Advertisement

Water Sensing in Plants

  • Hillel FrommEmail author
  • Yosef Fichman
Chapter

Abstract

Water is a key factor in plant life. Therefore, reaching and holding water is a crucial part in plant survival. Plants sense water through a set of sensors which includes sensors for water activity (potential), for specific components of water potential, or for specific solutes contributing to water potential and for hydraulic signals. While these sensors are common to different plants and other organisms, their functions and modes of action are yet far from being understood. It is also unknown how these sensing mechanisms are linked to cellular and whole-plant responses to changes in water status in the soil or in the atmosphere. Advanced technologies that would provide means for single-cell physiological manipulations together with high-throughput noninvasive real-time monitoring systems of shoots and roots and advanced biochemistry and structural studies at atomic resolution of sensor proteins and protein complexes are imperative for understanding water sensing by plants.

Keywords

Cell wall integral (CWI) signaling Extracellular matrix (ECM) Hydraulic pressure Hydrotropism Mechanosensors Osmosensing Receptor-like wall-associated kinases (WAKs) 

References

  1. Ahmad I, Devonshire J, Mohamed R, Schultze M, Maathuis FJ (2016) Overexpression of the potassium channel TPKb in small vacuoles confers osmotic and drought tolerance to rice. New Phytol 209:1040–1048PubMedCrossRefGoogle Scholar
  2. Amien S, Kliwer I, Márton ML, Debener T, Geiger D, Becker D, Dresselhaus T (2010) Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol 8:e1000388PubMedPubMedCentralCrossRefGoogle Scholar
  3. Anderson CM, Wagner TA, Perret M, He ZH, He D, Kohorn BD (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47:197–206Google Scholar
  4. Arnadóttir J, Chalfie M (2010) Eukaryotic mechanosensitive channels. Annu Rev Biophys 39:111–137PubMedCrossRefGoogle Scholar
  5. Auler PA, do Amaral MN, Rodrigues GDS, Benitez LC, da Maia LC, Souza GM, Braga EJB (2017) Molecular responses to recurrent drought in two contrasting rice genotypes. Planta 246:899–914PubMedCrossRefGoogle Scholar
  6. Balagué C, Gouget A, Bouchez O, Souriac C, Haget N, Boutet-Mercey S, Govers F, Roby D, Canut H (2017) The Arabidopsis thaliana lectin receptor kinase LecRK-I.9 is required for full resistance to Pseudomonas syringae and affects jasmonate signalling. Mol Plant Pathol 18:937–948PubMedCrossRefGoogle Scholar
  7. Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000 Res 5:1554CrossRefGoogle Scholar
  8. Bentrup FW (2017) Water ascent in trees and lianas: the cohesion-tension theory revisited in the wake of Otto Renner. Protoplasma 254:627–633PubMedCrossRefGoogle Scholar
  9. Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40:4–10PubMedCrossRefGoogle Scholar
  10. Buckley TN (2005) The control of stomata by water balance. New Phytol 168(2):275–292PubMedCrossRefGoogle Scholar
  11. Buckley TN, Sack L, Farquhar GD (2017) Optimal plant water economy. Plant Cell Environ 40:881–896PubMedCrossRefGoogle Scholar
  12. Chefdor F, Bénédetti H, Depierreux C, Delmotte F, Morabito D, Carpin S (2006) Osmotic stress sensing in Populus: components identification of a phosphorelay system. FEBS Lett 580:77–81PubMedCrossRefGoogle Scholar
  13. Choi WG, Miller G, Wallace I, Harper J, Mittler R, Gilroy S (2017) Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J 90:698–707PubMedPubMedCentralCrossRefGoogle Scholar
  14. Christmann A, Grill E, Huang J (2013) Hydraulic signals in long-distance signaling. Curr Opin Plant Biol 16:293–300PubMedCrossRefGoogle Scholar
  15. Clark RT, MacCurdy RB, Jung JK, Shaff JE, McCouch SR, Aneshansley DJ, Kochian LV (2011) Three-dimensional root phenotyping with a novel imaging and software platform. Plant Physiol 156:455–465PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cole ES, Mahall BE (2006) A test for hydrotropic behavior by roots of two coastal dune shrubs. New Phytol 172:358–368PubMedCrossRefGoogle Scholar
