Flowers under pressure: Ins and outs of turgor regulation in development

Annals of Botany

Volumn 114, Issue 7, 2014, Pages 1517-1533

  Beauzamy, Léna ^a,b   Nakayama, Naomi ^a,b,c   Boudaoud, Arezki ^a,b  

^a CNRS   (France)

^b Laboratoire Joliot Curie   (France)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

anther dehiscence; aquaporins; Flower development; flower opening,water potential; hydraulic conductivity; osmoregulation; osmotic pressure; plasmodesmata; pollen tube; turgor pressure

Indexed keywords

FLOWER; HYDRAULIC CONDUCTIVITY; OSMOREGULATION; OSMOSIS; PHYSIOLOGICAL RESPONSE; POLLEN;

WATER;

ARABIDOPSIS; EVAPOTRANSPIRATION; FLOWER; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OSMOREGULATION; OSMOTIC PRESSURE; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLASMODESMA; POLLEN TUBE;

ARABIDOPSIS; FLOWERS; OSMOREGULATION; OSMOTIC PRESSURE; PLANT LEAVES; PLANT ROOTS; PLANT TRANSPIRATION; PLASMODESMATA; POLLEN TUBE; WATER;

EID: 84913593297     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu187     Document Type: Review

References (162)

1. Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G. 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant cell 15: 439-447.
2. ApseM,AharonG, SneddenW,Blumwald E. 1999. Salt tolerance conferredby overexpression of avacuolarNa+/H+antiport inArabidopsis. Science285: 1256-1258.
3. Azad A, Sawa Y, Ishikawa T, Shibata H. 2004. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals. Plant and Cell Physiology 45: 608-617.
4. Azad A,KatsuharaM, SawaY, IshikawaT, Shibata H. 2008. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant and Cell Physiology 49: 1196-1208.
5. Barstow B, Ando N, Kim C, Gruner S. 2008. Alteration of citrine structure by hydrostatic pressure explains the accompanying spectral shift. Proceedings of the National Academy of Sciences, USA 105: 13362-13366.
6. Barstow B, Ando N, Kim C, Gruner S. 2009. Coupling of pressure-induced structural shifts to spectral changes in a yellow fluorescent protein. Biophysical Journal 97: 1719-1727.
7. Bassil E,Tajima H, LiangY, et al. 2011. The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. The Plant Cell 23: 3482-3497.
8. Benitez-Alfonso Y, Jackson D, Maule A. 2011. Redox regulation of intercellular transport. Protoplasma 248: 131-140.
9. Benitez-AlfonsoY,Faulkner C,Pendle A, Miyashima S, HelariuttaY, Maule A. 2013. Symplastic intercellular connectivity regulates lateral root patterning. Developmental Cell 26: 136-147.
10. Benkert R, ObermeyerG, BentrupF. 1997. The turgor pressure of growing lily pollen tubes. Protoplasma 198: 1-8.
11. van den Berg B,Wain R, Dobson C, Ellis R. 2000. Macromolecular crowding perturbs protein refolding kinetics: implications for folding inside the cell. EMBO Journal 19: 3870-3875.
12. Bieleski R, Elgar J, Heyes J. 2000. Mechanical aspects of rapid flower opening in Asiatic lily. Annals of Botany 86: 1175-1183.
13. Bots M, Feron R, Uehlein N,Weterings K, Kaldenhoff R, Mariani T. 2005a. PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. Journal of Experimental Botany 56: 113-121.
14. Bots M, Vergeldt F, Wolters-Arts M, Weterings K, van As H, Mariani C. 2005b. Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco. Plant Physiology 137: 1049-1056.
15. BoursiacY, BoudetJ,PostaireO,LuuD,Tournaire-RouxC,Maurel C. 2008. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. The Plant Journal 56: 207-218.
16. Boyer J. 1966. Isopiestic technique: measurement of accurate leaf water potentials. Science 154: 1459-60.
17. Boyer J. 1995. Measuring the water status of plants and soils. San Diego, Academic Press.
18. Boyer J, Knipling E. 1965. Isopiestic technique for measuring leaf water potentials with a thermocouple psychrometer. Proceedings of the National Academy of Sciences, USA 54: 1044-1051.
19. Briegel A, Ladinsky M, Oikonomou C, et al. 2014. Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling. eLife 3: e02151.
20. Burch-Smith T, Zambryski P. 2012. Plasmodesmata paradigm shift: regulation from without versus within. Annual Review of Plant Biology 63: 239-260.
21. Cazalé AC, Rouet-Mayer MA, Barbier-Brygoo H, Mathieu Y, Laurière C. 1998. Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiology 116: 659-669.
