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The enigma of environmental pH sensing in plants

Nature Plants volume 7, pages 106–115 (2021)Cite this article

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Abstract

Environmental pH is a critical parameter for innumerable chemical reactions, myriad biological processes and all forms of life. The mechanisms that underlie the perception of external pH (pHe) have been elucidated in detail for bacteria, fungi and mammalian cells; however, little information is available on whether and, if so, how pHe is perceived by plants. This is particularly surprising since hydrogen ion activity of the substrate is of paramount significance for plants, governing the availability of mineral nutrients, the structure of the soil microbiome and the composition of natural plant communities. Rapid changes in soil pH require constant readjustment of nutrient acquisition strategies, which is associated with dynamic alterations in gene expression. Referring to observations made in diverse experimental set-ups that unambiguously show that pHe per se affects gene expression, we hypothesize that sensing of pHe in plants is mandatory to prioritize responses to various simultaneously received environmental cues.

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Fig. 1: Factors that determine soil pH and effects of soil pH on plants.
Fig. 2: pH sensing in bacteria.
Fig. 3: pH sensing in eukaryotes.
Fig. 4: Acid-activated KIR channels in plants.
Fig. 5: Environmental pH modulates the biosynthesis of catecholic coumarins.
Fig. 6: Signature pH values of plant organelles.

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References

  1. Gregory, P. J. & Hinsinger, P. New approaches to studying chemical and physical changes in the rhizosphere: an overview. Plant Soil 211, 1–9 (1999).

    Article  CAS  Google Scholar 

  2. Misra, A. & Tyler, G. Influence of soil moisture on soil solution chemistry and concentrations of minerals in the calcicoles Phleum phleoides and Veronica spicata grown on a limestone soil. Ann. Bot. 84, 401–410 (1999).

    Article  CAS  Google Scholar 

  3. Göttlein, A., Heim, A. & Matzner, E. Mobilization of aluminium in the rhizosphere soil solution of growing tree roots in an acidic soil. Plant Soil 211, 41–49 (1999).

    Article  Google Scholar 

  4. Rousk, J. et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340–1351 (2010).

    Article  PubMed  Google Scholar 

  5. Arnon, D. I. & Johnson, C. M. Influence of hydrogen ion concentration on the growth of higher plants under controlled conditions. Plant Physiol. 17, 525–539 (1942).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Raven, J. A. Sensing pH? Plant Cell Environ. 13, 721–729 (1990).

    Article  CAS  Google Scholar 

  7. Krulwich, T. A., Sachs, G. & Padan, E. Molecular aspects of bacterial pH sensing and homeostasis. Nat. Rev. Microbiol. 9, 330–343 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tohidifar, P., Plutz, M. J., Ordal, G. W. & Rao, C. V. The mechanism of bidirectional pH taxis in Bacillus subtilis. J. Bacteriol. 202, e00491-19 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Yang, Y. & Sourjik, V. Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis. Mol. Microbiol. 86, 1482–1489 (2012).

    Article  CAS  PubMed  Google Scholar 

  10. Hu, B. & Tu, Y. Precision sensing by two opposing gradient sensors: how does Escherichia coli find its preferred pH level? Biophys. J. 105, 276–285 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Haneburger, I., Eichinger, A., Skerra, A. & Jung, K. New insights into the signaling mechanism of the pH-responsive, membrane-integrated transcriptional activator CadC of Escherichia coli. J. Biol. Chem. 286, 10681–10689 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Buchner, S., Schlundt, A., Lassak, J., Sattler, M. & Jung, K. Structural and functional analysis of the signal-transducing linker in the pH-responsive one-component system CadC of Escherichia coli. J. Mol. Biol. 427, 2548–2561 (2015).

    Article  CAS  PubMed  Google Scholar 

  13. Schlundt, A. et al. Structure–function analysis of the DNA-binding domain of a transmembrane transcriptional activator. Sci. Rep. 7, 1051 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Taglicht, D., Padan, E. & Schuldiner, S. Overproduction and purification of a functional Na+/H+ antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266, 11289–11294 (1991).

    Article  CAS  PubMed  Google Scholar 

  15. Padan, E. The enlightening encounter between structure and function in the NhaA Na+–H+ antiporter. Trends Biochem. Sci. 33, 435–443 (2008).

