Plant water uptake in drying soils

Plant Physiology

Volumn 164, Issue 4, 2014, Pages 1619-1627

  Lobet, Guillaume ^a   Couvreur, Valentin ^b,c   Meunier, Félicien ^c   Javaux, Mathieu ^c,d   Draye, Xavier ^c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SOIL; WATER;

BIOLOGICAL MODEL; DESICCATION; METABOLISM; PLANT; PLANT ROOT; SOIL;

DESICCATION; MODELS, BIOLOGICAL; PLANT ROOTS; PLANTS; SOIL; WATER;

EID: 84898665124     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.233486     Document Type: Article

References (116)

1. Alsina MM, Smart DR, Bauerle T, de Herralde F, Biel C, Stockert C, Negron C, Save R (2011) Seasonal changes of whole root system conductance by a drought-tolerant grape root system. J Exp Bot 62: 99-109.
2. Armengaud P, Zambaux K, Hills A, Sulpice R, Pattison RJ, Blatt MR, Amtmann A (2009) EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J 57: 945-956.
3. Beff L, Günther T, Vandoorne B, Couvreur V, Javaux M (2013) Threedimensional monitoring of soil water content in a maize field using electrical resistivity tomography. Hydrol Earth Syst Sci 17: 595-609.
4. Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62: 59-68.
5. 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.
6. Bramley H, Turner DW, Tyerman SD, Turner NC (2007) Water flow in the roots of crop species: the influence of root structure, aquaporin activity, and waterlogging. Adv Agron 96: 133-196.
7. 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.
8. 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. Funct Plant Biol 37: 183-193.
9. Burton AL, Brown KM, Lynch JP (2013) Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Sci 53: 1042-1055.
10. Burton AL, Williams M, Lynch JP, Brown KM (2012) RootScan: software for high-throughput analysis of root anatomical traits. Plant Soil 357: 189-203.
11. Carminati A, Schneider CL, Moradi AB, Zarebanadkouki M, Vetterlein D, Vogel J, Hildebrandt A, Weller U, Schueler L, Oswald SE (2011) How the rhizosphere may favor water availability to roots. Vadose Zone J 10: 988-998.
12. Carminati A, Vetterlein D (2013) Plasticity of rhizosphere hydraulic properties as a key for efficient utilization of scarce resources. Ann Bot (Lond) 112: 277-290.
13. Cassiani G, Bruno V, Villa A, Fusi N (2006) A saline trace test monitored via time-lapse surface electrical resistivity tomography. J Appl Geophys 59: 244-259.
14. Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164: 1600-1618.
15. Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol 193: 713-720.
16. Clark RT, Famoso AN, Zhao K, Shaff JE, Craft EJ, Bustamante CD, McCouch SR, Aneshansley DJ, Kochian LV (2013) High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development. Plant Cell Environ 36: 454-466.
17. Clark RT, MacCurdy RB, Jung JK, Shaff JE, McCouch SR, Aneshansley DJ, Kochian LV (2011) Three-dimensional root phenotyping with a novel imaging and software platform. Plant Physiol 156: 455-465.
18. Cochard H, Barigah ST, Kleinhentz M, Eshel A (2008) Is xylem cavitation resistance a relevant criterion for screening drought resistance among Prunus species? J Plant Physiol 165: 976-982.
19. Cochard H, Casella E, Mencuccini M (2007a) Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiol 27: 1761-1767.
20. Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007b) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143: 122-133.
21. Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4: 442.
22. Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Gozé E, Kilian A, et al (2013) Genome-wide association mapping of root traits in a japonica rice panel. PLoS ONE 8: e78037.
23. Couvreur V (2013) Horizontal soil water potential heterogeneity: simplifying approaches for crop water dynamics models. In Emergent Properties of Plant Hydraulic Architecture a Modelling Study. Université Catholique de Louvain, Louvain-la-Neuve, Belgium, pp 57-102.
24. Couvreur V, Vandenborg J, Javaux M (2012) A simple three-dimensional macroscopic root water uptake. Hydrol Earth Syst Sci 16: 2957-2971.
25. Dai X, Wang Y, Yang A, Zhang WH (2012) OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphatestarvation responses and root architecture in rice. Plant Physiol 159: 169-183.
26. Delzon S, Douthe C, Sala A, Cochard H (2010) Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant Cell Environ 33: 2101-2111.
27. Domec JC, Lachenbruch B, Meinzer FC (2006) Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93: 1588-1600.
28. Doussan C, Pagès L, Vercambre G (1998) Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption-model description. Ann Bot (Lond) 81: 213-223.