22. ChaumontF,Tyerman S. 2014. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164: 1600-1618.
23. ChaumontF, MoshelionM,DanielsM.2005.Regulation of plant aquaporin activity. Biology of the Cell 97: 749-764.
24. Chebli Y, Geitmann A. 2007. Mechanical principles governing pollen tube growth. Functional Plant Science and Biotechnology 1: 232-245.
25. ChenW, Yin X,Wang L, et al. 2013. Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Molecular Biology 83: 219-233.
26. Colombani M, Forterre Y. 2011. Biomechanics of rapid movements in plants: poroelastic measurements at the cell scale. Computer Methods in Biomechanics and Biomedical Engineering 14: 115-117.
27. Coster H. 1976. Turgor pressure sensing in plant cell membranes. Plant Physiology 58: 636-643.
28. Dashek W, Harwood H. 1974. Proline, hydroxyproline, and lily pollen tube elongation. Annals of Botany 38: 947-959.
29. Dainty J. 1972. Plant cell-water relations: the elasticity of the cell wall. Proceedings of the Royal Society of Edinburgh. Section A. Mathematical and Physical Sciences 70: 89-93.
30. DelauneyA,Verma D. 1993. Proline biosynthesis and osmoregulation in plants. The Plant Journal 4: 215-223.
31. DengY, Sun M, Shaevitz J. 2011. Direct measurement of cellwall stress stiffening and turgor pressure in live bacterial cells. Physical Review Letters 107: 158101.
32. van Doorn W, Van Meeteren U. 2003. Flower opening and closure: a review. Journal of Experimental Botany 54: 1801-1812.
33. Dumais J, Forterre Y. 2012. 'Vegetable dynamicks': the role of water in plant movements. Annual Review of Fluid Mechanics 44: 453-478.
34. Ellis R. 2001. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Current opinion in structural biology 11: 114-9.
35. Fetter K, Van Wilder V, Moshelion M, Chaumont F. 2004. Interactions between plasma membrane aquaporins modulate their water channel activity. The Plant Cell 16: 215-228.
36. Forouzesh E, Goel A, Mackenzie SA, Turner JA. 2013. In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling. The Plant Journal 73: 509-520.
37. Forterre Y. 2013. Slow, fast and furious: understanding the physics of plant movements. Journal of Experimental Botany 64: 4745-4760.
38. Fricke W, Leigh R, Tomos A. 1994. Concentrations of inorganic and organic solutes in extracts from individual epidermal, mesophyll and bundle-sheath cells of barley leaves. Planta 192: 310-316.
39. FrickeW, Jarvis M, Brett C. 2000. Turgor pressure, membrane tension and the control of exocytosis in higher plants. Plant, Cell and Environment 23: 999-1003.
40. Geitmann A. 2006. Experimental approaches used to quantify physical parameters at cellular and subcellular levels. American Journal of Botany 93: 1380-1390.
41. Geitmann A, Ortega J. 2009. Mechanics and modeling of plant cell growth. Trends in Plant Science 14: 467-478.
42. GerbeauP,AmodeoG, HenzlerT, SantoniV, RipocheP,Maurel C. 2002. The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. The Plant Journal 30: 71-81.
43. Gerdenitsch W. 1984. Microscopic contributions to the pressure-volume diagram of the cell-water relations as demonstrated with tissue cells. Protoplasma 119: 35-47.
44. Gisel A, Barella S, Hempel F, Zambryski P. 1999. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126: 1879-1889.
45. Green P. 1968. Growth physics in Nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiology 43: 1169-1184.
46. GriffithsA,Parry A, JonesH,TomosA. 1996. Abscisic acid and turgor pressure regulation in tomato roots. Journal of Plant Physiology 149: 372-376.
47. HainesT. 1994.Water transport across biologicalmembranes.FEBSLetters 346: 115-122.
48. Hamant O, Traas J. 2010. The mechanics behind plant development. New Phytologist 185: 369-385.
49. Han X, Hyun T, Zhang M, et al. 2014. Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Developmental Cell 28: 132-146.
50. Hanson A, Kende H. 1975. Ethylene-enhanced ion and sucrose efflux in morning glory flower tissue. Plant Physiology 55: 663-669.
51. Harrington M, Razghandi K, Ditsch F, et al. 2011. Origami-like unfolding of hydro-actuated ice plant seed capsules. Nature Communications 2: 337.
52. Haydon M, Bell L,Webb A. 2011. Interactions between plant circadian clocks and solute transport. Journal of Experimental Botany 62: 2333-2348.