  17. Cook GD, Dixon JR, Leopold AC (1964) Transpiration: its effects on plant leaf temperature. Science 144:546–547PubMedCrossRefGoogle Scholar
  18. Darwin C, Darwin F (1880) The power of movement in plants. John Murray, LondonGoogle Scholar
  19. De Schepper V, De Swaef T, Bauweraerts I, Steppe K (2013) Phloem transport: a review of mechanisms and controls. J Exp Bot 64:4839–4850PubMedCrossRefGoogle Scholar
  20. Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. J Plant Physiol 171:696–707PubMedCrossRefGoogle Scholar
  21. Dietrich D, Pang L, Kobayashi A, Fozard JA, Boudolf V, Bhosale R, Antoni R, Nguyen T, Hiratsuka S, Fujii N, Miyazawa Y, Bae TW, Wells DM, Owen MR, Band LR, Dyson RJ, Jensen OE, King JR, Tracy SR, Sturrock CJ, Mooney SJ, Roberts JA, Bhalerao RP, Dinneny JR, Rodriguez PL, Nagatani A, Hosokawa Y, Baskin TI, Pridmore TP, De Veylder L, Takahashi H, Bennett MJ (2017) Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat Plants 8:17057CrossRefGoogle Scholar
  22. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620CrossRefGoogle Scholar
  23. Falik O, Mordoch Y, Ben-Natan D, Vanunu M, Goldstein O, Novoplansky A (2012) Plant responsiveness to root-root communication of stress cues. Ann Bot 110:271–280PubMedPubMedCentralCrossRefGoogle Scholar
  24. Feller U (2016) Drought stress and carbon assimilation in a warming climate: reversible and irreversible impacts. J Plant Physiol 203:84–94PubMedCrossRefGoogle Scholar
  25. Feng D, Huang X, Liu Y, Willison JH (2016) Growth and changes of endogenous hormones of mulberry roots in a simulated rocky desertification area. Environ Sci Pollut Res Int 23:11171–11180PubMedCrossRefGoogle Scholar
  26. Gagliano M, Grimonprez M, Depczynski M, Renton M (2017) Tuned in: plant roots use sound to locate water. Oecologia 184:151–160PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–22230PubMedCrossRefGoogle Scholar
  28. Ghatak A, Chaturvedi P, Weckwerth W (2017) Cereal crop proteomics: systemic analysis of crop drought stress responses towards marker-assisted selection breeding. Front Plant Sci 8:757PubMedPubMedCentralCrossRefGoogle Scholar
  29. Giarola V, Hou Q, Bartels D (2017) angiosperm plant desiccation tolerance: hints from transcriptomics and genome sequencing. Trends Plant Sci 22:705–717PubMedCrossRefGoogle Scholar
  30. Gorgolewski S, Rozej B (2001) Evidence for electrotropism in some plant species. Adv Space Res 28:633–638PubMedCrossRefGoogle Scholar
  31. Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rougé P, Pont-Lezica R, Canut H (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140:81–90PubMedPubMedCentralCrossRefGoogle Scholar
  32. Ham BK, Lucas WJ (2014) The angiosperm phloem sieve tube system: a role in mediating traits important to modern agriculture. J Exp Bot 65:1799–1816PubMedCrossRefGoogle Scholar
  33. Hamilton ES, Jensen GS, Maksaev G, Katims A, Sherp AM, Haswell ES (2015) Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350:438–441PubMedPubMedCentralCrossRefGoogle Scholar
  34. Harkenrider M, Sharma R, De Vleesschauwer D, Tsao L, Zhang X, Chern M, Canlas P, Zuo S, Ronald PC (2016) Overexpression of rice wall-associated kinase 25 (OsWAK25) alters resistance to bacterial and fungal pathogens. PLoS One 11:e0147310PubMedPubMedCentralCrossRefGoogle Scholar
  35. Haswell ES, Phillips R, Rees DC (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19:1356–1369PubMedPubMedCentralCrossRefGoogle Scholar
  36. Héricourt F, Chefdor F, Bertheau L, Tanigawa M, Maeda T, Guirimand G, Courdavault V, Larcher M, Depierreux C, Bénédetti H, Morabito D, Brignolas F, Carpin S (2013) Characterization of histidine-aspartate kinase HK1 and identification of histidine phosphotransfer proteins as potential partners in a populus multistep phosphorelay. Physiol Plant 149:188–199PubMedCrossRefGoogle Scholar
