dependent ROS Synthesis and ROS Scavenging by Plant Specialized Metabolites To Modulate Plant Development and Stress Responses. , 2019, Chemical research in toxicology.

[12]  M. Palmgren,et al.  Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana , 2018, Physiologia plantarum.

[13]  G. Muday,et al.  Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress , 2018, Proceedings of the National Academy of Sciences.

[14]  R. Morris,et al.  Cellular Ca2+ Signals Generate Defined pH Signatures in Plants[OPEN] , 2018, Plant Cell.

[15]  S. Karpiński,et al.  Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses , 2018, Free radical biology & medicine.

[16]  J. Estevez,et al.  How Does pH Fit in with Oscillating Polar Growth? , 2018, Trends in plant science.

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

[18]  Qiangsheng Wu,et al.  Reactive Oxygen Species Signaling and Root Hair Development , 2017 .

[19]  S. Tyerman,et al.  Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. , 2017, Plant, cell & environment.

[20]  Yiyong Zhu,et al.  Arabidopsis plasma membrane H+-ATPase genes AHA2 and AHA7 have distinct and overlapping roles in the modulation of root tip H+ efflux in response to low-phosphorus stress , 2017, Journal of experimental botany.

[21]  K. Meng,et al.  Isolation and Characterization of Two Persimmon Xyloglucan Endotransglycosylase/Hydrolase (XTH) Genes That Have Divergent Functions in Cell Wall Modification and Fruit Postharvest Softening , 2016, Front. Plant Sci..

[22]  M. Palmgren,et al.  Plasma Membrane H(+)-ATPase Regulation in the Center of Plant Physiology. , 2016, Molecular plant.

[23]  K. Vissenberg,et al.  Cell Fate Determination and the Switch from Diffuse Growth to Planar Polarity in Arabidopsis Root Epidermal Cells , 2015, Front. Plant Sci..

[24]  A. Fuglsang,et al.  The plasma membrane H(+) -ATPase AHA2 contributes to the root architecture in response to different nitrogen supply. , 2015, Physiologia plantarum.

[25]  S. Persson,et al.  Root hair growth: it's a one way street , 2015, F1000prime reports.

[26]  Kathleen T DiNapoli,et al.  The anthocyanin reduced Tomato Mutant Demonstrates the Role of Flavonols in Tomato Lateral Root and Root Hair Development1[W][OPEN] , 2014, Plant Physiology.

[27]  F. Sánchez,et al.  Actin polymerization drives polar growth in Arabidopsis root hair cells , 2014, Plant signaling & behavior.

[28]  C. Douglas,et al.  Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis , 2014, Scientific Reports.

[29]  Guozeng Zhang,et al.  A Receptor-Like Kinase Mediates Ammonium Homeostasis and Is Important for the Polar Growth of Root Hairs in Arabidopsis[W] , 2014, Plant Cell.

[30]  M. Sussman,et al.  A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion , 2014, Science.

[31]  T. Ketelaar.  The actin cytoskeleton in root hairs: all is fine at the tip. , 2013, Current opinion in plant biology.

[32]  Wenfeng Li,et al.  Mapping gene activity of Arabidopsis root hairs , 2013, Genome Biology.

[33]  W. York,et al.  A Galacturonic Acid–Containing Xyloglucan Is Involved in Arabidopsis Root Hair Tip Growth[W] , 2012, Plant Cell.

[34]  K. Keegstra,et al.  Mutations in Multiple XXT Genes of Arabidopsis Reveal the Complexity of Xyloglucan Biosynthesis1[W][OA] , 2012, Plant Physiology.

[35]  Herman Höfte,et al.  Cell wall mechanics and growth control in plants: the role of pectins revisited , 2012, Front. Plant Sci..

[36]  F. Guo,et al.  A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells , 2011, Nature Cell Biology.

[37]  L. Dolan,et al.  Root hairs: development, growth and evolution at the plant-soil interface , 2011, Plant and Soil.

[38]  A. Bacic,et al.  O-Glycosylated Cell Wall Proteins Are Essential in Root Hair Growth , 2011, Science.

[39]  G. Wasteneys,et al.  Root hair-specific disruption of cellulose and xyloglucan in AtCSLD3 mutants, and factors affecting the post-rupture resumption of mutant root hair growth , 2011, Planta.

[40]  W. Nasser,et al.  Biochemical Properties of Pectate Lyases Produced by Three Different Bacillus Strains Isolated from Fermenting Cocoa Beans and Characterization of Their Cloned Genes , 2010, Applied and Environmental Microbiology.

