A redundant hydraulic function of root hairs in barley plants grown in hydroponics
Shannon Burke A , Emma Sadaune A * , Lisa Rognon A * , Alexane Fontana A * , Marianne Jourdrin A * and Wieland Fricke
A B
+ Author Affiliations
- Author Affiliations
A School of Biology and Environmental Sciences, University College Dublin, Belfield, Dublin 4, Republic of Ireland.
B Corresponding author. Email: wieland.fricke@ucd.ie
Functional Plant Biology - https://doi.org/10.1071/FP20287
Submitted: 10 September 2020 Accepted: 25 November 2020 Published online: 22 December 2020
Abstract
The root hair-less brb of Hordeum vulgare L. (bald root barley) mutant was used to assess the significance that root hairs have for the hydraulic properties of roots and response to a limited supply of mineral nutrients in plants grown on hydroponics. The barley brb mutant and its parent wild-type (H. vulgare cv. Pallas) were grown under nutrient sufficient control conditions, and under conditions of low supply of P and N. Plants were analysed when they were 14–18 days old. Root hydraulic conductivity (Lp) was determined for excised root systems and intact transpiring plants, and cell Lp was determined through cell pressure probe measurements. The formation of Casparian bands and suberin lamellae was followed through staining of cross-sections. The presence or absence of root hairs had no effect on the overall hydraulic response of plants to nutritional treatments. Root and cell Lp did not differ between the two genotypes. The most apparent difference between brb and wild-type plants was the consistently reduced formation of apoplastic barriers in brb plants. Any hydraulic function of root hairs can be redundant in barley, at least under the hydroponic conditions tested.
Keywords: barley, brb mutant, endodermis, Hordeum vulgare L., hydraulic conductivity, mineral nutrition, N deficiency, P deficiency, root hair.
References
Ahmed MA, Passioura J, Carminati A (2018) Hydraulic processes in roots and the rhizosphere pertinent to increasing yield of water-limited grain crops: a critical review Journal of Experimental Botany 69, 3255–3265.| Hydraulic processes in roots and the rhizosphere pertinent to increasing yield of water-limited grain crops: a critical reviewCrossref | GoogleScholarGoogle Scholar | 29767797PubMed |
Armand T, Cullen M, Boiziot F, Li L, Fricke W (2019) Cortex cell hydraulic conductivity, endodermal apoplastic barriers and root hydraulics change in barley (Hordeum vulgare L.) in response to a low supply of N and P. Annals of Botany 124, 1091–1107.
| Cortex cell hydraulic conductivity, endodermal apoplastic barriers and root hydraulics change in barley (Hordeum vulgare L.) in response to a low supply of N and P.Crossref | GoogleScholarGoogle Scholar | 31309230PubMed |
Barberon M (2017) The endodermis as a checkpoint for nutrients. New Phytologist 213, 1604–1610.
| The endodermis as a checkpoint for nutrients.Crossref | GoogleScholarGoogle Scholar |
Barberon M, Vermeer J, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447–459.
| Adaptation of root function by nutrient-induced plasticity of endodermal differentiation.Crossref | GoogleScholarGoogle Scholar | 26777403PubMed |
Besse M, Knipfer T, Miller AJ, Verdeil JL, Jahn TP, Fricke W (2011) Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. Journal of Experimental Botany 62, 4127–4142.
| Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves.Crossref | GoogleScholarGoogle Scholar | 21737414PubMed |
Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiology 150, 348–364.
| Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots.Crossref | GoogleScholarGoogle Scholar | 19321713PubMed |
Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Annals of Botany 110, 319–328.
| What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)?Crossref | GoogleScholarGoogle Scholar | 22539540PubMed |
Brundrett MC, Enstone DE, Peterson CA (1988) A berberine aniline blue staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146, 133–142.
| A berberine aniline blue staining procedure for suberin, lignin, and callose in plant tissue.Crossref | GoogleScholarGoogle Scholar |
Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry 66, 111–116.
