Abstract
Hydraulic redistribution could contribute significantly to plant water balance under limiting conditions, reducing plant sensitivity to drought. We hypothesized that citrus species are able to redistribute water under drought, transporting water from a wet to a dry portion of root system. Using an unusual experimental design, ‘Rangpur’ lime and ‘Swingle’ citrumelo rootstocks were inarched into Valencia sweet orange trunk and subjected to water withholding. In a split root system, each plant was composed by two rootstocks, isolated from each other. During water deficit, only one rootstock faced low water availability while the other remained well watered. Sap flow, leaf water potential and soil moisture were monitored for 42 days. We found reserve sap flow in both rootstocks, with water being transported from the irrigated rootstock to the non-irrigated one. Nocturnal sap flow of well-watered rootstocks revealed that water redistribution continued at night, with ‘Rangpur’ lime showing higher hydraulic redistribution than ‘Swingle’ citrumelo. The ability of Citrus roots to redistribute water is genotype-dependent and may be an important physiological mechanism associated with drought tolerance in Citrus rootstocks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Basile B, Marsal J, Solari LI, Tyree MT, Bryla DR, Dejong TM (2003) Hydraulic conductance of peach trees grafted on rootstocks with differing size-controlling potentials. J Hortic Sci Biotechnol 78:768–774. https://doi.org/10.1080/14620316.2003.11511697
Bauerle TL, Richards JH, Smart DR, Eissenstat DM (2008) Importance of internal hydraulic redistribution for prolonging the lifespan of roots in dry soil. Plant, Cell Environ 31:177–186. https://doi.org/10.1111/j.1365-3040.2007.01749.x
Boscariol-Camargo R, Berger IJ, Souza AA, Amaral AM, Carlos EF, Freitas-Astúa J, Takita MA, Targon MLPN, Medina CL, Reis MS, Machado MA (2007) In silico analysis of ESTs from roots of Rangpur lime (Citrus limonia Osbeck) under water stress. Genet Mol Biol 30:906–916. https://doi.org/10.1590/S1415-47572007000500019
Brooks JR, Meinzer FC, Coulombe R, Gregg J (2002) Hydraulic redistribution of soil water during summer drought in two contrasting Pacific Northwest coniferous forests. Tree Physiol 22:1107–1117. https://doi.org/10.1093/treephys/22.15-16.1107
Burgess SSO, Dawson TE (2008) Using branch and basal trunk sap flow measurements to estimate whole-plant water capacitance: a caution. Plant Soil 305:5–13. https://doi.org/10.1007/s11104-007-9378-2
Burgess SSO, Downey A (2014) SFM1 sap flow meter manual. Version 4.0. ICT International Pty Ltd., Armidale
Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115:306–311. https://doi.org/10.1007/s004420050521
Burgess SSO, Adams MA, Turner NC, Beverly CR, Ong CK, Khan AAH, Bleby TM (2001) An improved heat pulse method to measure low and reverse rates of sap flow in woody plants. Tree Physiol 21:589–598. https://doi.org/10.1093/treephys/21.9.589
Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161. https://doi.org/10.1007/s004420050363
Chaves M, Davies B (2010) Drought effects and water use efficiency: improving crop production in dry environments. Funct Plant Biol 37:3–6. https://doi.org/10.1071/FPv37n2_FO
Cohen S, Naor A (2002) The effect of three rootstocks on water use, canopy conductance and hydraulic parameters of apple trees and predicting canopy from hydraulic conductance. Plant, Cell Environ 25:17–28. https://doi.org/10.1046/j.1365-3040.2002.00795.x
Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95:565–574. https://doi.org/10.1007/BF00317442
Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance and transpiration analyses: the roles of tree size and hydraulic lift. Tree Physiol 16:263–272. https://doi.org/10.1093/treephys/16.1-2.263
Dodd IC, Egea G, Watts CW, Whalley WR (2010) Root water potential integrates discrete soil physical properties to influence ABA signalling during partial rootzone drying. J Exp Bot 61:3543–3551. https://doi.org/10.1093/jxb/erq195
Domec JC, Warren JM, Meinzer FC, Brooks JR, Coulombe R (2004) Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution. Oecologia 141:7–16. https://doi.org/10.1007/s00442-004-1621-4
Erismann NM, Machado EC, Tucci MLS (2008) Photosynthetic limitation by CO2 diffusion in drought stressed orange leaves on three rootstocks. Photosynth Res 96:163–172. https://doi.org/10.1007/s11120-008-9297-y
Forster MA (2014) How significant is nocturnal sap flow? Tree Physiol 34:757–765. https://doi.org/10.1093/treephys/tpu051
