Abstract
There exists an increasing number of reports which show that the gene transcript, and in some cases also protein level, of particular aquaporin (AQP) isoforms is higher in growing than in nongrowing plant tissues. This suggests that AQPs play a role in the process of cell expansion. The most likely role of AQPs is that of facilitating water inflow into cells as they expand to a multiple of their original volume. The question is whether this is the major role which AQPs play in expanding cells and whether expanding cells actually need AQPs given the rate at which they expand and the hydraulic conductivity (Lp) of their membranes. These questions are addressed in this chapter by using a combination of molecular (AQP), biophysical (Lp, driving forces and water potential difference), anatomical (apoplastic barriers) and physiological (cell dimensions and relative growth rates) data for growing plant tissues and cells. The focus of analyses is on growing root and leaf tissues and on plasma membrane intrinsic (PIPs) and tonoplast intrinsic proteins (TIPs). It is concluded that a high expression of AQPs and a high Lp in growing plant cells are required more for facilitating water transport at significant (and high) rates through cells and tissues rather than for facilitating water transport into cells to sustain the (comparatively smaller) water uptake rates required for the volume expansion of these cells.
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Abbreviations
- AQP:
-
Aquaporin
- Lp:
-
Hydraulic conductivity
- NIP:
-
Nodule-26 like intrinsic protein
- PIP:
-
Plasma membrane intrinsic protein
- SIP:
-
Small basic intrinsic protein.
- TIP:
-
Tonoplast intrinsic protein
- ΔΨ:
-
Water potential difference
- Ψ:
-
Water potential
References
Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjelbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484
Aslam U, Bashir A, Khatoon A, Cheema HMN (2013) Identification and characterization of plasma membrane aquaporins from Calotropis procera. J Zhejiang Univ-SC B 14(7):586–595
Azaizeh H, Gunse B, Steudle E (1992) Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiol 99:886–894
Balk PA, de Boer AD (1999) Rapid stalk elongation in tulip (Tulipa gesneriana L. cv. Apeldoorn) and the combined action of cold-induced invertase and the water-channel protein γTIP. Planta 209:346–354
Barrieu F, Thomas D, Marty-Mazars D, Charbonnier M, Marty F (1998) Tonoplast intrinsic proteins from cauliflower (Brassica oleracea L. var. botrytis): immunological analysis, cDNA cloning and evidence for expression in meristematic tissues. Planta 204:335–344
Beaudette PC, Chlup M, Yee J, Emery RJ (2007) Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl2 and ABA. J Exp Bot 58:1291–1300
Besse M, Knipfer T, Miller AJ, Verdeil J-L, Jahn TP, Fricke W (2011) Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J Exp Bot 62:4127–4142
Bouchabké O, Tardieu F, Simonneau T (2006) Leaf growth and turgor in growing cells of maize (Zea mays L.) respond to evaporative demand under moderate irrigation but not in water-saturated soil. Plant Cell Environ 29:1138–1148
Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J 56:207–218
Boyer JS (2001) Growth-induced water potentials originate from wall yielding during growth. J Exp Bot 52:1483–1488
Boyer JS, Silk WK (2004) Hydraulics of plant growth. Funct Plant Biol 31:761–773
Boyer JS, Cavalieri AJ, Schulze ED (1985) Control of the rate of cell enlargement: excision, wall relaxation, and growth-induced water potentials. Planta 163:527–543
Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806
Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol 150:348–364
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 4:1600–1618
Chaumont F, Barrieu F, Herman EM, Chrispeels MJ (1998) Characterization of a maize tonoplast aquaporin expressed in zones of cell division and elongation. Plant Physiol 117:1143–1152
Cosgrove DJ (1993) Water uptake by growing cells: an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int J Plant Sci 154:10–21
Ehlert C, Maurel C, Tardieu F, Simonneau T (2009) Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiol 150:1093–1104
Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351
Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228
Frangne N, Maeshima M, Schäffner AR, Mandel T, Martinoia E, Bonnemain JL (2001) Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212:270–278
Frensch J, Steudle E (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiol 91:719–726
Fricke W (2000) Water movement between epidermal cells of barley leaves – a symplastic connection? Plant Cell Environ 23:991–997
Fricke W (2002) Botanical briefing review: biophysical limitation of cell elongation in cereal leaves. Ann Bot 90:1–11
Fricke W, Flowers TJ (1998) Control of leaf cell elongation in barley. Generation rates of osmotic pressure and turgor, and growth-associated water potential gradients. Planta 206:53–65
Fricke W, Peters WS (2002) The biophysics of leaf growth in salt-stressed barley, a study at the cell level. Plant Physiol 129:1–15
Fricke W, McDonald AJS, Mattson-Djos L (1997) Why do leaves and leaf cells of N-limited barley elongate at reduced rates? Planta 202:522–530
Gambetta GA, Fei J, Rost TL, Knipfer T, Matthews MA, Shackel KA, Walker MA, McElrone AJ (2013) Water uptake along the length of grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol 163:1254–1265
Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323
Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 68:337–353
Hachez C, Veselov D, Ye Q, Reinhardt H, Knipfer T, Fricke W, Chaumont F (2012) Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. Plant Cell Environ 35:185–198
Hachez C, Veljanovski V, Reinhardt H, Guillaumont, Vanhee C, Chaumont F, Batako H (2014) The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation. Plant Cell 26:4974–4990
Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985
Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32
Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the barley (Hordeum vulgare L.) aquaporin gene family. PLoS ONE 10(6):e0128025. doi:10.1371/journal.pone.0128025
Hukin D, Doering-Saad C, Thomas CR, Pritchard J (2002) Sensitivity of cell hydraulic conductivity to mercury is coincident with symplasmic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215:1047–1056
Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güçlü J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522
Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–460
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893
Katsuhara M (2007) Molecular mechanisms of water uptake and transport in plant roots: research progress with water channel aquaporins. Plant Root 1:22–26
Knipfer T, Fricke W (2011) Water uptake by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.). J Exp Bot 62:717–733
Knipfer T, Besse M, Verdeil J-L, Fricke W (2011) Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J Exp Bot 62:4115–4126
Lee SH, Chung GC, Jang JY, Ahn SJ, Zwiazek JJ (2012) Overexpression of PIP2;5 aquaporin alleviates effects of low root temperature on cell hydraulic conductivity and growth in Arabidopsis. Plant Physiol 159:479–488
Lersten NR (1997) Occurrence of endodermis with a casparian strip in stem and leaf. Bot Rev 63:265–272
Li GW, Zhang MH, Cai WM, Sun WN, Su WA (2008) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49:1851–1858
Li DD, Ruan XM, Zhang J, Wu YJ, Wang XL, Li XB (2013) Cotton plasma membrane intrinsic protein 2s (PIP2s) selectively interact to regulate their water channel activities and are required for fibre development. New Phytol 199(3):695–707
Lockhart JA (1965) An analysis of irreversible plant cell growth. J Theor Biol 8:264–275
Lopez F, Bousser A, Sissoeff I, Gaspar M, Lachaise B, Hoarau J, Mahe A (2003) Diurnal regulation of water transport and aquaporin gene expression in maize roots: contribution of PIP2 proteins. Plant Cell Physiol 44:1384–1395
Ma N, Xue JQ, Li YH, Liu XJ, Dai FW, Jia WS, Luo YB, Gao JP (2008) Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol 148:894–907
Martre P, Bogeat-Triboulot MB, Durand JL (1999) Measurement of a growth-induced water potential gradient in tall fescue leaves. New Phytol 142:435–439
Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236
Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–2247
Miyamoto N, Ookawa T, Takahashi H, Hirasawa T (2002) Water uptake and hydraulic properties of elongation cells in hydrotropically bending roots of Pisum sativum L. Plant Cell Physiol 43:393–401
