Abstract
Pollen is the male gametophyte of plants, and its major function is to deliver sperm cells to the ovules to ensure a successful fertilisation. Sperm cells are carried inside the pollen tube, a growth extension of the vegetative cell of pollen that grows through the stigma and style tissue. The elongation/growth of pollen tubes is a highly regulated biological process, and the uptake of water is thought to account for the enormous increase in cell volume. Water transport into the pollen grain initiates the transition from the quiescent mature to the active, rehydrated pollen grain and subsequently allows the large increase in volume during tube growth. To maintain the water uptake, internal pollen water potential has to be lower than the external water potential which can be achieved by lowering the turgor pressure, by increasing the internal osmotic pressure or by decreasing the external osmotic pressure. Uptake or synthesis of osmotic active compounds may be necessary to adapt the internal osmotic pressure due to changes in osmotic conditions during the tube's journey through the stigma tissue. Especially in periods of severe drought stress, the water potential of the stigma cells may drop, and thus water uptake into the pollen tube is distorted. The ability to sense and to adapt to osmotic conditions is therefore an important feature of the pollen to warrant a successful fertilisation and in consequence to ensure high crop yields.
Keywords
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Abbreviations
- AQP:
-
Aquaporin
- LP :
-
Hydraulic conductivity
- MIP:
-
Major intrinsic protein
- PIP:
-
Plasma membrane intrinsic protein
- PM:
-
Plasma membrane
- Pos :
-
Osmotic permeability
References
Alqudah AM, Samarah NH, Mullen RE (2011) Drought stress effect on crop pollination, seed set, yield and quality. Sustain Agric Rev 6:193–213. doi:10.1007/978-94-007-0186-1_6
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58
Beauzamy L, Nakayama N, Boudaoud A (2014) Flowers under pressure: ins and outs of turgor regulation in development. Ann Bot 114:1517–1533
Becker JD, Boavida LC, Carneiro J, Haury M, Feijo J (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characterictics of the pollen transcriptome. Plant Physiol 133:713–725
Benkert R, Obermeyer G, Bentrup F-W (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198:1–8
Bhargava S, Sawant K (2013) Drought stress adaption: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32
Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168
Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo J, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181
Bots M, Feron R, Uehlein N, Weterings K, Kaldenhoff R, Mariani C (2005) PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. J Exp Bot 56:113–121
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Boyer JS (1995) Measuring the water status of plants and soils. Academic Press, San Diego
Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764
Claeys H, Inzé D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol 162:1768–1779
Crowe JA, Hoekstra FA, Crowe LM (1989) Membrane phase transitions are responsible for imbibitional change in dry pollen. Proc Natl Acad Sci USA 86:520–523
Dainty J (1963) Water relations of plants. Adv Bot Res 1:279–326
Dearnaley JDW, Levina NN, Lew RR, Heath IB, Goring DR (1997) Interrelationships between cytoplasmic Ca2+ peaks, pollen hydration and plasma membrane conductances during compatible and incompatible pollinations of Brassica napus papillae. Plant Cell Physiol 38:985–999
Dixit R, Rizzo C, Nasrallah ME, Nasrallah JB (2001) The Brassica MIP-MOD gene encodes a functional water channel that is expressed in the stigma epidermis. Plant Mol Biol 45:51–62
Elleman CJ, Dickinson HG (1986) Pollen-stigma interactions in Brassica. IV. Structural organization in the pollen grains during hydration. J Cell Sci 80:141–157
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19
Fang X, Turner NC, Yan G, Li F, Siddique KHM (2010) Flower numbers, pod production, pollen viability, and pistil function are reduced and flower and pod abortion increased in chickpea (Cicer arietinum L.) under terminal drought stress. J Exp Bot 61:335–345
Feijó JA, Malhó R, Obermeyer G (1995) Ion dynamics and its possible role during in vitro pollen germination and tube growth. Protoplasma 187:155–167
Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro S, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 23(1):86–94
Firon N, Nepi M, Pacini E (2012) Water status and associated processes mark critical stages in pollen development and functioning. Ann Bot 109:1201–1213
Foley JA, Ramankutty N, Brauman KA, Dassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for cultivated planet. Nature 478:337–342
Gilbert N (2012) Water under pressure. Nature 483:256–257
Gordon-Kamm WJ, Steponkus PL (1984) Lamellar-to-hexagonal II phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Proc Natl Acad Sci USA 81:6373–6377
Heslop-Harrison J (1979) An interpretation of the hydrodynamics of pollen. Am J Bot 66:737–743
Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32
Hill AE, Shachar-Hill B, Skepper JN, Powell J, Shachar-Hill Y (2012) An osmotic model of the growing pollen tube. PLoS One 7:e36585. doi:10.1371/journal.pone.0036585
Hirano Y, Okimoto N, Kadohira I, Suematsu M, Yasuoka K, Yasui M (2010) Molecular mechanisms of how mercury inhibits water permeation through aquaporin-1: understanding by molecular dynamics simulation. Biophys J 98:1512–1519
Hoekstra FA, Crowe JH, Crowe LM (1991) Effect of sucrose on phase behaviour of membranes in intact pollen of Typha latifolia L., as measured with Fourier transform infrared spectroscopy. Plant Physiol 97:1073–1079
Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652
Hüsken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiol 61:158–163
Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820
Jäger K, Fabian A, Barnabas B (2008) Effect of water deficit and elevated temperature on pollen development of drought sensitive and tolerant winter wheat (Triticum aestivum L.) genotypes. Acta Biol Szeged 52:67–71
Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4. doi:10.3389/fpls.2013.00494
Katifori E, Alben S, Cerda E, Nelson DR, Dumais J (2010) Foldable structures and the natural design of pollen grains. Proc Natl Acad Sci USA 197:7635–7639
Kedem O, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246
Kramer PJ, Boyer JS (1995) Water relations in plants and soil. Academic Press, San Diego
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Lang V, Usadel B, Obermeyer G (2014) De novo sequencing and analysis of the lily pollen transcriptome: an open access data source for an orphan plant species. Plant Mol Biol 87:69–80
Linthilhac PM, Wei C, Tanguay JJ, Outwater JO (2000) Ball tonometry: a rapid, nondestructive method for measuring cell turgor pressure in thin-walled plant cells. J Plant Growth Regul 19:90–97
Loraine AE, McCormick S, Estrada A, Patel K, Qin P (2013) RNA-Seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162:1092–1109
Ludewig U, Dynowski M (2009) Plant aquaporin selectivity: where transport assays, computer simulations and physiology meet. Cell Mol Life Sci 66:3161–3175
Lush WM, Grieser F, Wolters-Arts M (1998) Directional guidance of Nicotiana alata pollen tubes in vitro and on the stigma. Plant Physiol 118:733–741
Ma J-F, Liu Z-H, Chu C-P, Hu Z-Y, Wang X-L, Zhang XS (2012) Different regulatory processes control pollen hydration and germination in Arabidopsis. Sex Plant Reprod 25:77–82
Malhó R, Pais MSS (1992) Kinetics and hydrodynamics of Agapanthus umbellatus pollen tube growth: a structural and stereological study. Sex Plant Reprod 5:163–168
Manjarrez-Sandoval P, Gonzalez-Hernandez VA, Mendoza-Onofre LE, Engelman EM (1989) Drought stress effects on the grain yield and panicle development of sorghum. Can J Plant Sci 69:631–641
Marin-Olivier M, Chevalier T, Fobis-Loisy I, Dumas C, Gaude T (2000) Aquaporin PIP genes are not expressed in the stigma papillae in Brassica napus. Plant J 24:231–240
Mascarenhas JP (1993) Molecular mechanisms of pollen tube growth and differentiation. Plant Cell 5:1303–1314
Matsui T, Omasa K, Horie T (2000) Rapid swelling of pollen grains in the dehiscing anther of two-rowed barley (Hordeum distichum L. emed. LAM.) Ann Bot 85:345–350
Maurel C, Boursiac Y, Luu D-T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:3121–1358
Mayfield JA, Preuss D (2000) Rapid initiation of Arabidopsis pollination requires the oleosin domain protein GRP17. Nat Cell Biol 2:128–130
Messerli M, Robinson KR (2003) Ionic and osmotic disruption of the lily pollen tube oscillator: testing proposed models. Planta 217:147–157
