Root hydraulics in salt-stressed wheat
Wieland Fricke A E , Ehsan Bijanzadeh B , Yahya Emam C and Thorsten Knipfer A DA School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Ireland.
B Crop Production Department, College of Agriculture and Natural Resources of Darab, Shiraz University, Shiraz 71345, Iran.
C Crop Production and Plant Breeding Department, Agriculture College, Shiraz University, Shiraz 71345, Iran.
D Present address: Department of Viticulture and Enology, University of California Davis, CA 95616-5270, USA.
E Corresponding author. Email: wieland02fricke@yahoo.co.uk
Functional Plant Biology 41(4) 366-378 https://doi.org/10.1071/FP13219
Submitted: 25 July 2013 Accepted: 6 October 2013 Published: 14 November 2013
Abstract
The aim of the present study was to test whether salinity, which can impact through its osmotic stress component on the ability of plants to take up water, affects root water transport properties (hydraulic conductivity) in bread wheat (Triticum aestivum L). Hydroponically grown plants were exposed to 100 mM NaCl when they were 10–11 days old. Plants were analysed during the vegetative stage of development when they were 15–17 days old and the root system consisted entirely of seminal roots, and when they were 22–24 days old, by which time adventitious roots had developed. Root hydraulic conductivity (Lp) was determined through exudation experiments (osmotic Lp) on individual roots and the entire plant root system, and through experiments involving intact, transpiring plants (hydrostatic Lp). Salt stress caused a general reduction (40–80%) in Lp, irrespective of whether individual seminal and adventitious roots, entire root systems or intact, transpiring plants were analysed. Osmotic and hydrostatic Lp were in the same range. The data suggest that most radial root water uptake in wheat grown in the presence and absence of NaCl occurs along a pathway that involves the crossing of membranes. As wheat plants develop, a nonmembraneous (apoplast) pathway contributes increasingly to radial water uptake in control but not in NaCl-stressed plants.
Additional keywords: cell pressure probe, root hydraulic conductivity, salinity, transpiration, Triticum aestivum L., xylem tension.
References
Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63, 43–57.| Regulation of root water uptake under abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yms7rP&md5=30009a5f7ee07066a862aeec42f2af9eCAS | 21914658PubMed |
Azaizeh H, Steudle E (1991) Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiology 97, 1136–1145.
| Effects of salinity on water transport of excised maize (Zea mays L.) roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XotVKhsg%3D%3D&md5=c50ea79c135252b17738a8c56ee40e5cCAS | 16668500PubMed |
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 Physiology 99, 886–894.
| Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVOns7g%3D&md5=851f30a44c9b84d26cc5567444957902CAS | 16669016PubMed |
Bennett JM, Cortes PM (1985) Errors in measuring water potential of small samples resulting from water adsorption by thermocouple psychrometer chambers. Plant Physiology 79, 184–188.
| Errors in measuring water potential of small samples resulting from water adsorption by thermocouple psychrometer chambers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhs1Ggtw%3D%3D&md5=c131f0ee0cf1226cc95328c89437d8c9CAS | 16664367PubMed |
Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behaviour of roots. Plant Physiology 150, 348–364.
| Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behaviour of roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsL8%3D&md5=5f8d993aaae4bf678b6afc2d5fc4a23aCAS | 19321713PubMed |
Bramley H, Turner NC, Turner DW, Tyerman SD (2010) The contrasting influence of short-term hypoxia on the hydraulic properties of cells and roots of wheat and lupin. Functional Plant Biology 37, 183–193.
| The contrasting influence of short-term hypoxia on the hydraulic properties of cells and roots of wheat and lupin.Crossref | GoogleScholarGoogle Scholar |
Caird MA, Richards JH, Donovan LA (2007) Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiology 143, 4–10.
| Nighttime stomatal conductance and transpiration in C3 and C4 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Ohtw%3D%3D&md5=ed43ddb7cc168577a77c4ccaa46a5e98CAS | 17210908PubMed |
Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany 51, 61–70.
| Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXpslKjtw%3D%3D&md5=09cb1b46362f67f68ff0dde037632d02CAS | 10938796PubMed |
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 Physiology 150, 1093–1104.
| Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleiu78%3D&md5=5911a9ecbc3b5bd426ecdb8ecb7430d2CAS | 19369594PubMed |
Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21, 335–351.
| Root endodermis and exodermis: structure, function, and responses to the environment.Crossref | GoogleScholarGoogle Scholar |
Esau K (1965) ‘Plant anatomy.’ 2nd edn. (Wiley and Sons, Inc.: New York)
Frensch J, Steudle E (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiology 91, 719–726.
| Axial and radial hydraulic resistance to roots of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhvFansQ%3D%3D&md5=1691e8179e4fd27e6d6f17b9f2cdf908CAS | 16667092PubMed |
Fricke W (1997) Cell turgor, osmotic pressure and water potential in the upper epidermis of barley leaves in relation to cell location and in response to NaCl and air humidity. Journal of Experimental Botany 48, 45–58.
| Cell turgor, osmotic pressure and water potential in the upper epidermis of barley leaves in relation to cell location and in response to NaCl and air humidity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtleis7w%3D&md5=1f48e340502f324b71b7fe455e135d86CAS |
Fricke W (2012) Single-cell sampling and analysis (SICSA). In ‘Plant salt tolerance. Methods in molecular biology. Vol. 913’. (Eds S Shabala, TA Cuin) pp. 79–100 (Springer-Verlag: Berlin)
Fricke W, Peters WS (2002) The biophysics of leaf growth in salt-stressed barley: a study at the cell level. Plant Physiology 129, 374–388.
| The biophysics of leaf growth in salt-stressed barley: a study at the cell level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFSms7g%3D&md5=f30fcdf3950b5fd66fcb3ea8c5dd0236CAS | 12011367PubMed |
Fricke W, Leigh RA, Tomos AD (1996) The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. Journal of Experimental Botany 47, 1413–1426.
| The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslWlsrY%3D&md5=611d91e21b1d498e6017d7dd98d88a92CAS |
Garcia A, Rizzo CA, Ud-Din J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR (1997) Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium:potassium selectivity differs between rice and wheat. Plant, Cell & Environment 20, 1167–1174.
| Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium:potassium selectivity differs between rice and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVekt7k%3D&md5=898ee90995bcf770c1085b7ce91778b1CAS |
Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Annals of Botany 90, 301–313.
| The role of aquaporins in root water uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVOhu7k%3D&md5=db438916fd61923057ceea7515aa345cCAS | 12234142PubMed |
Joly RJ (1989) Effects of sodium chloride on the hydraulic conductivity of soybean root systems. Plant Physiology 91, 1262–1265.
| Effects of sodium chloride on the hydraulic conductivity of soybean root systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFGqu70%3D&md5=f952a950a20e3a951b95833cb0aaf6efCAS | 16667173PubMed |
Katsuhara M, Shibasaka M (2007) Barley root hydraulic conductivity and aquaporin expression in relation to salt tolerance. Soil Science and Plant Nutrition 53, 466–470.
| Barley root hydraulic conductivity and aquaporin expression in relation to salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVemsLzM&md5=a877672202c10b95c2cfd121e958bedfCAS |
Knipfer T, Fricke W (2010) Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare). New Phytologist 187, 159–170.
| Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare).Crossref | GoogleScholarGoogle Scholar | 20412443PubMed |
Knipfer T, Fricke W (2011) Water uptake of seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.). Journal of Experimental Botany 62, 717–733.
| Water uptake of seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyrsb%2FJ&md5=17dcfb2fc016bc7d61cf56150a619869CAS | 20974734PubMed |
Kramer PJ (1932) The absorption of water by root systems of plants. American Journal of Botany 19, 148–164.
| The absorption of water by root systems of plants.Crossref | GoogleScholarGoogle Scholar |
Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). Journal of Experimental Botany 62, 4215–4228.
| Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeit7jP&md5=406821eb6edbef667618853a790c994eCAS | 21558150PubMed |
Ktitorova IN, Skobeleva OV, Sharova EI, Ermakov EI (2002) Hydrogen peroxide appears to mediate a decrease in hydraulic conductivity in wheat roots under salt stress. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 49, 369–380.