Muto Y, Segami S, Hayashi H, Sakurai J, Murai-Hatano M, Hattori Y, Ashikari M, Maeshima M (2011) Vacuolar proton pumps and aquaporins involved in rapid internode elongation of deepwater rice. Biosci Biotechnol Biochem 75:114–122
O’Brien TP, Carr DJ (1970) A suberized layer in the cell walls of the bundle sheath of grasses. Aust J Biol Sci 23:275–287
O’Brien TP, Kuo J (1975) Development of the suberized lamella in the mestome sheath of wheat leaves. Aust J Bot 23:783–794
Obroucheva NV, Sin’kevich IA (2010) Aquaporins and cell growth. Russ J Plant Physiol 57:153–165
Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and ABA effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149:2000–2012
Pritchard J (1994) The control of cell expansion in roots. New Phytol 127:3–26
Reinhardt H, Hachez C, Bienert MD, Beebo A, Swarup K, Voß U, Bouhidel K, Frigerio L, Schjoerring LK, Bennett MJ, Chaumont F (2016) Tonoplast aquaporins facilitate lateral root emergence. Plant Physiol 170:1640–1654
Richardson A, Franke R, Kerstiens G, Jarvis M, Schreiber L, Fricke W (2005) Cuticular wax deposition in barley leaves commences in relation to the point of emergence from sheaths of older leaves. Planta 222:472–483
Sade N, Shatil-Cohen A, Attia Z, Maurel C, Boursiac Y, Kelly G et al (2014) The role of plasma membrane aquaporins in regulating the bundle sheath-mesophyll continuum and leaf hydraulics. Plant Physiol 166:1609–1620
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577
Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39
Schüssler MD, Alexandersson E, Bienert GP, Kichey T, Laursen KH, Johanson U, Kjellbom P, Schjoerring JK, Jahn TP (2008) The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana. Plant J 56:756–767
Shatil-Cohen A, Attia Z, Moshelion M (2011) Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J 67:72–80
Steudle E (2000) Water uptake by plant roots:an integration of views. Plant Soil 226:46–56
Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788
Tang AC, Boyer JS (2002) Growth-induced water potentials and the growth of maize leaves. J Exp Bot 53:489–503
Touati M, Knipfer T, Visnovitz T, Kameli A, Fricke W (2015) Limitation of cell elongation in barley (Hordeum vulgare L.) leaves through mechanical and tissue-hydraulic properties. Plant Cell Physiol 56:1364–1373
Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397
Tyerman SD, Hatcher AI, West RJ, Larkum AWD (1984) Posidonia australis growing in altered salinities – leaf growth, regulation of turgor and the development of osmotic gradients. Aust J Plant Physiol 11:35–47
Van den Honert TH (1948) Water transport in plants as a catenary process. Disc Faraday Soc 3:146–153
Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460
Volkov V, Hachez C, Moshelion M, Draye X, Chaumont F, Fricke W (2007) Water permeability differs between growing and non-growing barley leaf tissues. J Exp Bot 58:377–390
Wei W, Alexandersson E, Golldack D, Miller AJ, Kjellbom PO, Fricke W (2007) HvPIP1;6, a barley (Hordeum vulgare L.) plasma membrane water channel particularly expressed in growing compared with non-growing leaf tissues. Plant Cell Physiol 48:1132–1147
Wu X, Lin J, Lin Q, Wang J, Schreiber L (2005) Casparian strips in needles are more solute-permeable than endodermal transport barriers in roots of Pinus bungeana. Plant Cell Physiol 46:1799–1808
Yang S, Cui L (2009) The action of aquaporins in cell elongation, salt stress and photosynthesis. Chin J Biotechnol 25:321–327
Ye Q, Holbrook NM, Zwieniecki MA (2008) Cell-to-cell pathway dominates xylem-epidermis hydraulic connection in Tradescantia fluminensis (Vell. Conc.) leaves. Planta 227:1311–1317
Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci U S A 104:12359–12364
Zhang WH, Tyerman SD (1991) Effect of low O2 concentration and azide on hydraulic conductivity and osmotic volume of the cortical-cells of wheat roots. Aust J Plant Physiol 18:603–613
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Fricke, W., Knipfer, T. (2017). Plant Aquaporins and Cell Elongation. In: Chaumont, F., Tyerman, S. (eds) Plant Aquaporins. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-49395-4_5
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