Miermont A, Uhlendorf J, McClean M, Hersen P (2011) The dynamic systems properties of the HOG signaling cascade. J Signal Transduct. doi:10.1155/2011/930940
Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 64:4651–4662
Mizuta Y, Higashijima T (2014) Antisense gene inhibition by phosphorothioate antisense oligonucleotide in Arabidopsis pollen tubes. Plant J 78:516–528
Moshelion M, Moran N, Chaumont F (2004) Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol 135:2301–2317
Moutinho A, Camacho L, Haley A, Salomé-Pais M, Trewavas A, Malhó R (2001) Antisense perturbation of protein function in living pollen tubes. Sex Plant Reprod 14:101–104
Murai-Hatano M, Kuwagata T (2007) Osmotic water permeability of plasma and vacuolar membrane in protoplasts. I. High osmotic water permeability in radish (Raphanus sativus) root cells as measured by a new method. J Plant Res 120:175–189
Murphy R, Smith JAC (1998) Determination of cell water-relation parameters using the pressure probe: extended theory and practice of the pressure-clamp technique. Plant Cell Environ 21:637–657
Muzzey D, Gomez-Uribe CA, Mettetal JT, van Oudenaarden A (2009) A systems-level analysis of perfect adaption in yeast osmoregulation. Cell 138:160–171
Nezhad AS, Naghavi M, Packirisamy M, Bhata R, Geitmann A (2013) Quantification of the Young’s modulus of the primary plant cell wall using Bending-Lab-On-Chip (BLOC). Lab Chip 13:2599–2608
Niemietz CM, Tyerman SD (2002) New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Lett 531:443–447
Nobel PS (2009) Physicochemical and environmental plant physiology, 4th edn. Academic Press, Oxford
Obermeyer G, Fragner L, Lang V, Weckwerth W (2013) Dynamic adaption of metabolic pathways during germination and growth of lily pollen tubes after inhibition of the lectron transport chain. Plant Physiol 162:1822–1833
Okono A, Monneveux P, Ribaut J-M (2013) Facing the challenges of global agriculture today: what can we do about drought? Front Physiol 4. doi:10.3389/fphys.2013.00289
Onsager L (1931) Reciprocal relations in irreversible processes. Phys Rev 37:405–426
Patil BS, Ravikumar RL (2011) Osmotic adjustment in pollen grains: measure of drought adaptation in sorghum? Curr Sci 100:377–382
Pertl H, Schulze WX, Obermeyer G (2009) The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen. J Proteome Res 8:5142–5152
Pertl H, Poeckl M, Blaschke C, Obermeyer G (2010) Osmoregulation in Lilium pollen grains occurs via modulation of the plasma membrane H+ ATPase activity by 14-3-3 proteins. Plant Physiol 154:1921–1928
Pertl-Obermeyer H, Schulze WX, Obermeyer G (2014) In vivo cross-linking combined with mass spectrometry analysis reveals receptor-like kinases and Ca2+ signalling proteins as putative interaction partners of pollen plasma membrane H+ ATPases. J Proteomics 108:17–29
Potocky M, Jones MA, Bezvoda R, Smirnoff N, Zarsky V (2007) Reactive oxigen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751
Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5. doi:10.1371/journal.pgen.1000621
Ramahaleo T, Morillon R, Alexandre J, Lassalles J-P (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119:885–896
Rehman S, Yun SJ (2006) Developmental regulation of K accumulation 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? J Exp Bot 57:1315–1321
Rehman S, Rha ES, Ashraf M, Lee KJ, Yun SJ, Kwak YG, Yoo NH, Kim J-K (2004) Does barley (Hordeum vulgaris L.) pollen swell in fractions of a second? Plant Sci 167:137–142
Reinhard H, Hachez C, Bienert MD, Beebo A, Swarup K, Voß U, Bouhidel K, Frigerio L, Schjoerring JK, Bennett MJ, Chaumont F (2016) Tonoplast aquaporins facilitate lateral root emergence. Plant Physiol 170:1640–1654
Richards FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–300
Routier-Kierzkowska A-L, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS (2012) Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol 158:1514–1522
Ruiter RK, van Eldik GJ, van Herpen RMA, Schrauwen JAM, Wullems GJ (1997) Characterization of oleosins in the pollen coat of Brassica oleracea. Plant Cell 9:1621–1631
Saragih AA, Puteh AB, Ismail MR, Mondal MMA (2013) Pollen quality traits of ciltivated (Oryza sativa L. ssp. indica) and weedy (Oryza sativa L. ssp. nivara) rice to water stress at reproductive stage. Aust J Crop Sci 7:1106–1112
Sarker RH, Elleman CJ, Dickinson HG (1988) Control of pollen hydration in Brassica requires continued protein synthesis, and gylcosylation is necessary for intraspecific incompatibility. Proc Natl Acad Sci USA 85:4340–4344