    Article  CAS  PubMed  Google Scholar 

  16. Herz, K., Rimon, A., Olkhova, E., Kozachkov, L. & Padan, E. Transmembrane segment II of NhaA Na+/H+ antiporter lines the cation passage, and Asp65 is critical for pH activation of the antiporter. J. Biol. Chem. 285, 2211–2220 (2010).

    Article  CAS  PubMed  Google Scholar 

  17. Călinescu, O. et al. Lysine 300 is essential for stability but not for electrogenic transport of the Escherichia coli NhaA Na+/H+ antiporter. J. Biol. Chem. 292, 7932–7941 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gerchman, Y. et al. Histidine-226 is part of the pH sensor of NhaA, a Na+/H+ antiporter in Escherichia coli. Proc. Natl Acad. Sci. USA 90, 1212–1216 (1993).

    Article  CAS  PubMed  Google Scholar 

  19. Wen, Y., Feng, J., Scott, D. R., Marcus, E. A. & Sachs, G. The HP0165–HP0166 two-component system (ArsRS) regulates acid-induced expression of HP1186 α-carbonic anhydrase in Helicobacter pylori by activating the pH-dependent promoter. J. Bacteriol. 189, 2426–2434 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Müller, S., Götz, M. & Beier, D. Histidine residue 94 is involved in pH sensing by histidine kinase ArsS of Helicobacter pylori. PLoS ONE 4, e6930 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Yu, X. J., McGourty, K., Liu, M., Unsworth, K. E. & Holden, D. W. pH sensing by intracellular Salmonella induces effector translocation. Science 328, 1040–1043 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wimmi, S. et al. Dynamic relocalization of the cytosolic type III secretion system components prevents premature protein secretion at low external pH. Preprint at bioRxiv https://doi.org/10.1101/869214 (2019).

  23. Tresguerres, M., Buck, J. & Levin, L. R. Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch. Eur. J. Phy. 460, 953–964 (2010).

    Article  CAS  Google Scholar 

  24. Deyev, I. E. et al. Insulin receptor-related receptor as an extracellular alkali sensor. Cell Metab. 13, 679–689 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Deyev, I. E., Chachina, N. A., Shayahmetova, D. M., Serova, O. V. & Petrenko, A. G. Mapping of alkali-sensing sites of the insulin receptor-related receptor. The role of L2 and fibronectin domains. Biochimie 111, 1–9 (2015).

    Article  CAS  PubMed  Google Scholar 

  26. Reyes, R. et al. Cloning and expression of a novel pH-sensitive two pore domain K+ channel from human kidney. J. Biol. Chem. 273, 30863–30869 (1998).

    Article  CAS  PubMed  Google Scholar 

  27. Zúñiga, L. et al. Gating of a pH-sensitive K2P potassium channel by an electrostatic effect of basic sensor residues on the selectivity filter. PLoS ONE 6, e16141 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Levin, L. R. & Buck, J. Physiological roles of acid–base sensors. Annu. Rev. Physiol. 77, 347–362 (2015).

    Article  CAS  PubMed  Google Scholar 

  29. Ludwig, M. et al. Proton-sensing G-protein-coupled receptors. Nature 425, 93–98 (2003).

    Article  CAS  PubMed  Google Scholar 

  30. Tobo, M. et al. Previously postulated “ligand-independent” signaling of GPR4 is mediated through proton-sensing mechanisms. Cell. Signal. 19, 1745–1753 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. Wang, J. Q. et al. TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J. Biol. Chem. 279, 45626–45633 (2004).

    Article  CAS  PubMed  Google Scholar 

  32. Jasti, J., Furukawa, H., Gonzales, E. B. & Gouaux, E. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449, 316–323 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. Paukert, M., Chen, X., Polleichtner, G., Schindelin, H. & Gründer, S. Candidate amino acids involved in H+ gating of acid-sensing ion channel 1a. J. Biol. Chem. 283, 572–581 (2008).

    Article  CAS  PubMed  Google Scholar 

  34. Vullo, S. et al. Role of acidic pocket in ASIC gating. Proc. Natl Acad. Sci. USA 114, 3768–3773 (2017).

    Article  CAS  PubMed  Google Scholar 

  35. Vullo, S. & Kellenberger, S. A molecular view of the function and pharmacology of acid-sensing ion channels. Pharmacol. Res. 154, 104166 (2020).