29. Doussan C, Pierret A, Garrigues E, Pagès L (2006) Water uptake by plant roots: II-Modelling of water transfer in the soil root-system with explicit account of flow within the root system-Comparison with experiments. Plant Soil 283: 99-117.
30. Draye X, Kim Y, Lobet G, Javaux M (2010) Model-assisted integration of physiological and environmental constraints affecting the dynamic and spatial patterns of root water uptake from soils. J Exp Bot 61: 2145-2155.
31. Dunbabin VM, Postma JA, Schnepf A, Pagès L, Javaux M, Wu L, Leitner D, Chen YL, Rengel Z, Diggle AJ (2013) Modelling root-soil interactions using three-dimensional models of root growth, architecture and function. Plant Soil 372: 93-124.
32. Enstone DE, Peterson CA (2005) Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions. Plant Cell Environ 28: 444-455.
33. 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.
34. Esser HG, Carminati A, Vontobel P, Lehmann EH, Oswald SE (2010) Neutron radiography and tomography of water distribution in the root zone. J Plant Nutr Soil Sci 173: 757-764.
35. Fan M, Bai R, Zhao X, Zhang J (2007) Aerenchyma formed under phosphorus deficiency contributes to the reduced root hydraulic conductivity in maize roots. J Integr Plant Biol 49: 598-604.
36. Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr Biol 23: 2044-2050.
37. Garrigues E, Doussan C, Pierret A (2006) Water uptake by plant roots: I-Formation and propagation of a water extraction front in mature root systems as evidenced by 2D light transmission imaging. Plant Soil 283: 83-98.
38. Gebauer R, Volařík D (2012) Root hydraulic conductivity and vessel structure modification with increasing soil depth of two oak species: Quercus pubescens and Quercus robur. Trees (Berl) 27: 523-531.
39. Giehl RFH, Gruber BD, von Wirén N (2013) It's time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65: 769-778.
40. Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163: 161-179.
41. 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.
42. 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.
43. Hammer G, Dong Z, Mclean G, Doherty A, Messina C, Schussler J, Zinselmeier C, Paszkiewicz S, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the U. S. corn belt? Crop Sci 49: 299-312.
44. Hammer GL, van Oosterom E, McLean G, Chapman SC, Broad I, Harland P, Muchow RC (2010) Adapting APSIM to model the physiology and genetics of complex adaptive traits in field crops. J Exp Bot 61: 2185-2202.
45. Herbette S, Cochard H (2010) Calcium is a major determinant of xylem vulnerability to cavitation. Plant Physiol 153: 1932-1939.
46. Hill K, Porco S, Lobet G, Zappala S, Mooney S, Draye X, Bennett MJ (2013) Root systems biology: bridging regulatory networks to rhizospherescale processes. Plant Physiol 163: 1487-1503.
47. Hund A, Trachsel S, Stamp P (2009) Growth of axile and lateral roots of maize: I. Development of a phenotying platform. Plant Soil 325: 335-349.
48. Iwata S, Miyazawa Y, Fujii N, Takahashi H (2013) MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions. Ann Bot (Lond) 112: 103-114.
49. Iyer-Pascuzzi AS, Symonova O, Mileyko Y, Hao Y, Belcher H, Harer J, Weitz JS, Benfey PN (2010) Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems. Plant Physiol 152: 1148-1157.
50. Jahnke S, Menzel MI, van Dusschoten D, Roeb GW, Bühler J, Minwuyelet S, Blümler P, Temperton VM, Hombach T, Streun M, et al (2009) Combined MRI-PET dissects dynamic changes in plant structures and functions. Plant J 59: 634-644.
51. Jarvis PG (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond B Biol Sci 273: 593-610.
52. Javaux M, Couvreur V, Vanderborght J (2013) Root water uptake: from three-dimensional biophysical processes to macroscopic modeling approaches. Vadose Zone J 12: 1-16.
53. Javaux M, Schroeder T, Vanderborght J, Vereecken H (2008) Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J 7: 1079-1088.
54. Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güçlü J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, et al (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15: 509-522.
55. Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012) Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance. Plant Cell Environ 35: 760-769.
56. Kellermeier F, Chardon F, Amtmann A (2013) Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation. Plant Physiol 161: 1421-1432.
57. Knipfer T, Besse M, Verdeil JL, Fricke W (2011) Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J Exp Bot 62: 4115-4126.