53. Hayot C, Forouzesh E, Goel A, Avramova Z, Turner J. 2012. Viscoelastic properties of cell walls of single living plant cells determined by dynamic nanoindentation. Journal of Experimental Botany 63: 2525-2540.
54. Henzler T, Steudle E. 2000. Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. Journal of Experimental Botany 51: 2053-66.
55. HenzlerT,Waterhouse R, Smyth A, et al. 1999. Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210: 50-60.
56. Hill A, Shachar-Hill B, Skepper J,Powell J, Shachar-HillY. 2012.Anosmotic model of the growing pollen tube. PloS One 7: e36585.
57. Holdaway-Clarke T,Walker N, Hepler P, Overall R. 2000. Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210: 329-335.
58. Hüsken D, Steudle E, Zimmermann U. 1978. Pressure probe technique for measuring water relations of cells in higher-plants. Plant Physiology 61: 158-163.
59. Imlau A, Truernit E, Sauer N. 1999. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. The Plant Cell 11: 309-322.
60. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K. 2001. The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. The Plant Cell 13: 2191-2209.
61. Javot H, Lauvergeat V, Santoni V, et al. 2003. Role of a single aquaporin isoform in root water uptake. The Plant Cell 15: 509-522.
62. Johanson U, Karlsson M, Johansson I, et al. 2001. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology 126: 1358-1369.
63. Johnson K, Chrispeels M. 1992. Tonoplast-bound protein kinase phosphorylates tonoplast intrinsic protein. Plant Physiology 100: 1787-1795.
64. Joshi A, KnipferT, Steudle E. 2009. Effects ofwater storage in the stele on measurements of the hydraulics of young roots of corn and barley. New Phytologist 184: 631-643.
65. Kamiya N, Tazawa M, Takata T. 1963. The relation of turgor pressure to cell volume in nitella with special reference to mechanical properties of the cell wall. Protoplasma 57: 501-521.
66. Keijzer C, Hoek I,Willemse M. 1987. The processes of anther dehiscence and pollen dispersal III. The dehydration of the filament tip and the anther in three monocotyledonous species. New Phytologist 106: 281-287.
67. Knipfer T, Das D, Steudle E. 2007. During measurements of root hydraulics with pressure probes, the contribution of unstirred layers is minimized in the pressure relaxation mode: comparison with pressure clamp and highpressure flowmeter. Plant, Cell and Environment 30: 845-860.
68. Kochian LV, Shaff JE, KühtreiberWM,Jaffe LF, Lucas WJ. 1992. Use of an extracellular, ion-selective, vibrating microelectrode system for the quantification of K+, H+, and Ca2+ fluxes in maize roots and maize suspension cells. Planta 188: 601-610.
69. Kolb K, Sperry J, Lamont B. 1996. A method for measuring xylem hydraulic conductance and embolism in entire root and shoot systems. Journal of Experimental Botany 47: 1805-1810.
70. Korolev A, Tomos A, Bowtell R, Farrar J. 2000. Spatial and temporal distribution of solutes in the developing carrot taproot measured at single-cell resolution. Journal of Experimental Botany 51: 567-577.
71. Kroeger J, Zerzour R, Geitmann A. 2011. Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PloS One 6: e18549.
72. Kühtreiber WM, Jaffe LF. 1990. Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. Journal of Cell Biology 110: 1565-1573.
73. Kumar MN, Jane WN, Verslues PE. 2013. Role of the putative osmosensor Arabidopsis Histidine Kinase1 in dehydration avoidance and low-waterpotential response. Plant Physiology 163: 942-953.
74. Lalonde S, Boles E, HellmannH, et al. 1999. The dual function of sugar carriers. Transport and sugar sensing. The Plant Cell 11: 707-726.
75. Lee S, Singh A, Chung G, Ahn S, Noh E, Steudle E. 2004. Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients. Physiologia Plantarum 120: 413-420.
76. Lei B, Huang Y, Sun J, et al. 2014. Scanning ion-selective electrode technique and X-ray microanalysis provide direct evidence of contrasting Na+ transport ability from root to shoot in salt-sensitive cucumber and salttolerant pumpkin under NaCl stress. Physiologia Plantarum (in press).
77. LiW, Zhao Y, Liu C, et al. 2012. Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cellmovement of Soybean mosaic virus. Plant Cell Reports 31: 905-916.
