Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Conservative water use under high evaporative demand associated with smaller root metaxylem and limited trans-membrane water transport in wheat

Rémy Schoppach A , Diego Wauthelet B , Linda Jeanguenin C and Walid Sadok A D
+ Author Affiliations
- Author Affiliations

A Earth and Life Institute-Agronomy, Université catholique de Louvain, Croix du Sud 2, L7.05.14, 1348 Louvain-la-Neuve, Belgium.

B Graduate School of Biological, Agricultural and Environmental Engineering, Université catholique de Louvain, Belgium.

C Institut des Sciences de la Vie, Université catholique de Louvain, Croix du Sud 4, L7.07.14, 1348 Louvain-la-Neuve, Belgium.

D Corresponding author. Email: walid.sadok@uclouvain.be

Functional Plant Biology 41(3) 257-269 https://doi.org/10.1071/FP13211
Submitted: 19 July 2013  Accepted: 23 September 2013   Published: 6 November 2013

Abstract

Efficient breeding of drought-tolerant wheat (Triticum spp.) genotypes requires identifying mechanisms underlying exceptional performances. Evidence indicates that the drought-tolerant breeding line RAC875 is water-use conservative, limiting its transpiration rate (TR) sensitivity to increasing vapour pressure deficit (VPD), thereby saving soil water moisture for later use. However, the physiological basis of the response remains unknown. The involvement of leaf and root developmental, anatomical and hydraulic features in regulating high-VPD, whole-plant TR was investigated on RAC875 and a drought-sensitive cultivar (Kukri) in 12 independent hydroponic and pot experiments. Leaf areas and stomatal densities were found to be identical between lines and de-rooted plants didn’t exhibit differential TR responses to VPD or TR sensitivity to four aquaporin (AQP) inhibitors that included mercury chloride (HgCl2). However, intact plants exhibited a differential sensitivity to HgCl2 that was partially reversed by β-mercaptoethanol. Further, root hydraulic conductivity of RAC875 was found to be lower than Kukri’s and root cross-sections of RAC875 had significantly smaller stele and central metaxylem diameters. These findings indicate that the water-conservation of RAC875 results from a root-based hydraulic restriction that requires potentially heritable functional and anatomical features. The study revealed links between anatomical and AQP-based processes in regulating TR under increasing evaporative demand.

Additional keywords: aquaporins, drought tolerance, hydraulic restriction, transpiration.


References

Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.

Babé A, Lavigne T, Séverin JP, Nagel KA, Walter A, Chaumont F, Batoko H, Beekman T, Draye X (2012) Repression of early lateral root initiation events by transient water deficit in barley and maize. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 1534–1541.
Repression of early lateral root initiation events by transient water deficit in barley and maize.Crossref | GoogleScholarGoogle Scholar | 22527396PubMed |

Bennett D, Reynolds M, Mullan D, Izanloo A, Kuchel H, Langridge P, Schnurbusch T (2012) Detection of two major grain yield QTL in bread wheat (Triticum aestivum L.) under heat, drought and high yield potential environments. Theoretical and Applied Genetics 125, 1473–1485.
Detection of two major grain yield QTL in bread wheat (Triticum aestivum L.) under heat, drought and high yield potential environments.Crossref | GoogleScholarGoogle Scholar | 22772727PubMed |

Bonneau J, Taylor J, Parent B, Bennett D, Reynolds M, Feuillet C, Langridge P, Mather D (2013) Multi-environment analysis and improved mapping of a yield-related QTL on chromosome 3B of wheat. Theoretical and Applied Genetics 126, 747–761.
Multi-environment analysis and improved mapping of a yield-related QTL on chromosome 3B of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtlWrsrg%3D&md5=93b758cac047457bc42a7482e0abdc58CAS | 23262551PubMed |

Boursiac Y, Chen S, Luu D-T, Sorieul M, Van Den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology 139, 790–805.
Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCgsb7I&md5=a33150b1e4cf10670e11f666fc1bb783CAS | 16183846PubMed |

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 | 1:CAS:528:DC%2BD1MXlvFahsL8%3D&md5=5f8d993aaae4bf678b6afc2d5fc4a23aCAS | 19321713PubMed |