| Hydrogen peroxide appears to mediate a decrease in hydraulic conductivity in wheat roots under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlGgtr8%3D&md5=94f01082828df95d6f706939d18dd4cdCAS |
Kuwagata T, Ishikawa-Sakurai J, Hayashi H, Nagasuga K, Fukushi K, Ahamed A, Takasugi K, Katsuhara M, Murai-Hatano M (2012) Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. Plant & Cell Physiology 53, 1418–1431.
| Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1egur3N&md5=7a0e5557cc316a87ef81a3f6848ccafaCAS |
Läuchli A, James RA, Huang CX, McCully M, Munns R (2008) Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion. Plant, Cell & Environment 31, 1565–1574.
| Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion.Crossref | GoogleScholarGoogle Scholar |
Laur J, Hacke U (2013) Transpirational demand affects aquaporin expression in poplar roots. Journal of Experimental Botany 64, 2283–2293.
| Transpirational demand affects aquaporin expression in poplar roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvV2nurw%3D&md5=82c43630e0e7b4e50735d5c7587ca720CAS | 23599275PubMed |
Malone M, Leigh RA, Tomos AD (1989) Extraction and analysis of sap from individual wheat leaf-cells - the effect of sampling speed on the osmotic pressure of extracted sap. Plant, Cell & Environment 12, 919–926.
| Extraction and analysis of sap from individual wheat leaf-cells - the effect of sampling speed on the osmotic pressure of extracted sap.Crossref | GoogleScholarGoogle Scholar |
Martínez-Ballesta MC, Aparicio F, Pallás V, Martínez V, Carvajal M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. Journal of Plant Physiology 160, 689–697.
| Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12872491PubMed |
Martre P, Cochard H, Durand J-L (2001) Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.). Plant, Cell & Environment 24, 65–76.
| Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.).Crossref | GoogleScholarGoogle Scholar |
Melcher PJ, Meinzer FC, Yount DE, Goldstein G, Zimmermann U (1998) Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe. Journal of Experimental Botany 49, 1757–1760.
Munns R (1993) Physiological processes limiting plant growth in saline soil: some dogmas and hypotheses. Plant, Cell & Environment 16, 15–24.
| Physiological processes limiting plant growth in saline soil: some dogmas and hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yjsr0%3D&md5=a884c868738a00c05e702ebf444e38dbCAS |
Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Australian Journal of Plant Physiology 22, 561–569.
| The significance of a two-phase growth response to salinity in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1erur0%3D&md5=2b6f1089b9e0e3ba5bd4f40b6d0c1989CAS |
Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
| Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1GlsrY%3D&md5=e52874acd87072d96bffb5975e10415bCAS | 16510517PubMed |
Pickard WF (2003) The riddle of root pressure. II. Root exudation at extreme osmolalities. Functional Plant Biology 30, 135–141.
| The riddle of root pressure. II. Root exudation at extreme osmolalities.Crossref | GoogleScholarGoogle Scholar |
Rodriguez P, Dell’Amico J, Morales D, Sánchez Blanco MJ, Alarcón JJ (1997) Effects of salinity on growth, shoot water relations and root hydraulic conductivity in tomato plants. Journal of Agricultural Sciences, Cambridge 128, 439–444.
| Effects of salinity on growth, shoot water relations and root hydraulic conductivity in tomato plants.Crossref | GoogleScholarGoogle Scholar |
Sakurai-Ishikawa J, Murai-Hatano M, Hayashi H, Ahamed A, Fukushi K, Matsumoto T, Kitagawa Y (2011) Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant, Cell & Environment 34, 1150–1163.
| Transpiration from shoots triggers diurnal changes in root aquaporin expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsVKhtbw%3D&md5=73825e8d276c0e49b07bca8b37f9f0e2CAS |
Schneider H, Zhu JJ, Zimmermann U (1997) Xylem and cell turgor pressure probe measurements in intact roots of glycophytes: transpiration induces a change in the radial and cellular reflection coefficients. Plant, Cell & Environment 20, 221–229.
| Xylem and cell turgor pressure probe measurements in intact roots of glycophytes: transpiration induces a change in the radial and cellular reflection coefficients.Crossref | GoogleScholarGoogle Scholar |
Shackel KA (1984) Theoretical and experimental errors for in situ measurements of plant water potential. Plant Physiology 75, 766–772.