    Article  CAS  PubMed  Google Scholar 

  36. Ikeda, M., Kihara, A., Denpoh, A. & Igarashi, Y. The Rim101 pathway is involved in Rsb1 expression induced by altered lipid asymmetry. Mol. Biol. Cell 19, 1922–1931 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Obara, K., Yamamoto, H. & Kihara, A. Membrane protein Rim21 plays a central role in sensing ambient pH in Saccharomyces cerevisiae. J. Biol. Chem. 287, 38473–38481 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Xu, W., Smith, F. J., Subaran, R. & Mitchell, A. P. Multivesicular body-ESCRT components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol. Biol. Cell 15, 5528–5537 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Peñalva, M. A., Lucena-Agell, D. & Arst, H. N. Jr. Liaison alcaline: Pals entice non-endosomal ESCRTs to the plasma membrane for pH signaling. Curr. Opin. Microbiol. 22, 49–59 (2014).

    Article  PubMed  Google Scholar 

  40. Nishino, K., Obara, K. & Kihara, A. The C-terminal cytosolic region of Rim21 senses alterations in plasma membrane lipid composition: insights into sensing mechanisms for plasma membrane lipid asymmetry. J. Biol. Chem. 290, 30797–30805 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Obara, K. & Kihara, A. Signaling events of the Rim101 pathway occur at the plasma membrane in a ubiquitination-dependent manner. Mol. Cell. Biol. 34, 3525–3534 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hayashi, M., Fukuzawa, T., Sorimachi, H. & Maeda, T. Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol. Cell. Biol. 25, 9478–9490 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69–77 (1998).

    Article  CAS  PubMed  Google Scholar 

  44. Pandey, S., Zhang, W. & Assmann, S. M. Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett. 581, 2325–2336 (2007).

    Article  CAS  PubMed  Google Scholar 

  45. Clark, M. D., Contreras, G. F., Shen, R. & Perozo, E. Electromechanical coupling in the hyperpolarization-activated K+ channel KAT1. Nature 583, 145–149 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hoth, S. et al. Molecular basis of plant-specific acid activation of K+ uptake channels. Proc. Natl Acad. Sci. USA 94, 4806–4810 (1997).

    Article  CAS  PubMed  Google Scholar 

  47. Hoth, S. & Hedrich, R. Distinct molecular bases for pH sensitivity of the guard cell K+ channels KST1 and KAT1. J. Biol. Chem. 274, 11599–11603 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. González, W. et al. The pH sensor of the plant K+-uptake channel KAT1 is built from a sensory cloud rather than from single key amino acids. Biochem. J. 442, 57–63 (2012).

    Article  PubMed  Google Scholar 

  49. Wang, L. et al. The S1–S2 linker determines the distinct pH sensitivity between ZmK2.1 and KAT 1. Plant J. 85, 675–685 (2016).

    Article  CAS  PubMed  Google Scholar 

  50. Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 14, 1112–1115 (2018).

    Article  Google Scholar 

  51. Shao, Q. et al. Two glutamate- and pH-regulated Ca2+ channels are required for systemic wound signaling in Arabidopsis. Sci. Signal. 13, eaba1453 (2020).

    Article  CAS  PubMed  Google Scholar 

  52. Causton, H. C. et al. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12, 323–337 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Canadell, D. et al. Impact of high pH stress on yeast gene expression: a comprehensive analysis of mRNA turnover during stress responses. Biochim. Biophys. Acta Gene Regul. Mech. 1849, 653–664 (2015).

    Article  CAS  Google Scholar 

  54. Serra-Cardona, A., Canadell, D. & Ariño, J. Coordinate responses to alkaline pH stress in budding yeast. Microb. Cell 2, 182–196 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Barad, S. et al. Fungal and host transcriptome analysis of pH-regulated genes during colonization of apple fruits by Penicillium expansum. BMC Genomics 17, 330 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Payá-Milans, M. et al. Regulation of gene expression in roots of the pH-sensitive Vaccinium corymbosum and the pH-tolerant Vaccinium arboreum in response to near neutral pH stress using RNA-seq. BMC Genomics 18, 580 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Lager, I. D. A. et al. Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant Cell Environ. 33, 1513–1528 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Tsai, H. H. & Schmidt, W. pH-dependent transcriptional profile changes in iron-deficient Arabidopsis roots. BMC Genomics 21, 694 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Von Uexküll, H. R. & Mutert, E. Global extent, development and economic impact of acid soils. Plant Soil 171, 1–15 (1995).