[41]  Yuxian Zhu,et al.  Comparative Proteomics Indicates That Biosynthesis of Pectic Precursors Is Important for Cotton Fiber and Arabidopsis Root Hair Elongation* , 2010, Molecular & Cellular Proteomics.

[42]  C. Ringli.  Monitoring the Outside: Cell Wall-Sensing Mechanisms1[C] , 2010, Plant Physiology.

[43]  L. Dolan,et al.  A basic helix-loop-helix transcription factor controls cell growth and size in root hairs , 2010, Nature Genetics.

[44]  W. Schmidt,et al.  Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. , 2009, The New phytologist.

[45]  A. S. Raghavendra,et al.  Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan , 2009, Plant signaling & behavior.

[46]  Hyung-Taeg Cho,et al.  cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis1[C][W][OA] , 2009, Plant Physiology.

[47]  L. Cárdenas.  New findings in the mechanisms regulating polar growth in root hair cells , 2009, Plant signaling & behavior.

[48]  S. Gilroy,et al.  Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis1[W][OA] , 2008, Plant Physiology.

[49]  J. Rodríguez-León,et al.  Exclusion of a Proton ATPase from the Apical Membrane Is Associated with Cell Polarity and Tip Growth in Nicotiana tabacum Pollen Tubes[W] , 2008, The Plant Cell Online.

[50]  S. Gilroy,et al.  Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs , 2007, Proceedings of the National Academy of Sciences.

[51]  Grégoire M. Hummel,et al.  NaRALF, a peptide signal essential for the regulation of root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. , 2007, The Plant journal : for cell and molecular biology.

[52]  Jian-Kang Zhu,et al.  Arabidopsis Protein Kinase PKS5 Inhibits the Plasma Membrane H+-ATPase by Preventing Interaction with 14-3-3 Protein , 2007, The Plant Cell Online.

[53]  Zhenbiao Yang,et al.  NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. , 2007, Journal of experimental botany.

[54]  P. Hussey,et al.  Oscillatory Increases in Alkalinity Anticipate Growth and May Regulate Actin Dynamics in Pollen Tubes of Lily[W][OA] , 2006, The Plant Cell Online.

[55]  M. Blatt,et al.  Membrane trafficking and polar growth in root hairs and pollen tubes. , 2006, Journal of experimental botany.

[56]  V. Citovsky,et al.  Pollen-specific pectin methylesterase involved in pollen tube growth. , 2006, Developmental biology.

[57]  I. Szarejko,et al.  Molecular Cloning and Characterization of β-Expansin Gene Related to Root Hair Formation in Barley1 , 2006, Plant Physiology.

[58]  M. Galway.  Root hair cell walls: filling in the frameworkThis review is one of a selection of papers published in the Special Issue on Plant Cell Biology. , 2006 .

[59]  I. Lorenzen,et al.  A novel fluorescent pH probe for expression in plants , 2006, Plant Methods.

[60]  W. Schmidt,et al.  Environmentally Induced Plasticity of Root Hair Development in Arabidopsis1 , 2004, Plant Physiology.

[61]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[62]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[63]  D. Cosgrove,et al.  Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006437. , 2002, The Plant Cell Online.

[64]  L. Vidali,et al.  The Regulation of Actin Organization by Actin-Depolymerizing Factor in Elongating Pollen Tubes Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003038. , 2002, The Plant Cell Online.

[65]  Ying Fu,et al.  The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root Hair Initiation and Tip Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010359. , 2002, The Plant Cell Online.

[66]  S. Gilroy,et al.  Root Hair Development , 2002, Journal of Plant Growth Regulation.

[67]  J. Verbelen,et al.  Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. , 2001, Plant physiology.

[68]  M. Palmgren.  PLANT PLASMA MEMBRANE H+-ATPases: Powerhouses for Nutrient Uptake. , 2001, Annual review of plant physiology and plant molecular biology.

[69]  E. Blancaflor,et al.  Changes in Root Cap pH Are Required for the Gravity Response of the Arabidopsis Root , 2001, Plant Cell.

[70]  A. Emons,et al.  Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. , 2000, Molecular plant-microbe interactions : MPMI.

[71]  M. Braun,et al.  Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. , 2000, Developmental biology.

[72]  W. Schmidt,et al.  Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. , 2000, Plant physiology.