58. Lambot S, Binley A, Slob E, Hubbard S (2008) Ground penetrating radar in hydrogeophysics. Vadose Zone J 7: 137-139.
59. Lamy JB, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C (2014) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol 201: 874-88.
60. Landi P, Giuliani S, Salvi S, Ferri M, Tuberosa R, Sanguineti MC (2010) Characterization of root-yield-1. 06, a major constitutive QTL for root and agronomic traits in maize across water regimes. J Exp Bot 61: 3553-3562.
61. Leitner D, Felderer B, Vontobel P, Schnepf A (2014) Recovering root system traits using image analysis exemplified by two-dimensional neutron radiography images of lupine. Plant Physiol 164: 24-35.
62. Lenochova Z, Soukup A, Votrubova O (2009) Aerenchyma formation in maize roots. Biol Plant 53: 263-270.
63. Li X, Wang X, Yang Y, Li R, He Q, Fang X, Luu DT, Maurel C, Lin J (2011) Single-molecule analysis of PIP2; 1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23: 3780-3797.
64. Li Y, Sperry JS, Shao M (2009) Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance. Environ Exp Bot 66: 341-346.
65. Lobet G, Draye X (2013) Novel scanning procedure enabling the vectorization of entire rhizotron-grown root systems. Plant Methods 9: 1.
66. Lobet G, Draye X, Périlleux C (2013) An online database for plant image analysis software tools. Plant Methods 9: 38.
67. Lobet G, Pagès L, Draye X (2011) A novel image-analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiol 157: 29-39.
68. Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot (Lond) 112: 347-357.
69. Mairhofer S, Zappala S, Tracy S, Sturrock C, Bennett MJ, Mooney SJ, Pridmore TP (2013) Recovering complete plant root system architectures from soil via X-ray μ-computed tomography. Plant Methods 9: 8.
70. Manschadi AM, Christopher JT, Hammer GL, deVoil P (2010) Experimental and modelling studies of drought-adaptive root architectural traits in wheat (Triticum aestivum L.). Plant Biosys 144: 458-462.
71. Maurel C, Chrispeels MJ (2001) Aquaporins: a molecular entry into plant water relations. Plant Physiol 125: 135-138.
72. McCulloh K, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytol 186: 439-450.
73. McMichael BL, Lascano RJ (2010) Evaluation of hydraulic lift in cotton (Gossypium hirsutum L.) germplasm. Environ Exp Bot 68: 26-30.
74. Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvationinduced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155: 1000-1012.
75. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, et al (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102: 7760-7765.
76. Mooney SJ, Pridmore TP, Helliwell J, BennettMJ (2012) Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant Soil 352: 1-22.
77. Moradi AB, Carminati A, Lamparter A, Woche SK, Bachmann J, Vetterlein D, Vogel HJ, Oswald SE (2012) Is the rhizosphere temporarily water repellent? Vadose Zone J https://www. soils. org/publications/vzj/abstracts/11/3/vzj2011. 0120.
78. Moriwaki T, Moriwaki T, Miyazawa Y, Miyazawa Y, Fujii N, Fujii N, Takahashi H, Takahashi H (2014) Plant science. Plant Sci 215-216: 141-149.
79. Pagès L, Serra V, Draye X, Doussan C, Pierret A (2010) Estimating root elongation rates from morphological measurements of the root tip. Plant Soil 328: 35-44.
80. Passioura JB (1984) Roots and water economy of wheat. In W. Day, R. K. Atkin, eds, Wheat Growth and Modelling, NATO ASI Series A Life Science, Plenum, New York 86: 185-198.
81. Passioura JB (2012) Phenotyping for drought tolerance in grain crops: when is it useful to breeders? Funct Plant Biol 39: 851.
82. Pinheiro HA, Damatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Ann Bot (Lond) 96: 101-108.
83. Pound MP, French AP, Atkinson JA, Wells DM, BennettMJ, Pridmore T (2013) RootNav: navigating images of complex root architectures. Plant Physiol 162: 1802-1814.
84. Purushothaman R, Zaman-Allah M, Mallikarjuna N, Pannirselvam R, Krishnamurthy L, Gowda CLL (2013) Root anatomical traits and their possible contribution to drought tolerance in grain legumes. Plant Prod Sci 16: 1-8.
85. Rewald B, Ephrath JE, Rachmilevitch S (2011) A root is a root is a root? Water uptake rates of Citrus root orders. Plant Cell Environ 34: 33-42.
86. Robinson DA, Jones SB, Wraith JM, Or D, Friedman SP (2003) A review of advances in dielectric and electrical conductivity measurement in soils using time domain reflectometry. Vadose Zone J 2: 444-475.
87. Schoppach RM, Wauthelet D, Jeanguenin L, SadokW(2013) Conservative water use under high evaporative demand associated with smaller root metaxylem and limited trans-membrane water transport in wheat. Funct Plant Biol 41: 257-269.