| Efficient lipid staining in plant material with Sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol.Crossref | GoogleScholarGoogle Scholar |
Carminati A, Passioura JB, Zarebanadkouki M, Ahmed MA, Ryan PR, Watt M, Delhaize E (2017) Root hairs enable high transpiration rates in drying soils. New Phytologist 216, 771–781.
| Root hairs enable high transpiration rates in drying soils.Crossref | GoogleScholarGoogle Scholar |
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164, 1600–1618.
| Aquaporins: highly regulated channels controlling plant water relations.Crossref | GoogleScholarGoogle Scholar | 24449709PubMed |
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 | 10938796PubMed |
Coffey O, Bonfield R, Corre F, Sirigiri JA, Meng D, Fricke W (2018) Root and cell hydraulic conductivity, apoplastic barriers and aquaporin gene expression in barley (Hordeum vulgare L.) grown at low supply of potassium. Annals of Botany 122, 1131–1141.
| Root and cell hydraulic conductivity, apoplastic barriers and aquaporin gene expression in barley (Hordeum vulgare L.) grown at low supply of potassium.Crossref | GoogleScholarGoogle Scholar | 29961877PubMed |
Dodd IC, Diatloff E (2016) Enhanced root growth of the brb (bald root barley) mutant in drying soil allows similar shoot physiological responses to soil water deficit as wild‐type plants. Functional Plant Biology 43, 199–206.
| Enhanced root growth of the brb (bald root barley) mutant in drying soil allows similar shoot physiological responses to soil water deficit as wild‐type plants.Crossref | GoogleScholarGoogle Scholar | 32480453PubMed |
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 | 19369594PubMed |
Even M, Sabo M, Meng D, Kreszies T, Schreiber L, Fricke W (2018) Night-time transpiration in barley (Hordeum vulgare L.) facilitates respiratory carbon dioxide release and is regulated during salt stress. Annals of Botany 122, 569–582.
| Night-time transpiration in barley (Hordeum vulgare L.) facilitates respiratory carbon dioxide release and is regulated during salt stress.Crossref | GoogleScholarGoogle Scholar | 29850772PubMed |
Farr CH (1925) The formation of root hairs in water. Proceedings of the Iowa Academy of Science 32, 57–65.
Fricke W (2020) Energy costs of salinity tolerance in crop plants: night‐time transpiration and growth. New Phytologist 225, 1152–1165.
| Energy costs of salinity tolerance in crop plants: night‐time transpiration and growth.Crossref | GoogleScholarGoogle Scholar |
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 | 12011367PubMed |
Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low‐ and high‐P soils. Plant, Cell & Environment 26, 1759–1766.
| Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low‐ and high‐P soils.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
| A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake.Crossref | GoogleScholarGoogle Scholar |
Gambetta G, Knipfer T, Fricke W, McElrone AJ (2017) Aquaporins and root water uptake. In ‘Plant aquaporins’. (Eds F. Chaumont and S Tyerman.) pp. 133–153. (Springer Verlag: Heidelberg, Germany.)
Geldner N (2013) The endodermis. Annual Review of Plant Biology 64, 531–558.
| The endodermis.Crossref | GoogleScholarGoogle Scholar | 23451777PubMed |
Gitto A, Fricke W (2018) Zinc treatment of hydroponically-grown barley (H. vulgare) plants causes a reduction in root and cell hydraulic conductivity and isoform-dependent decrease in aquaporin gene expression. Physiologia Plantarum 164, 176–190.
| Zinc treatment of hydroponically-grown barley (H. vulgare) plants causes a reduction in root and cell hydraulic conductivity and isoform-dependent decrease in aquaporin gene expression.Crossref | GoogleScholarGoogle Scholar | 29381217PubMed |
Hepworth C, Caine RS, Harrison EL, Sloan J, Gray JE (2018) Stomatal development: focusing on the grasses. Current Opinion in Plant Biology 41, 1–7.