    Article  Google Scholar 

  60. Parker, J. L. & Newstead, S. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507, 68–72 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Tsay, Y. F., Schroeder, J. I., Feldmann, K. A. & Crawford, N. M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705–713 (1993).

    Article  CAS  PubMed  Google Scholar 

  62. Iuchi, S. et al. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc. Natl Acad. Sci. USA 104, 9900–9905 (2007).

    Article  PubMed  Google Scholar 

  63. Kidd, P. S. & Proctor, J. Why plants grow poorly on very acid soils: are ecologists missing the obvious? J. Exp. Bot. 52, 791–799 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Ikka, T. et al. Natural variation of Arabidopsis thaliana reveals that aluminum resistance and proton resistance are controlled by different genetic factors. Theor. Appl. Genet. 115, 709–719 (2007).

    Article  CAS  PubMed  Google Scholar 

  65. Jiang, F. et al. Identification and characterization of suppressor mutants of stop1. BMC Plant Biol. 17, 128 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Kobayashi, Y. et al. STOP2 activates transcription of several genes for Al-and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol. Plant 7, 311–322 (2014).

    Article  CAS  PubMed  Google Scholar 

  67. Balzergue, C. et al. Low phosphate activates STOP1–ALMT1 to rapidly inhibit root cell elongation. Nat. Comm. 8, 15300 (2017).

    Article  CAS  Google Scholar 

  68. Boukhalfa, H. & Crumbliss, A. L. Chemical aspects of siderophore mediated iron transport. Biometals 15, 325–339 (2002).

    Article  CAS  Google Scholar 

  69. Römheld, V. & Marschner, H. Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175–180 (1986).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Siwinska, J. et al. Scopoletin 8-hydroxylase: a novel enzyme involved in coumarin biosynthesis and iron-deficiency responses in Arabidopsis. J. Exp. Bot. 69, 1735–1748 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Rajniak, J. et al. Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nat. Chem. Biol. 14, 442–450 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Tsai, H. H. et al. Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobilization. Plant Physiol. 177, 194–207 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Sisó-Terraza, P. et al. Accumulation and secretion of coumarinolignans and other coumarins in Arabidopsis thaliana roots in response to iron deficiency at high pH. Front. Plant Sci. 7, 1711 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Kim, S. A., LaCroix, I. S., Gerber, S. A. & Guerinot, M. L. The iron deficiency response in Arabidopsis thaliana requires the phosphorylated transcription factor URI. Proc. Natl Acad. Sci. USA 116, 24933–24942 (2019).

    Article  CAS  PubMed  Google Scholar 

  75. Colangelo, E. P. & Guerinot, M. L. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16, 3400–3412 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Ahn, Y. O. et al. Scopolin-hydrolyzing β-glucosidases in roots of Arabidopsis. Plant Cell Physiol. 51, 132–143 (2010).

    Article  CAS  PubMed  Google Scholar 

  77. Zamioudis, C., Hanson, J. & Pieterse, C. M. J. β-Glucosidase BGLU 42 is a MYB 72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. N. Phytol. 204, 368–379 (2014).

    Article  CAS  Google Scholar 

  78. Oba, K., Conn, E. E., Canut, H. & Boudet, A. M. Subcellular localization of 2-(β-d-glucosyloxy)-cinnamic acids and the related β-glucosidase in leaves of Melilotus alba Desr. Plant Physiol. 68, 1359–1363 (1981).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Dietz, K. J., Sauter, A., Wichert, K., Messdaghi, D. & Hartung, W. Extracellular β-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. J. Exp. Bot. 51, 937–944 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Morant, A. et al. β-Glucosidases as detonators of plant chemical defense. Phytochemistry 69, 1795–1813 (2008).

    Article  CAS  PubMed  Google Scholar 

  81. Martinière, A. et al. Uncovering pH at both sides of the root plasma membrane interface using noninvasive imaging. Proc. Natl Acad. Sci. USA 115, 6488–6493 (2018).