78. Liarzi O, Epel B. 2005. Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225: 67-76.
79. Lintilhac P,Wei C,Tanguay J, Outwater J. 2000. Ball tonometry: a rapid, nondestructive method for measuring cell turgor pressure in thin-walled plant cells. Journal of Plant Growth Regulation 19: 90-97.
80. Lockhart JA. 1965. An analysis of irreversible plant cell elongation. Journal of Thoeretical Biology 8: 264-275.
81. Lucas M, Kenobi K, vonWangenheim D, et al. 2013. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proceedings of the National Academy of Sciences, USA 110: 5229-5234.
82. Lucas W, Lee J. 2004. Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology 5: 712-726.
83. Ma N, Xue J, Li Y, et al. 2008. Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiology 148: 894-907.
84. Martre P, Morillon R, Barrieu F, North G, Nobel P, Chrispeels M. 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology 130: 2101-2110.
85. Matsui T, Omasa K, Horie T. 2000. Anther dehiscence in two-rowed barley (Hordeum distichum) triggered by mechanical stimulation. Journal of Experimental Botany 51: 1319-1321.
86. Mattioli R, Falasca G, Sabatini S, Altamura M, Costantino P, Trovato M. 2009. The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiologia Plantarum 137: 72-85.
87. Maurel C, Verdoucq L, Luu D, Santoni V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology 59: 595-624.
88. Meshcheryakov A, Steudle E, Komor E. 1992. Gradients of turgor, osmotic pressure, and water potential in the cortex of the hypocotyl of growing ricinus seedlings: effects of the supply of water from the xylem and of solutes from the Phloem. Plant Physiology 98: 840-852.
89. Messerli MA, Smith PJS, Lewis RC, Robinson KR. 2004. Chloride fluxes in lily pollen tubes: a critical reevaluation. The Plant Journal 40: 799-812.
90. Milani P, Braybrook S, Boudaoud A. 2013. Shrinking the hammer: micromechanical approaches to morphogenesis. Journal of Experimental Botany 64: 4651-4662.
91. Molz FJ, Boyer JS. 1978. Growth-induced water potentials in plant cells and tissues. Plant Physiology 62: 423-429.
92. Monshausen G, Haswell E. 2013. A force of nature: molecular mechanisms of mechanoperception in plants. Journal of Experimental Botany 64: 4663-4680.
93. Morgan J. 1984. Osmoregulation and water stress in higher plants. Annual Review of Plant Physiology 35: 299-319.
94. Munns R, Greenway H, Setter T, Kuo J. 1983. Turgor pressure, volumetric elastic modulus, osmotic volume and ultrastructure of Chlorella emersonii grown at high and low external NaCl. Journal of Experimental Botany 34: 144-155.
95. Murata K, Mitsuoka K, Hirai T, et al. 2000. Structural determinants of water permeation through aquaporin-1. Nature 407: 599-605.
96. Nelson M, Band L, Dyson R, et al. 2012. A biomechanical model of anther opening reveals the roles of dehydration and secondary thickening. New Phytologist 196: 1030-1037.
97. Niemietz C, Tyerman S. 2002. New potent inhibitors of aquaporins: silver and gold compoundsinhibit aquaporins of plant and humanorigin.FEBSLetters 531: 443-447.
98. Nonami H, Boyer J, Steudle E. 1987. Pressure probe and isopiestic psychrometer measure similar turgor. Plant Physiology 83: 592-595.
99. Oparka K, Prior D. 1992. Direct evidence for pressure-generated closure of plasmodesmata. The Plant Journal 2: 741-750.
100. Oparka K, Prior D, Wright K. 1995. Symplastic communication between primary and developing lateral roots of Arabidopsis thaliana. Journal of Experimental Botany 46: 187-197.
101. ParreE,GeitmannA. 2004.More than a leak sealant.Themechanical properties of callose in pollen tubes. Plant Physiology 137: 274-286.
102. Pei H, Ma N, Tian J, et al. 2013. An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiology 163: 775-791.
103. Perbal M, Haughn G, Saedler H, Schwarz-Sommer Z. 1996. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122: 3433-3441.
104. Péret B, Li G, Zhao J, et al. 2012. Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology 14: 991-998.
105. Peters W, Tomos A. 1996. The history of tissue tension. Annals of Botany 77: 657-665.