Brenchley R, Spannagl M, Pfeifer M, Barker GLA, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo M-C, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705–710.
Analysis of the bread wheat genome using whole-genome shotgun sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCnu7nL&md5=48bdc7dc27f9f616020a2f82a72bda96CAS | 23192148PubMed |

Brisson N, Gate P, Gouache D, Charmet G, Oury F-X, Huard F (2010) Why are wheat yields stagnating in Europe? A comprehensive data analysis for France. Field Crops Research 119, 201–212.
Why are wheat yields stagnating in Europe? A comprehensive data analysis for France.Crossref | GoogleScholarGoogle Scholar |

Carpentieri-Pipolo V, Pipolo AE, Abdel-Haleem H, Boerma HR, Sinclair TR (2012) Identification of QTLs associated with limited leaf hydraulic conductance in soybean. Euphytica 186, 679–686.
Identification of QTLs associated with limited leaf hydraulic conductance in soybean.Crossref | GoogleScholarGoogle Scholar |

Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199, 372–381.
Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFGlsLw%3D&md5=6cff4e3fb0a64ee8ffb0398816ad8751CAS |

Chenu K, Deihimfard R, Chapman SC (2013) Large-scale characterization of drought pattern: a continent-wide modelling approach applied to the Australian wheatbelt – spatial and temporal trends. New Phytologist 198, 801–820.
Large-scale characterization of drought pattern: a continent-wide modelling approach applied to the Australian wheatbelt – spatial and temporal trends.Crossref | GoogleScholarGoogle Scholar | 23425331PubMed |

Condon AG, Farquhar GD, Richards RA (1990) Genotypic variation in carbon isotope discrimination and transpiration efficiency in wheat. Leaf gas exchange and whole-plant studies. Australian Journal of Plant Physiology 17, 9–22.
Genotypic variation in carbon isotope discrimination and transpiration efficiency in wheat. Leaf gas exchange and whole-plant studies.Crossref | GoogleScholarGoogle Scholar |

Devi MJ, Sadok W, Sinclair TR (2012) Transpiration response of de-rooted peanut plants to aquaporin inhibitors. Environmental and Experimental Botany 78, 167–172.
Transpiration response of de-rooted peanut plants to aquaporin inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisFGisbo%3D&md5=dabf5f8da0484b388ba19a35e71de8f4CAS |

Fletcher AL, Sinclair TR, Allen LH (2007) Transpiration responses to vapour pressure deficit in well watered ‘slow-wilting’ and commercial soybean. Environmental and Experimental Botany 61, 145–151.
Transpiration responses to vapour pressure deficit in well watered ‘slow-wilting’ and commercial soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvF2qtb8%3D&md5=2f99c27966e6fa1cc682beb099cb9a41CAS |

Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. Journal of Experimental Botany 61, 3211–3222.
Genetic and genomic tools to improve drought tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVymsLc%3D&md5=a98e802d83dfa9b9c9067ee56eba2d86CAS | 20525798PubMed |

Frick A, Järvå M, Ekvall M, Uzdavinys P, Nyblom M, Törnroth-Horsefield S (2013) Mercury increases water permeability of a plant aquaporin through a non-cysteine related mechanism. Biochemical Journal 454, 491–499.
Mercury increases water permeability of a plant aquaporin through a non-cysteine related mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGmt7jF&md5=e0ce88190330a18fbfc70e5fc01d6e51CAS | 23819815PubMed |

Gholipoor M, Prasad PVV, Mutava RN, Sinclair TR (2010) Genetic variability of transpiration response to vapor pressure deficit among sorghum genotypes. Field Crops Research 119, 85–90.
Genetic variability of transpiration response to vapor pressure deficit among sorghum genotypes.Crossref | GoogleScholarGoogle Scholar |

Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WTB, Wojciechowski T, Young IM (2009) Root phenomics of crops: opportunities and challenges. Functional Plant Biology 36, 922–929.
Root phenomics of crops: opportunities and challenges.Crossref | GoogleScholarGoogle Scholar |

Henry A, Cal AJ, Batoto TC, Torres RO, Serraj R (2012) Root attributes affecting water uptake of rice (Oryza sativa) under drought. Journal of Experimental Botany 63, 4751–4763.
Root attributes affecting water uptake of rice (Oryza sativa) under drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1KjsLbI&md5=f5ea588b481f174bb8fa7c208a25fd48CAS | 22791828PubMed |