  37. Hill AE, Shachar-Hill Y (2015) Are aquaporins the missing transmembrane osmosensors? J Membr Biol 248:753–765PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hussain SS, Kayani MA, Amjad M (2011) Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol Prog 27:297–306PubMedCrossRefPubMedCentralGoogle Scholar
  39. Jahnke S, Menzel MI, van Dusschoten D, Roeb GW, Bühler J, Minwuyelet S, Blümler P, Temperton VM, Hombach T, Streun M, Beer S, Khodaverdi M, Ziemons K, Coenen HH, Schurr U (2009) Combined MRI-PET dissects dynamic changes in plant structures and functions. Plant J 59:634–644PubMedCrossRefPubMedCentralGoogle Scholar
  40. Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kamano S, Kume S, Iida K, Lei KJ, Nakano M, Nakayama Y, Iida H (2015) Transmembrane topologies of Ca2+-permeable mechanosensitive channels MCA1 and MCA2 in Arabidopsis thaliana. J Biol Chem 290:30901–30909PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kohorn BD, Kohorn SL (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Front Plant Sci 3:88PubMedPubMedCentralCrossRefGoogle Scholar
  43. Krieger G, Shkolnik D, Miller G, Fromm H (2016) reactive oxygen species tune root tropic responses. Plant Physiol 172:1209–1220PubMedPubMedCentralGoogle Scholar
  44. Kumar MN, Jane WN, Verslues PE (2013) Role of the putative osmosensor Arabidopsis histidine kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol 161:942–953PubMedCrossRefGoogle Scholar
  45. Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654PubMedCrossRefGoogle Scholar
  46. Kurusu T, Iida H, Kuchitsu K (2012a) Roles of a putative mechanosensitive plasma membrane Ca2+-permeable channel OsMCA1 in generation of reactive oxygen species and hypo-osmotic signaling in rice. Plant Signal Behav 7:796–798PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kurusu T, Nishikawa D, Yamazaki Y, Gotoh M, Nakano M, Hamada H, Yamanaka T, Iida K, Nakagawa Y, Saji H, Shinozaki K, Iida H, Kuchitsu K (2012b) Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol 12:11PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kurusu T, Yamanaka T, Nakano M, Takiguchi A, Ogasawara Y, Hayashi T, Iida K, Hanamata S, Shinozaki K, Iida H, Kuchitsu K (2012c) Involvement of the putative Ca2+-permeable mechanosensitive channels, NtMCA1 and NtMCA2, in Ca2+ uptake, Ca2+-dependent cell proliferation and mechanical stress-induced gene expression in tobacco (Nicotiana tabacum) BY-2 cells. J Plant Res 125:555–568PubMedCrossRefGoogle Scholar
  49. Kushwaha HR, Singla-Pareek SL, Pareek A (2014) Putative osmosensor–OsHK3b–a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J Biomol Struct Dyn 32:1318–1332PubMedCrossRefGoogle Scholar
  50. Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79PubMedCrossRefGoogle Scholar
  51. Lee CP, Maksaev G, Jensen GS, Murcha MW, Wilson ME, Fricker M, Hell R, Haswell ES, Millar AH, Sweetlove LJ (2016) MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress. Plant J 88:809–825.PubMedCrossRefGoogle Scholar
  52. Louf JF, Guéna G, Badel E, Forterre Y (2017) Universal poroelastic mechanism for hydraulic signals in biomimetic and natural branches. Proc Natl Acad Sci USA 114:11034–11039PubMedCrossRefGoogle Scholar
  53. Maathuis FJM (2011) Vacuolar two-pore K+ channels act as vacuolar osmosensors. New Phytol 191:81–91CrossRefGoogle Scholar
  54. MacRobbie EA (2006) Osmotic effects on vacuolar ion release in guard cells. Proc Natl Acad Sci USA 103:1135–1140PubMedCrossRefGoogle Scholar
  55. Mahmood NA, Biemans-Oldehinkel E, Patzlaff JS, Schuurman-Wolters GK, Poolman B (2006) Ion specificity and ionic strength dependence of the osmoregulatory ABC transporter OpuA. J Biol Chem 281:29830–29839PubMedCrossRefGoogle Scholar