106. PostaireO, Tournaire-Roux C, Grondin A, et al. 2010.A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiology 152: 1418-1430.
107. Prado K, Maurel C. 2013. Regulation of leaf hydraulics: from molecular to whole plant levels. Frontiers in Plant Science 4: 255.
108. Prado K, Boursiac Y, Tournaire-Roux C, et al. 2013. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. The Plant Cell 25: 1029-1039.
109. RamahaleoT, Morillon R, Alexandre J, Lassalles J. 1999. Osmoticwater permeability of isolated protoplasts. Modifications during development. Plant Physiology 119: 885-896.
110. Rehman S, YunS. 2006. Developmental regulation of Kaccumulation in pollen, anthers, and papillae: are anther dehiscence, papillae hydration, and pollen swelling leading to pollination and fertilization in barley (Hordeum vulgare L.) regulated by changes in K concentration? Journal of Experimental Botany 57: 1315-1321.
111. Reid M, Evans R, Dodge L, Mor Y. 1989. Ethylene and silver thiosulfate influence opening of cut rose flowers. Journal of the American Society for Horticultural Science 114: 436-440.
112. Riesmeier J,Willmitzer L, FrommerW. 1994. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO Journal 13: 1-7.
113. Rinne P, van der Schoot C. 1998. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125: 1477-1485.
114. Robinson S, Burian A,Couturier E, et al. 2013. Mechanical control of morphogenesis at the shoot apex. Journal of Experimental Botany 64: 4729-4744.
115. Routier-Kierzkowska A, Smith R. 2012. Measuring the mechanics of morphogenesis. Current Opinion in Plant Biology 16: 25-32.
116. Routier-Kierzkowska A, Weber A, Kochova P, et al. 2012. Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiology 158: 1514-1522.
117. RuanY, Llewellyn D,FurbankR. 2001.The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. The Plant Cell 13: 47-60.
118. Rutschow H, Baskin T, Kramer E. 2011. Regulation of solute flux through plasmodesmata in the root meristem. Plant Physiology 155: 1817-1826.
119. Rygol J, Pritchard J, Zhu J, Tomos A, Zimmermann U. 1993. Transpiration induces radial turgor pressure gradients in wheat and maize roots. Plant Physiology 103: 493-500.
120. Sack L, Holbrook N. 2006. Leaf hydraulics. Annual Reviewof Plant Biology 57: 361-381.
121. Sack L, Melcher PJ, ZwienieckiMA,HolbrookNM.2002. The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53: 2177-2184.
122. SanatiNezhadA,GeitmannA. 2013. Thecellular mechanics of an invasive lifestyle. Journal of Experimental Botany 64: 4709-4728.
123. Scholander P, Hammel H, Hemmingsen E, Bradstreet E. 1964. Hydrostatic pressure and osmotic potential in leaves of mangroves and some other plants. Proceedings of the National Academy of Sciences, USA 52: 119-125.
124. Schwacke R, Grallath S, Breitkreuz K, et al. 1999. LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. The Plant Cell 11: 377-392.
125. Scott R, Spielman M, Dickinson H. 2004. Stamen structure and function. The Plant Cell 16 Suppl: S46-S60.
126. Sessions A,YanofskyM,Weigel D. 2000.Cell-cell signaling andmovement by the floral transcription factors LEAFY and APETALA1. Science 289: 779-782.
127. Shabala S, Lew R. 2002. 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 measurements. Plant Physiology 129: 290-299.
128. Shachar-Hill B, Hill A, Powell J, Skepper J, Shachar-Hill Y. 2013. Mercury-sensitive water channels as possible sensors of water potentials in pollen. Journal of Experimental Botany 64: 5195-5205.
129. Sibaoka T. 1969. Physiology of rapid movements in higher plants. Annual Review of Plant Physiology 20: 165-184.
130. Sivitz A,ReindersA,Ward J. 2008. Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiology 147: 92-100.
131. Stadler R, Truernit E, Gahrtz M, Sauer N. 1999. The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. The Plant Journal 19: 269-278.
132. Steudle E, Oren R, Schulze ED. 1987. Measurement of hydraulic conductivity, solute permeability, and of reflection coefficients of excised roots using the root pressure probe. Plant Physiology 84: 1220-1232.
133. Szabados L, Savouré A. 2010. Proline: a multifunctional amino acid. Trends in Plant Science 15: 89-97.
134. Taiz L, Zeiger E. 2010. Plant physiology, 5th edn. Sunderland, MA: Sinauer Associates.