| Stomatal development: focusing on the grasses.Crossref | GoogleScholarGoogle Scholar | 28826033PubMed |
Jones H, Tomos AD, Leigh RA, Wyn Jones RG (1983) Water-relation parameters of epidermal and cortical cells in the primary root of Triticum aestivum L. Planta 158, 230–236.
| Water-relation parameters of epidermal and cortical cells in the primary root of Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar | 24264612PubMed |
Kano-Nakata M, Suralta RR, Niones JM, Yamauchi A (2012) Root sampling by using a root box–pinboard method. In ‘Methodologies for root drought studies in rice’. (Eds H. E. Shashidhar, A. Henry and B. Hardy.) p. 4. (International Rice Research Institute (IRRI): Manila, Philippines.)
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant & Cell Physiology 43, 885–893.
| Functional analysis of water channels in barley roots.Crossref | GoogleScholarGoogle Scholar |
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 L.). 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 L.).Crossref | GoogleScholarGoogle Scholar |
Knipfer T, Fricke W (2011) Water uptake by 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 by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 20974734PubMed |
Knipfer T, Besse M, Verdeil JL, Fricke W (2011) Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. Journal of Experimental Botany 62, 4115–4126.
| Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots.Crossref | GoogleScholarGoogle Scholar | 21441404PubMed |
Marzec M, Melzer M, Szarejko I (2015) Root hair development in the grasses: what we already know and what we still need to know. Plant Physiology 168, 407–414.
| Root hair development in the grasses: what we already know and what we still need to know.Crossref | GoogleScholarGoogle Scholar | 25873551PubMed |
Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiological Reviews 95, 1321–1358.
| Aquaporins in plants.Crossref | GoogleScholarGoogle Scholar | 26336033PubMed |
Meng D, Walsh M, Fricke W (2016) Rapid changes in root hydraulic conductivity and aquaporin expression in rice (Oryza sativa L.) in response to shoot removal – xylem tension as a possible signal. Annals of Botany 118, 809–819.
| Rapid changes in root hydraulic conductivity and aquaporin expression in rice (Oryza sativa L.) in response to shoot removal – xylem tension as a possible signal.Crossref | GoogleScholarGoogle Scholar | 27524161PubMed |
Munns R, Passioura JB (1984) Effect of prolonged exposure to NaCl on the osmotic pressure of leaf xylem sap from intact, transpiring barley plants. Australian Journal of Plant Physiology 11, 497–507.
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |
Rosene HF (1943) Quantitative measurements of the velocity of water absorption in individual root hairs by a microtechnique. Plant Physiology 18, 588–607.
| Quantitative measurements of the velocity of water absorption in individual root hairs by a microtechnique.Crossref | GoogleScholarGoogle Scholar | 16653878PubMed |
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 |
Segal E, Kushnir T, Mualem Y, Shani U (2008) Water uptake and hydraulics of the root hair rhizosphere. Vadose Zone Journal 7, 1027–1034.
| Water uptake and hydraulics of the root hair rhizosphere.Crossref | GoogleScholarGoogle Scholar |
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 |
Steudle E, Peterson CA (1998) How does water get through roots? Journal of Experimental Botany 49, 775–788.
Suku S, Knipfer T, Fricke W (2014) Do root hydraulic properties change during the early vegetative stage of plant development in barley (Hordeum vulgare)? Annals of Botany 113, 385–402.
| Do root hydraulic properties change during the early vegetative stage of plant development in barley (Hordeum vulgare)?Crossref | GoogleScholarGoogle Scholar | 24287810PubMed |
Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. Journal of Experimental Botany 65, 1497–1512.
| Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses.Crossref | GoogleScholarGoogle Scholar | 24501179PubMed |
Vandeleur RK, Sullivan W, Athman A, Jordans C, Gilliham M, Kaiser BN, Tyerman SD (2014) Rapid shoot‐to‐root signalling regulates root hydraulic conductance via aquaporins. Plant, Cell & Environment 37, 520–538.
| Rapid shoot‐to‐root signalling regulates root hydraulic conductance via aquaporins.Crossref | GoogleScholarGoogle Scholar |