    Article  PubMed  Google Scholar 

  82. Cosgrove, D. J. Diffuse growth of plant cell walls. Plant Physiol. 176, 16–27 (2018).

    Article  CAS  PubMed  Google Scholar 

  83. Hager, A., Menzle, H. & Krauss, A. Versuche und hypothese zur primarwirkung des auxins beim streckungswachstum. Planta 100, 47–75 (1971).

    Article  CAS  PubMed  Google Scholar 

  84. Geilfus, C. M., Tenhaken, R. & Carpentier, S. C. Transient alkalinization of the leaf apoplast stiffens the cell wall during onset of chloride salinity in corn leaves. J. Biol. Chem. 292, 18800–18813 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Pearce, G., Moura, D. S., Stratmann, J. & Ryan, C. A. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl Acad. Sci. USA 98, 12843–12847 (2001).

    Article  CAS  PubMed  Google Scholar 

  86. Amano, Y., Tsubouchi, H., Shinohara, H., Ogawa, M. & Matsubayashi, Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl Acad. Sci. USA 104, 18333–18338 (2007).

    Article  CAS  PubMed  Google Scholar 

  87. Gjetting, S. K. et al. Evidence for multiple receptors mediating RALF–triggered Ca2+ signaling and proton pump inhibition. Plant J. https://doi.org/10.1111/tpj.14935 (2020).

  88. Fuglsang, A. T. et al. Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. Plant J. 80, 951–964 (2014).

    Article  CAS  PubMed  Google Scholar 

  89. Haruta, M., Sabat, G., Stecker, K., Minkoff, B. B. & Sussman, M. R. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Masachis, S. et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1, 16043 (2016).

    Article  CAS  PubMed  Google Scholar 

  91. Stegmann, M. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355, 287–289 (2017).

    Article  CAS  PubMed  Google Scholar 

  92. Li, C. Y. et al. Two FERONIA-like receptor (FLR) genes are required to maintain architecture, fertility, and seed yield in rice. Mol. Breed. 36, 151 (2016).

    Article  Google Scholar 

  93. Xu, G. et al. FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in response to the carbon/nitrogen ratio. J. Exp. Bot. 70, 6375–6388 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zhu, S. et al. The RALF1–FERONIA complex phosphorylates eIF4E1 to promote protein synthesis and polar root hair growth. Mol. Plant 13, 698–716 (2020).

    Article  CAS  PubMed  Google Scholar 

  95. Roberts, J. K. M., Wade-Jardetzky, N. & Jardetsky, O. Intracellular pH measurements by phosphorus-31 nuclear magnetic resonance. Influence of factors other than pH on phosphorus-31 chemical shifts. Biochemistry 20, 5389–5394 (1981).

    Article  CAS  PubMed  Google Scholar 

  96. Pfeffer, P. E., Tu, S., Gerasimowicz, W. V. & Borswell, R. T. Effects of aluminum on the release and-or immobilization of soluble phosphate in corn root tissue. Planta 172, 200–208 (1987).

    Article  CAS  PubMed  Google Scholar 

  97. Lacombe, B. et al. pH control of the plant outwardly-rectifying potassium channel SKOR. FEBS Lett. 466, 351–354 (2000).

    Article  CAS  PubMed  Google Scholar 

  98. Weisenseel, M. H., Dorn, A. & Jaffe, L. F. Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.). Plant Physiol. 64, 512–518 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Marschner, H. & Römheld, V. In vivo measurement of root-induced pH changes at the soil–root interface: effect of plant species and nitrogen source. Z. Pflanzenphysiol. 111, 241–251 (1983).

    Article  CAS  Google Scholar 

  100. Moorby, H., White, R. E. & Nye, P. H. The influence of phosphate nutrition on H ion efflux from the roots of young rape plants. Plant Soil 105, 247–256 (1988).

    Article  CAS  Google Scholar 

  101. Zhao, Q. et al. Ubiquitination-related MdBT scaffold proteins target a bHLH transcription factor for iron homeostasis. Plant Physiol. 172, 1973–1988 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wang, Y. & Lambers, H. Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives. Plant Soil 447, 135–156 (2020).

    Article  CAS  Google Scholar 

  103. Penny, M. G. & Bowling, D. J. F. Direct determination of pH in the stomatal complex of Commelina. Planta 122, 209–212 (1975).