88. Schroeder N, Javaux M, Vanderborght J, Steffen B, Vereecken H (2012) Effect of root water and solute uptake on apparent soil dispersivity: a simulation study. Vadoze Zone J 11: 1-14.
89. Schroeder N, Lazarovitch N, Vanderborght J, Vereecken H, Javaux M (2013) Linking transpiration reduction to rhizosphere salinity using a 3D coupled soil-plant model. Plant Soil http://dx. doi. org/10. 1007/s11104-013-1990-8.
90. Schroeder T, Tang L, Javaux M, Vanderborght J, Koerfgen B, Vereecken H (2009) A grid refinement approach for a three-dimensional soil-root water transfer model. Water Resour Res 45: W10412.
91. Shroeder T, Javaux M, Vanderborght J, Koerfgen B, Vereecken H (2008) Effect of local soil hydraulic conductivity drop using a three-dimensional root water uptake model. Vadose Zone J 7: 1089-1098.
92. Šimǔnek J, Hopmans JW (2009) Modeling compensated root water and nutrient uptake. Ecol Modell 220: 505-521.
93. Steele KA, Price AH, Witcombe JR, Shrestha R, Singh BN, Gibbons JM, Virk DS (2013) QTLs associated with root traits increase yield in upland rice when transferred through marker-assisted selection. Theor Appl Genet 126: 101-108.
94. Steudle E (2000) Water uptake by plant roots: an integration of views. Plant Soil 226: 45-56.
95. Steudle E (2001) The cohesion-tension mechanism and the acquisition of water by plant roots. Annu Rev Plant Physiol Plant Mol Biol 52: 847-875.
96. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49: 775-788.
97. Sutka M, Li G, Boudet J, Boursiac Y, Doumas P, Maurel C (2011) Natural variation of root hydraulics in Arabidopsis grown in normal and saltstressed conditions. Plant Physiol 155: 1264-1276.
98. Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J Exp Bot 63: 25-31.
99. Tombesi S, Johnson RS, Day KR, DeJong TM (2010) Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size-controlling capacity of peach rootstocks. Ann Bot (Lond) 105: 327-331.
100. Uga Y, Okuno K, Yano M(2008) QTLs underlying natural variation in stele and xylem structures of rice root. Breed Sci 58: 7-14.
101. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, et al (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45: 1097-1102.
102. Vadez V, Rao JS, Bhatnagar-Mathur P, Sharma KK (2013) DREB1A promotes root development in deep soil layers and increases water extraction under water stress in groundnut. Plant Biol (Stuttg) 15: 45-52.
103. Vadez V, Soltani A, Sinclair TR (2012) Modelling possible benefits of root related traits to enhance terminal drought adaptation of chickpea. Field Crops Res 137: 108-115.
104. 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.
105. Vanderborght J, Kemna A, Hardelauf H (2005) Potential of electrical resistivity tomography to infer aquifer transport characteristics from tracer studies: a synthetic case study. Water Resour Res 41: 1-23.
106. Vercambre G, Doussan C, Pagès L, Habib R, Pierret A (2002) Influence of xylem development on axial hydraulic conductance within Prunus root systems. Trees (Berl) 16: 479-487.
107. Walker JP, Willgoose GR, Kalma JD (2004) In situ measurement of soil moisture: a comparison of techniques. J Hydrol (Amst) 293: 85-99.
108. Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SVS, Rebetzke GJ, Kirkegaard JA, Christopher JT, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63: 3485-3498.
109. Watt M, Magee LJ, McCully ME (2008) Types, structure and potential for axial water flow in the deepest roots of field-grown cereals. New Phytol 178: 135-146.
110. Yang X, Li Y, Ren B, Ding L, Gao C, Shen Q, Guo S (2012) Droughtinduced root aerenchyma formation restricts water uptake in rice seedlings supplied with nitrate. Plant Cell Physiol 53: 495-504.
111. Zaman-Allah M, Jenkinson DM, Vadez V (2011a) A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea. J Exp Bot 62: 4239-4252.
112. Zaman-Allah M, Jenkinson DM, Vadez V (2011b) Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use. Funct Plant Biol 38: 270-281.
113. Zarebanadkouki M, Kim YX, Carminati A (2013) Where do roots take up water? Neutron radiography of water flow into the roots of transpiring plants growing in soil. New Phytol 199: 1034-1044.
114. Zhu J, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ 33: 740-749.
115. Zufferey V, Cochard H, Améglio T, Spring JL, Viret O (2011) Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas). J Exp Bot 62: 3885-3894.
116. Zwieniecki MA, Holbrook NM (2009) Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends Plant Sci 14: 530-534.