  56. Marcum H, Moore R (1990) Influence of electrical fields and asymmetric application of mucilage on curvature of primary roots of zea mays. Am J Bot 77:446–452PubMedCrossRefGoogle Scholar
  57. Mathur J (2006) Local interactions shape plant cells. Curr Opin Cell Biol 18:40–46PubMedCrossRefGoogle Scholar
  58. Mishra RC, Ghosh R, Bae H (2016) Plant acoustics: in the search of a sound mechanism for sound signaling in plants. J Exp Bot 67:4483–4494PubMedPubMedCentralCrossRefGoogle Scholar
  59. Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644PubMedCrossRefGoogle Scholar
  60. Nalepa A, Malferrari M, Lubitz W, Venturoli G, Möbius K, Savitsky A (2017) Local water sensing: water exchange in bacterial photosynthetic reaction centers embedded in a trehalose glass studied using multiresonance EPR. Phys Chem Chem Phys 19:28388–28400PubMedCrossRefGoogle Scholar
  61. Ota IM, Varshavsky A (1993) A yeast protein similar to bacterial two-component regulators. Science 262:566–569PubMedCrossRefGoogle Scholar
  62. Peyronnet R, Tran D, Girault T, Frachisse JM (2014) Mechanosensitive channels: feeling tension in a world under pressure. Front Plant Sci 5:558PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ramthun AD (2017) Plant electro-tropism. Water J 8:47–106Google Scholar
  64. Rellán-Álvarez R, Lobet G, Lindner H, Pradier PL, Sebastian J, Yee MC, Geng Y, Trontin C, LaRue T, Schrager-Lavelle A, Haney CH, Nieu R, Maloof J, Vogel JP, Dinneny JR (2015) GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. eLife 4:–e07597Google Scholar
  65. Rogers ED, Monaenkova D, Mijar M, Nori A, Goldman DI, Benfey PN (2016) X-Ray computed tomography reveals the response of root system architecture to soil texture. Plant Physiol 171:2028–2040PubMedPubMedCentralCrossRefGoogle Scholar
  66. Sade N, Gebremedhin A, Moshelion M (2012) Risk-taking plants: anisohydric behavior as a stress-resistance trait. Plant Signal Behav 7:767–770PubMedPubMedCentralCrossRefGoogle Scholar
  67. Schaller GE, Shiu SH, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21:R320–R330PubMedCrossRefGoogle Scholar
  68. Schiller D, Krämer R, Morbach S (2004) Cation specificity of osmosensing by the betaine carrier BetP of Corynebacterium glutamicum. FEBS Lett 563:108–112PubMedCrossRefGoogle Scholar
  69. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302PubMedCrossRefGoogle Scholar
  70. Sevanto S (2014) Phloem transport and drought. J Exp Bot 65:1751–1759PubMedCrossRefGoogle Scholar
  71. Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB, Venkateswarlu B (2014) Drought stress responses in crops. Funct Integr Genomics 14:11–22PubMedCrossRefGoogle Scholar
  72. Shkolnik D, Fromm H (2016) The Cholodny-Went theory does not explain hydrotropism. Plant Sci 252:400–403PubMedCrossRefGoogle Scholar
  73. Shkolnik D, Krieger G, Nuriel R, Fromm H (2016) hydrotropism: root bending does not require auxin redistribution. Mol Plant 9:757–759PubMedCrossRefGoogle Scholar
  74. Shkolnik D, Nuriel R, Bonza MC, Costa A, Fromm H (2018) MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted ca signal essential for root water tracking in Arabidopsis. Proc Natl Acad Sci U S A 115:8031–8036PubMedPubMedCentralCrossRefGoogle Scholar
  75. Stanley CE, Shrivastava J, Brugman R, Heinzelmann E, van Swaay D, Grossmann G (2018) Dual-flow-root chip reveals local adaptations of roots towards environmental asymmetry at the physiological and genetic levels. New Phytol 217:1357–1369PubMedCrossRefGoogle Scholar
  76. Steudle E (2001) The cohesion-tension mechanism and the acquisition of water by plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:847–875PubMedCrossRefGoogle Scholar
  77. Sussmilch FC, Brodribb TJ, McAdam SAM (2017) Up-regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required. J Exp Bot 68:2913–2918PubMedPubMedCentralCrossRefGoogle Scholar