[73]  C. Bernhardt,et al.  Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. , 2000, Plant physiology.

[74]  B. Jakob,et al.  pH and buffer capacities of apoplastic and cytoplasmic cell compartments in leaves , 1999, Planta.

[75]  M. Boutry,et al.  Expression analysis of two gene subfamilies encoding the plasma membrane H+-ATPase in Nicotiana plumbaginifolia reveals the major transport functions of this enzyme. , 1999, The Plant journal : for cell and molecular biology.

[76]  S J Remington,et al.  Structural and spectral response of green fluorescent protein variants to changes in pH. , 1999, Biochemistry.

[77]  J. Feijó,et al.  Growing Pollen Tubes Possess a Constitutive Alkaline Band in the Clear Zone and a Growth-dependent Acidic Tip , 1999, The Journal of cell biology.

[78]  S. Gilroy,et al.  Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. , 1998, Development.

[79]  Gero Miesenböck,et al.  Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins , 1998, Nature.

[80]  F. Sánchez,et al.  Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals , 1998, Plant physiology.

[81]  D. Prasher,et al.  Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[82]  J. Lynch,et al.  Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability , 1996 .

[83]  J. Schiefelbein,et al.  The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. , 1996, Development.

[84]  B. Regenberg,et al.  C-terminal deletion analysis of plant plasma membrane H(+)-ATPase: yeast as a model system for solute transport across the plant plasma membrane. , 1995, The Plant cell.

[85]  Claire S. Grierson,et al.  Clonal relationships and cell patterning in the root epidermis of Arabidopsis , 1994 .

[86]  K. VandenBosch,et al.  Secretion of cell wall polysaccharides in Vicia root hairs , 1994 .

[87]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[88]  S. McQueen-Mason,et al.  Two endogenous proteins that induce cell wall extension in plants. , 1992, The Plant cell.

[89]  M. Sussman,et al.  The Arabidopsis thaliana plasma membrane H(+)-ATPase multigene family. Genomic sequence and expression of a third isoform. , 1990, The Journal of biological chemistry.

[90]  R. Cleland,et al.  Calcium and the mechanical properties of soybean hypocotyl cell walls: Possible role of calcium and protons in cell-wall loosening , 1988, Planta.

[91]  M L Graber,et al.  Characteristics of fluoroprobes for measuring intracellular pH. , 1986, Analytical biochemistry.

[92]  H. Sze.  H+‐translocating ATPases of the plasma membrane and tonoplast of plant cells , 1984 .

[93]  R. M. Spanswick,et al.  Effects of vanadate on the plasma membrane ATPase of red beet and corn. , 1984, Plant physiology.

[94]  R. M. Spanswick,et al.  Characterization of the Electrogenicity of Soybean (Glycine max L.) Roots : ATP Dependence and Effect of ATPase Inhibitors. , 1984, Plant physiology.

[95]  L. Jaffe,et al.  Natural H Currents Traverse Growing Roots and Root Hairs of Barley (Hordeum vulgare L.). , 1979, Plant physiology.

[96]  R. Warner,et al.  Vanadate is a potent (Na,K)-ATPase inhibitor found in ATP derived from muscle. , 1977, The Journal of biological chemistry.

[97]  Masahito Hayashi,et al.  A conserved, buried cysteine near the P-site is accessible to cysteine modifications and increases ROS stability in the P-type plasma membrane H-ATPase , 2021 .

[98]  OUP accepted manuscript , 2021, Plant Physiology.

[99]  K. Vissenberg,et al.  Molecular Mechanisms Regulating Root Hair Tip Growth: A Comparison with Pollen Tubes , 2017 .

[100]  T. Kakimoto,et al.  Pathways involved in vanadate-induced root hair formation in Arabidopsis. , 2015, Physiologia plantarum.

[101]  P. Várnai,et al.  Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. , 2013, The New phytologist.

[102]  N. Smirnoff,et al.  Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[103]  J. Schiefelbein,et al.  Growth and ultrastructure ofArabidopsis root hairs: therhd3 mutation alters vacuole enlargement and tip growth , 2005, Planta.

[104]  Rod A. Wing,et al.  Molecular and genetic characterization of two pollen-expressed genes that have sequence similarity to pectate lyases of the plant pathogen Erwinia , 2004, Plant Molecular Biology.

[105]  C. Grierson,et al.  Root Hairs , 2002, The arabidopsis book.

[106]  J. Foreman,et al.  KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. , 2001, Genes & development.