    Article  CAS  PubMed  Google Scholar 

  104. Felle, H. H. The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation. J. Exp. Bot. 49, 987–995 (1998).

    Article  CAS  Google Scholar 

  105. Geilfus, C. M. The pH of the apoplast: dynamic factor with functional impact under stress. Mol. Plant 10, 1371–1386 (2017).

    Article  CAS  PubMed  Google Scholar 

  106. Hoffmann, B., Plänker, R. & Mengel, K. Measurements of pH in the apoplast of sunflower leaves by means of fluorescence. Physiol. Plant. 84, 146–153 (1992).

    Article  CAS  Google Scholar 

  107. Brauer, D., Otto, J. & Tu, S.-I. Selective accumulation of the fluorescent pH indicator, BCECF, in vacuoles of maize root-hair cells. J. Plant Physiol. 145, 57–61 (1995).

    Article  CAS  Google Scholar 

  108. Sano, T., Kutsuna, N. & Hasezawa, S. Improved cytoplasmic pH measurements in SNARF-1 stained plant cells by image processing. Plant Signal. Behav. 5, 406–408 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Barbez, E., Dünser, K., Gaidora, A., Lendl, T. & Busch, W. Apoplastic pH regulation in A. thaliana roots. Proc. Natl Acad. Sci. USA 114, E4884–E4893 (2017).

    Article  CAS  PubMed  Google Scholar 

  110. Kneen, M., Farinas, J., Li, Y. & Verkman, A. S. Green fluorescent protein as a non-invasive intracellular pH indicator. Biophys. J. 74, 1591–1599 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Miesenböck, G., De Angelis, D. & Rothman, J. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192–195 (1998).

    Article  PubMed  Google Scholar 

  112. Haseloff, J., Siemering, K. R., Prasher, D. C. & Hodge, S. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl Acad. Sci. USA 94, 2122–2127 (1997).

    Article  CAS  PubMed  Google Scholar 

  113. Moseyko, N. & Feldman, L. J. Expression of pH-sensitive green fluorescent protein in Arabidopsis thaliana. Plant Cell Environ. 24, 557–563 (2001).

    Article  CAS  PubMed  Google Scholar 

  114. Shen, J. et al. Organelle pH in the Arabidopsis endomembrane system. Mol. Plant 6, 1419–1437 (2013).

    Article  CAS  PubMed  Google Scholar 

  115. Gjetting, K. S., Ytting, C. K., Schulz, A. & Fuglsang, A. T. Live imaging of intra-and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J. Exp. Bot. 63, 3207–3218 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Zhang, Y., Xie, Q., Robertson, J. B. & Johnson, C. H. pHlash: a new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS ONE 7, e43072 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Dinkelaker, B., Römheld, V. & Marschner, H. Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ. 12, 285–292 (1989).

    Article  CAS  Google Scholar 

  118. Falhof, J., Pedersen, J. T., Fuglsang, A. T. & Palmgren, M. Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol. Plant 9, 323–337 (2016).

    Article  CAS  PubMed  Google Scholar 

  119. Canarini, A., Wanek, W., Merchant, A., Richter, A. & Kaiser, C. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10, 157 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  120. Zhou, L. J. et al. The SUMO E3 ligase MdSIZ1 targets MdbHLH104 to regulate plasma membrane H+-ATPase activity and iron homeostasis. Plant Physiol. 179, 88–106 (2019).

    Article  CAS  PubMed  Google Scholar 

  121. Martinière, A. et al. In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell 25, 4028–4043 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Research in the Schmidt Laboratory is funded by Academia Sinica and the Ministry of Science and Technology (MOST).

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Authors and Affiliations

  1. Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan

    Huei-Hsuan Tsai & Wolfgang Schmidt

  2. Biotechnology Center, National Chung-Hsing University, Taichung, Taiwan

    Wolfgang Schmidt

  3. Genome and Systems Biology Degree Program, College of Life Science, National Taiwan University, Taipei, Taiwan

    Wolfgang Schmidt

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  1. Huei-Hsuan Tsai
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  2. Wolfgang Schmidt
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H.-H.T. conducted research that led to the hypothesis put forward in the manuscript, composed the figures and contributed to the writing. W.S. initiated the research and wrote the paper.

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Correspondence to Wolfgang Schmidt.

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Tsai, HH., Schmidt, W. The enigma of environmental pH sensing in plants. Nat. Plants 7, 106–115 (2021). https://doi.org/10.1038/s41477-020-00831-8

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