Izanloo A, Condon AG, Langridge P, Tester M, Schnurbusch T (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. Journal of Experimental Botany 59, 3327–3346.
Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWit7rE&md5=69b3533b8d50a8667129b2837cac2da6CAS | 18703496PubMed |

Kholová J, Hash CT, Kumar PL, Yadav RS, Kocova M, Vadez V (2010) Terminal drought-tolerant pearl millet (Pennisetum glaucum (L.) R.Br.) have high leaf ABA and limit transpiration at high vapour pressure deficit. Journal of Experimental Botany 61, 1431–1440.
Terminal drought-tolerant pearl millet (Pennisetum glaucum (L.) R.Br.) have high leaf ABA and limit transpiration at high vapour pressure deficit.Crossref | GoogleScholarGoogle Scholar | 20142425PubMed |

Langridge P (2012) Genomics: decoding our daily bread. Nature 491, 678–680.
Genomics: decoding our daily bread.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCntLzK&md5=fa5f23a263a755b1e21012db526a73d6CAS | 23192142PubMed |

Lopes MS, Reynolds MP (2010) Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Functional Plant Biology 37, 147–156.
Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat.Crossref | GoogleScholarGoogle Scholar |

Monneveux P, Jing R, Misra SC (2012) Phenotyping for drought adaptation in wheat using physiological traits. Frontiers in Physiology 3, 429
Phenotyping for drought adaptation in wheat using physiological traits.Crossref | GoogleScholarGoogle Scholar | 23181021PubMed |

Munns R, James RA, Sirault XRR, Furbank RT, Jones HG (2010) New phenotyping methods for screening wheat and barley for beneficial responses to water deficit. Journal of Experimental Botany 61, 3499–3507.
New phenotyping methods for screening wheat and barley for beneficial responses to water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7jJ&md5=a67dee7bccdf032afecb6c53bbe5a30bCAS | 20605897PubMed |

Nagel KA, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Blossfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert AK, Galinski A, Scharr H, Fiorani F, Schurr U (2012) GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Functional Plant Biology 39, 891–904.
GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons.Crossref | GoogleScholarGoogle Scholar |

Niemietz CM, Tyerman SD (2002) New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Letters 531, 443–447.
New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFCksL0%3D&md5=7da9253f33048438cef90e1dd328bcfeCAS | 12435590PubMed |

Passioura JB (1972) The effect of root geometry on the yield of wheat growing on stored water. Australian Journal of Agricultural Research 23, 745–752.
The effect of root geometry on the yield of wheat growing on stored water.Crossref | GoogleScholarGoogle Scholar |

Przedpełska-Wasowicz E, Wierzbicka M (2011) Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma 248, 663–671.
Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells.Crossref | GoogleScholarGoogle Scholar | 20960016PubMed |

Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, Lutts S, Lefèvre I (2012) Combined transcriptomic and physiological approaches reveal strong differences between short- and long-term response of rice (Oryza sativa) to iron toxicity. Plant, Cell & Environment 35, 1837–1859.
Combined transcriptomic and physiological approaches reveal strong differences between short- and long-term response of rice (Oryza sativa) to iron toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht12itrvK&md5=0ddd3b4ba7115de8a1d1ea4f66346edcCAS |

Rebetzke GJ, Rattey AR, Farquhar GD, Richards RA, Condon ATG (2013) Genomic regions for canopy temperature and their genetic association with stomatal conductance and grain yield in wheat. Functional Plant Biology 40, 14–33.
Genomic regions for canopy temperature and their genetic association with stomatal conductance and grain yield in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVertLnI&md5=9e3ad99b9a3796b0b5cdb36c30bdcd9aCAS |

Rengel Z, Graham RD (1996) Uptake of zinc from chelate-buffered nutrient solutions by wheat genotypes differing in zinc efficiency. Journal of Experimental Botany 47, 217–226.
Uptake of zinc from chelate-buffered nutrient solutions by wheat genotypes differing in zinc efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhs1CktL4%3D&md5=43c0b84ffb7abf9520b192f20eb8b940CAS |

Richards RA, Passioura JB (1981a) Seminal root morphology and water use of wheat. I. Environmental effects. Crop Science 21, 249–252.
Seminal root morphology and water use of wheat. I. Environmental effects.Crossref | GoogleScholarGoogle Scholar |