  78. Taiz L, Zeiger E, Moller IM and Murphy A (2015a) Plant physiology and development, 6th edn (ed. Sinauer AD), pp 83–118. Sinauer Associates Sunderland, MAGoogle Scholar
  79. Taiz L, Zeiger E, Moller IM and Murphy A (2015b) Plant physiology and development, 6th edn (ed. Sinauer AD), pp 104—110. Sinauer Associates, Sunderland MAGoogle Scholar
  80. Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–238.PubMedCrossRefGoogle Scholar
  81. Tanigawa M, Kihara A, Terashima M, Takahara T, Maeda T (2012) Sphingolipids regulate the yeast high-osmolarity glycerol response pathway. Mol Cell Biol 32:2861–2870PubMedPubMedCentralCrossRefGoogle Scholar
  82. Tardieu F, Cabrera-Bosquet L, Pridmore T, Bennett M (2017) Plant phenomics, from sensors to knowledge. Curr Biol 27:R770–R783PubMedCrossRefPubMedCentralGoogle Scholar
  83. Tran D, Galletti R, Neumann ED, Dubois A, Sharif-Naeini R, Geitmann A, Frachisse JM, Hamant O, Ingram GC (2017) A mechanosensitive Ca2+ channel activity is dependent on the developmental regulator DEK1. Nat Commun 8:1009PubMedPubMedCentralCrossRefGoogle Scholar
  84. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60CrossRefGoogle Scholar
  85. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754.PubMedPubMedCentralCrossRefGoogle Scholar
  86. van Dusschoten D, Metzner R, Kochs J, Postma JA, Pflugfelder D, Bühler J, Schurr U, Jahnke S (2016) Quantitative 3d analysis of plant roots growing in soil using magnetic resonance imaging. Plant Physiol 170:1176–1188PubMedPubMedCentralCrossRefGoogle Scholar
  87. Veley KM, Marshburn S, Clure CE, Haswell ES (2012) Mechanosensitive channels protect plastids from hypoosmotic stress during normal plant growth. Curr Biol 22:408–413PubMedPubMedCentralCrossRefGoogle Scholar
  88. Veley KM, Maksaev G, Frick EM, January E, Kloepper SC, Haswell ES (2014) Arabidopsis MSL10 has a regulated cell death signaling activity that is separable from its mechanosensitive ion channel activity. Plant Cell 26:3115–3131PubMedPubMedCentralCrossRefGoogle Scholar
  89. Voxeur A, Höfte H (2016) Cell wall integrity signaling in plants: “To grow or not to grow that's the question”. Glycobiology 26:950–960PubMedCrossRefGoogle Scholar
  90. Wasson A, Bischof L, Zwart A, Watt M (2016) A portable fluorescence pectroscopy imaging system for automated root phenotyping in soil cores in the field. J Exp Bot 67:1033–1043PubMedPubMedCentralCrossRefGoogle Scholar
  91. Williams M, Oliver M, Pallardy S (2014) Teaching tools in plant biology™: lecture notes. water relations 1: uptake and transport. The Plant Cell. www.plantcell.org. American Society of Plant BiologistsGoogle Scholar
  92. Wilson ME, Jensen GS, Haswell ES (2011) Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23:2939–2949PubMedPubMedCentralCrossRefGoogle Scholar
  93. Wilson H, Mycock D, Weiersbye IM (2017) The salt glands of Tamarix usneoides E. Mey. ex Bunge (South African Salt Cedar). Int J Phytoremediation 19:587–595PubMedCrossRefGoogle Scholar
  94. Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20:1101–1117PubMedPubMedCentralCrossRefGoogle Scholar
  95. Wood JM (2006) Osmosensing in bacteria. Sciences STKE 357:pe48Google Scholar
  96. Yamanaka T, Nakagawa Y, Mori K, Nakano M, Imamura T, Kataoka H, Terashima A, Iida K, Kojima I, Katagiri T, Shinozaki K, Iida H (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296PubMedPubMedCentralCrossRefGoogle Scholar
  97. Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141PubMedPubMedCentralCrossRefGoogle Scholar
  98. Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B, Johnson DM, Swift GB, He Y, Siedow JN, Pei ZM (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–371.CrossRefGoogle Scholar
  99. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.School of Plant Sciences and Food Security, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

Personalised recommendations