Schütz K, Tyerman SD (1997) Water channels in Chara corallina. J Exp Bot 48:1511–1518
Shabala S, Lew RR (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 Physiol 129:290–299
Shachar-Hill B, Hill AE, Powell J, Skepper JN, Shachar-Hill Y (2013) Mercury-sensitive water channels as possible sensors of water potentials in pollen. J Exp Bot 64:5195–5205
Sommer A, Mahlknecht G, Obermeyer G (2007) Measuring the osmotic water permeability of the plant protoplast plasma membrane: implications of the non-osmotic volume. J Membr Biol 215:111–123
Sommer A, Geist B, Da Ines O, Gehwolf R, Schäffner AR, Obermeyer G (2008) Ectopic expression of Arabidopsis thaliana plasma membrane intrinsic protein 2 aquaporins in lily pollen increases the plasma membrane water permeability of grain but not of tube protoplasts. New Phytol 180:787–797
Soto G, Alleva K, Mazella MA, Amodeo G, Muschietti JP (2008) AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett 582:4077–4082
Steudle E (1989) Water flow in plants and its coupling to other processes: an overview. Methods Enzymol 174:183–225
Steudle E (1993) Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell, tissue, and organ level. In: Smith JAC, Griffiths H (eds) Water deficits: plant responses from cell to community. Bios Scientific, Oxford, pp 5–36
Steudle E, Tyerman SD (1983) Determination of permeability coefficients, reflection coefficients, and hydraulic conductivity of Chara corallina using the pressure probe: effects of solute concentration. J Mol Biol 75:85–96
Tiwari SC, Polito VS, Webster BD (1990) In dry peer (Pyrus communis) pollen, membranes assume a tighly packed multilamellate aspect that disappears rapidly upon hydration. Protoplasma 153:157–168
Tomos AD, Leigh RA (1999) The pressure probe: a versatile tool in plant cell physiology. Annu Rev Plant Physiol Plant Mol Biol 50:447–472
Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF (2013) A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161:1010–1020
Updegraff EP, Zhao F, Preuss D (2009) The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sex Plant Reprod 22:197–204
Vogler H, Draeger C, Weber A, Felekis D, Eichenberger C, Routier-Kierzkowska A-L, Boisson-Dernier A, Ringli C, Nelson BJ, Smith RS, Grossniklaus U (2013) The pollen tube: a soft shell with a hard core. Plant J 73:617–627
Wegner LH (2015) A thermodynamic analysis of the feasibility of water secretion into xylem vessels against a water potential gradient. Funct Plant Biol 42:828–835
Wilson C, Voronin V, Touraev A, Vicente O, Heberle-Bors E (1997) A developmental regulated MAP kinase activated by hydration in tobacco pollen. Plant Cell 9:2093–2100
Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369
Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2011) Pollen tubes and the physical world. Trends Plant Sci 16:353–355
Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen tube growth. Nature 392:818–821
Wu XN, Sanchez Rodriguez C, Pertl-Obermeyer H, Obermeyer G, Schulze WX (2013) Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis. Mol Cell Proteomics 12:2856–2873
Wudick MM, Luu D-T, Tournaire-Roux C, Sakamoto W, Maurel C (2014) Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol 164:1697–1706
Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446
Zeuthen T (1995) Molecular mechanisms for passive and active transport of water. Int Rev Cytol 160:99–161
Zimmermann U (1989) Water relations of plant cells: pressure probe technnique. Methods Enzymol 174:338–366
Zonia L, Munnik T (2004) Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol 134:813–823
Zonia L, Munnik T (2007) Life under pressure: hydrostatic pressure in cell growth and function. Trends Plant Sci 12:90–97
Zonia L, Munnik T (2009) Uncovering hidden treasures in pollen tube growth mechanics. Trends Plant Sci 14:318–327
Zonia L, Müller M, Munnik T (2006) Hydrodynamics and cell volume oscillations in the pollen tube apical region are integral components of the biomechanics of Nicotiana tabacum pollen tube growth. Cell Biochem Biophys 46:209–232
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Obermeyer, G. (2017). Water Transport in Pollen. In: Obermeyer, G., Feijó, J. (eds) Pollen Tip Growth. Springer, Cham. https://doi.org/10.1007/978-3-319-56645-0_2
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