Richards RA, Passioura JB (1981b) Seminal root morphology and water use of wheat. II. Genetic variation. Crop Science 21, 253–255.
Seminal root morphology and water use of wheat. II. Genetic variation.Crossref | GoogleScholarGoogle Scholar |

Richards RA, Passioura JB (1989) A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments. Australian Journal of Agricultural Research 40, 943–950.
A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments.Crossref | GoogleScholarGoogle Scholar |

Sadok W, Sinclair TR (2009) Genetic variability of transpiration response to vapour pressure deficit among soybean (Glycine max (L.) Merr.) genotypes selected from a recombinant inbred line population. Field Crops Research 113, 156–160.
Genetic variability of transpiration response to vapour pressure deficit among soybean (Glycine max (L.) Merr.) genotypes selected from a recombinant inbred line population.Crossref | GoogleScholarGoogle Scholar |

Sadok W, Sinclair TR (2010) Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors under high evaporative demand. Journal of Experimental Botany 61, 821–829.
Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors under high evaporative demand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSrtbY%3D&md5=d19da63b337bbb76f8d8211c5b0bed9cCAS | 19969533PubMed |

Sadok W, Sinclair TR (2012) Zinc treatment results in transpiration rate decreases that vary among soybean genotypes. Journal of Plant Nutrition 35, 1866–1877.
Zinc treatment results in transpiration rate decreases that vary among soybean genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKnurnK&md5=847b5e5ef7a8226ee5162f59233c2ea6CAS |

Schoppach R, Sadok W (2012) Differential sensitivities of transpiration to evaporative demand and soil water deficit among wheat elite cultivars indicate different strategies for drought tolerance. Environmental and Experimental Botany 84, 1–10.
Differential sensitivities of transpiration to evaporative demand and soil water deficit among wheat elite cultivars indicate different strategies for drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Schoppach R, Sadok W (2013) Transpiration sensitivities to evaporative demand and leaf areas vary with night and day warming regimes among wheat genotypes. Functional Plant Biology 40, 708–718.
Transpiration sensitivities to evaporative demand and leaf areas vary with night and day warming regimes among wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrtrrJ&md5=280522419f80b80eb23760b8019abbbdCAS |

Sinclair TR, Hammer GL, van Oosterom EJ (2005) Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate. Functional Plant Biology 32, 945–952.
Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, Zwieniecki MA, Holbrook NM (2008) Low leaf hydraulic conductance associated with drought tolerance in soybean. Physiologia Plantarum 132, 446–451.
Low leaf hydraulic conductance associated with drought tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktb4%3D&md5=47d8b0752057897d1ff441203c1fa497CAS | 18333998PubMed |

Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: Just design the right drought scenario. Journal of Experimental Botany 63, 25–31.
Any trait or trait-related allele can confer drought tolerance: Just design the right drought scenario.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yms73L&md5=999726b96ab3bc2946e769bd2a9341e7CAS | 21963615PubMed |

Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327, 818–822.
Breeding technologies to increase crop production in a changing world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslWisLg%3D&md5=54d0265feef85eb6a2d45ed3ffdd3536CAS | 20150489PubMed |

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 |

Vadez V, Kholová J, Yadav RS, Hash CT (2013) Small temporal differences in water uptake among varieties of pearl millet (Pennisetum glaucum (L.) R.Br.) are critical for grain yield under terminal drought. Plant and Soil 371, 447–462.
Small temporal differences in water uptake among varieties of pearl millet (Pennisetum glaucum (L.) R.Br.) are critical for grain yield under terminal drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsFertbY%3D&md5=4577e14d06b1ba8b16728408da31a9a2CAS |

Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
A decimal code for the growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |

Zaman-Allah M, Jenkinson DM, Vadez V (2011) A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea. Journal of Experimental Botany 62, 4239–4252.
A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeit7jJ&md5=3e69da176cd45047bf294c59160fa392CAS | 21610017PubMed |

Zhang W-H, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiology 120, 849–858.
Inhibition of water channels by HgCl2 in intact wheat root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks1amtbc%3D&md5=fc3afd7e7effb020c53ccf23e39d0848CAS | 10398721PubMed |