| Theoretical and experimental errors for in situ measurements of plant water potential.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhsFyksw%3D%3D&md5=b3a6674f4eff14506c923f94aa5d873fCAS | 16663701PubMed |
Shackel KA, Brinckmann E (1985) In situ measurement of epidermal cell turgor, leaf water potential, and gas exchange in Tradescantia virginiana L. Plant Physiology 78, 66–70.
| In situ measurement of epidermal cell turgor, leaf water potential, and gas exchange in Tradescantia virginiana L.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhs1ekug%3D%3D&md5=89018acb9d51be9a76add3af3b8f3d26CAS | 16664210PubMed |
Steudle E (2000) Water uptake by plant roots: an integration of views. Plant and Soil 226, 45–56.
| Water uptake by plant roots: an integration of views.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVGrtw%3D%3D&md5=98e1fc885af80e4a312fcaefa093b55dCAS |
Steudle E, Peterson CA (1998) How does water get through roots? Journal of Experimental Botany 49, 775–788.
Tang AC, Boyer JS (2008) Xylem tension affects growth-induced water potential and daily elongation of maize leaves. Journal of Experimental Botany 59, 753–764.
| Xylem tension affects growth-induced water potential and daily elongation of maize leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1KhtL8%3D&md5=24d917663befd7bd73a62dc1a8f71645CAS | 18349050PubMed |
Tomos AD, Leigh RA (1999) The pressure probe: a versatile tool in plant cell physiology. Annual Review of Plant Physiology and Plant Molecular Biology 50, 447–472.
| The pressure probe: a versatile tool in plant cell physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yksbY%3D&md5=e79f2fa0bebe420c56ffd4e59b3f1c4cCAS | 15012216PubMed |
Tomos AD, Hinde P, Richardson P, Pritchard J, Fricke W (1994) Microsampling and measurements of solutes in single cells. In ‘Plant cell biology – a practical approach.’ (Eds N Harris, KJ Oparka) pp. 297–314. (IRL Press: Oxford)
Trillo N, Fernández RJ (2005) Wheat plant hydraulic properties under prolonged experimental drought: stronger decline in root-system conductance than in leaf area. Plant and Soil 277, 277–284.
| Wheat plant hydraulic properties under prolonged experimental drought: stronger decline in root-system conductance than in leaf area.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GlsLrI&md5=ddcad0502105ad0938e3d6be6db49837CAS |
Tsuda M, Tyree MT (2000) Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany 51, 823–828.
| Plant hydraulic conductance measured by the high pressure flow meter in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLY%3D&md5=19854ec3a656993197ecd43e60ce4188CAS | 10938875PubMed |
Tyerman SD, Oats P, Gibbs J, Dracup M, Greenway H (1989) Turgor-volume regulation and cellular water relations of Nicotiana tabacum roots grown in high salinities. Australian Journal of Plant Physiology 16, 517–531.
| Turgor-volume regulation and cellular water relations of Nicotiana tabacum roots grown in high salinities.Crossref | GoogleScholarGoogle Scholar |
Vandeleur RK, Sullivan W, Athman A, Jordans C, Gilliham M, Kaiser BN, Tyerman SD (2013) Rapid shoot-to-root signalling regulates hydraulic conductance via aquaporins. Plant, Cell & Environment
| Rapid shoot-to-root signalling regulates hydraulic conductance via aquaporins.Crossref | GoogleScholarGoogle Scholar |
Vysotskaya LB, Arkhipova TN, Timergalina LN, Dedov AV, Veselov SY, Kudoyarova GR (2004) Effect of partial root excision on transpiration, root hydraulic conductance and leaf growth in wheat seedlings. Plant Physiology and Biochemistry 42, 251–255.
| Effect of partial root excision on transpiration, root hydraulic conductance and leaf growth in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1Wnt70%3D&md5=90d9e3a4ddb7b6a35b79c44c36a2bd75CAS | 15051049PubMed |
Vysotskaya L, Hedley PE, Sharipova G, Veselov D, Kudoyarova G, Morris J, Jones HG (2010) Effect of salinity on water relations of wild barley plants differing in salt tolerance. AoB PLANTS 2010,
| Effect of salinity on water relations of wild barley plants differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 22476064PubMed |