135. Talbott L, Zeiger E. 1998. The role of sucrose in guard cell osmoregulation. Journal of Experimental Botany 49: 329-337.
136. Tang W, He Y, Tu L, et al. 2014. Down-regulating annexin gene GhAnn2 inhibits cotton fiber elongation and decreases Ca2+ influx at the cell apex. Plant Molecular Biology 85: 613-625
137. Tomos A, Leigh R. 1999. The pressure probe: a versatile tool in plant cell physiology. Annual Review of Plant Physiology and Plant Molecular Biology 50: 447-472.
138. Tournaire-Roux C, Sutka M, JavotH, et al. 2003. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425: 393-397.
139. Trolinder N, McmichaelB, Upchurch D. 1993.Water relations of cotton flower petals and fruit. Plant, Cell and Environment 16: 755-760.
140. Tsuda M, Tyree M. 2000. Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany 51: 823-828.
141. Tyree M, Hammel H. 1972. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23: 267-282.
142. TyreeM, Patiño S, Bennink J, Alexander J. 1995. Dynamic measurements of root hydraulic conductance using a high-pressure flowmeter in the laboratory and field. Journal of Experimental Botany 46: 83-94.
143. TyreeM, Nardini A, Salleo S, Sack L, El Omari B. 2005. The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? Journal of Experimental Botany 56: 737-744.
144. Urao T, Yakubov B, Satoh R, et al. 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. The Plant Cell 11: 1743-1754.
145. VaténA, Dettmer J,WuS, et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Developmental Cell 21: 1144-1155.
146. Vella D, Ajdari A,Vaziri A, BoudaoudA. 2012a. Indentation of ellipsoidal and cylindrical elastic shells. Physical Review Letters 109: 144302.
147. Vella D, Ajdari A, Vaziri A, Boudaoud A. 2012b. The indentation of pressurized elastic shells: from polymeric capsules to yeast cells. Journal of the Royal Society, Interface/the Royal Society 9: 448-455.
148. Verbruggen N, Hermans C. 2008. Proline accumulation in plants: a review. Amino Acids 35: 753-759.
149. Vermeer J, vonWangenheim D, Barberon M, et al. 2014.Aspatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343: 178-183.
150. Vogler H, Draeger C,Weber A, et al. 2012. The pollen tube: a soft shell with a hard core. The Plant Journal 73: 617-627.
151. Walley JW, Coughlan S, Hudson ME, et al. 2007. Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genetics 3: 1800-1812.
152. Wang L, Hukin D, Pritchard J, Thomas C. 2006. Comparison of plant cell turgor pressure measurement by pressure probe and micromanipulation. Biotechnology Letters 28: 1147-1150.
153. Watanabe T, Imada K, Yoshizawa K, et al. 2013. Glycine insertion makes yellow fluorescent protein sensitive to hydrostatic pressure. PLoS One 8: e73212.
154. Wendler S, Zimmermann U. 1982. A new method for the determination of hydraulic conductivity and cell volume of plant cells by pressure clamp. Plant Physiology 69: 998-1003.
155. Wolf S, Deom C, Beachy R, Lucas W. 1989. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246: 377-379.
156. Yang C, Xu Z, Song J, et al. 2007. Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. The Plant Cell 19: 534-548.
157. Yooyongwech S, Horigane A, Yoshida M, et al. 2008. Changes in aquaporin gene expression and magnetic resonance imaging of water status in peach tree flower buds during dormancy. Physiologia Plantarum 134: 522-533.
158. Zhang WH,Tyerman SD. 1999. Inhibition ofwater channels by HgCl2 in intact wheat root cells. Plant Physiolgy 120: 849-858.
159. ZimmermannU. 1978. Physics of turgor and osmoregulation. Annual Reviewof Plant Physiology 29: 121-148.
160. Zimmermann U, Hüsken D. 1979. Theoretical and experimental exclusion of errors in the determination of the elasticity and water transport parameters of plant cells by the pressure probe technique. Plant Physiology 64: 18-24.
161. Zimmermann U, Steudle E, Lelkes P. 1976. Turgor pressure regulation in Valonia utricularis: effect of cell wall elasticity and auxin. Plant Physiology 58: 608-613.
162. Zimmermann U, Rygol J, Balling A, Klöck G, Metzler A, Haase A. 1992. Radial turgor and osmotic pressure profiles in intact and excised roots of Aster tripolium: pressure probe measurements and nuclear magnetic resonance-imaging analysis. Plant Physiology 99: 186-196.