Hsiao TC, Xu L (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. J Exp Bot 51:1595–1616. https://doi.org/10.1093/jexbot/51.350.1595
Marshall DC (1958) Measurement of sap flow in conifers by heat transport. Plant Physiol 33:385–396. https://doi.org/10.1104/pp.33.6.385
Martínez-Alcántara B, Rodriguez-Gamir J, Martínez-Cuenca MR, Iglesias DJ, Primo-Millo E, Forner-Giner MA (2013) Relationship between hydraulic conductance and citrus dwarfing by the Flying Dragon rootstock (Poncirus trifoliata L. Raft var. monstruosa). Trees Struct Funct 27:629–638. https://doi.org/10.1007/s00468-012-0817-1
Medina CL, Machado EC (1998) Trocas gasosas e relações hídricas em laranjeira “Valência” enxertada sobre limoeiro “Cravo” e Trifoliata e submetida à deficiência hídrica. Bragantia 57:15–22. https://doi.org/10.1590/S0006-87051998000100002
Medina CL, Machado EC, Pinto JM (1998) Fotossíntese de laranjeira ‘Valência’ enxertada sobre quatro porta-enxertos e submetida à deficiência hídrica. Bragantia 57:1–14. https://doi.org/10.1590/S0006-87051998000100001
Nardini A, Pitt F (1999) Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture. New Phytol 143:485–493. https://doi.org/10.1046/j.1469-8137.1999.00476.x
Nobel PS, Cuif M (1992) Shrinkage of attached roots of Opuntia ficus-indica in response to lowered water potentials—predicted consequences for water uptake or loss to soil. Ann Bot 70:485–491. https://doi.org/10.1093/oxfordjournals.aob.a088508
Oliveira RS, Dawson TE, Burgess SSO, Nepstad DC (2005) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363. https://doi.org/10.1007/s00442-005-0108-2
Pedroso FKJV, Prudente DA, Bueno ACR, Machado EC, Ribeiro RV (2014) Drought tolerance in citrus trees is enhanced by rootstock-dependent changes in root growth and carbohydrate availability. Environ Exp Bot 101:26–35. https://doi.org/10.1016/j.envexpbot.2013.12.024
Pompeu J Jr, Salva R, Blumer S (2004) Copas e porta-enxertos nos viveiros de mudas cítricas. Laranja 25:413–422. https://doi.org/10.1093/oxfordjournals.aob.a088508
Ribeiro RV, Machado EC (2007) Some aspects of citrus ecophysiology in subtropical climates: re-visiting photosynthesis under natural conditions. Braz J Plant Physiol 19:393–411. https://doi.org/10.1590/S1677-04202007000400009
Ribeiro RV, Machado EC, Santos MG, Oliveira RF (2009) Photosynthesis and water relations of well-watered orange plants as affected by winter and summer conditions. Photosynthetica 47:215–222. https://doi.org/10.1007/s11099-009-0035-2
Ribeiro RV, Espinoza-Nunez E, Pompeu J Jr, Mourão Filho FAA, Machado EC (2014) Citrus rootstocks for improving the horticultural performance and physiological responses under constraining environments. In: Ahmad P, Wani, Azooz MM (eds) Improvement of crops in the era of climatic changes, vol 1. Springer, New York, pp 1–36. https://doi.org/10.1007/978-1-4614-8830-9_1
Sakuratani T, Aoe T, Higuchi H (1999) Reverse flow in roots of Sesbania rostrata measured using the constant power heat balance method. Plant, Cell Environ 22:1153–1160. https://doi.org/10.1046/j.1365-3040.1999.00464.x
Schulze AE, Caldwell MM, Canadell J, Mooney HA, Jackson RB, Scholes R, Sala OE, Trimborn P (1998) Downward flux of water through roots (i.e. inverse hydraulic lift) in dry Kalahari sands. Oecologia 115:460–462. https://doi.org/10.1007/s004420050541
Smith DM, Jackson NA, Roberts JM, Ong CK (1999) Reverse flow of sap in tree roots and downward siphoning of water by Grevillea robusta. Funct Ecol 13:256–264. https://doi.org/10.1046/j.1365-2435.1999.00315.x
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 105:327–331. https://doi.org/10.1093/aob/mcp281
Williams DG, Cable W, Hultine K, Hoedjes JCB, Yepez EA, Simonneaux V, Er-Raki S, Boulet G, De Bruin HAR, Chehbouni A (2004) Evapotranspiration components determined by stable isotope, sap flow and eddy covariance techniques. Agric For Meteorol 125:241–258. https://doi.org/10.1016/j.agrformet.2004.04.008
Zeppel MJB, Lewis JD, Phillips NG, Tissue DT (2014) Consequences of nocturnal water loss: a synthesis of regulating factors and implications for capacitance, embolism and use in models. Tree Physiol 34:1047–1055. https://doi.org/10.1093/treephys/tpu089
Acknowledgements
The authors acknowledge the financial support provided by the National Council for Scientific and Technological Development (CNPq, Brazil; Grant No. 401104/2016-8) and the São Paulo Research Foundation (FAPESP, Brazil; Grant No. 2016/11906-9), as well as the FAPESP scholarships to MTM and SFS (Grants Nos. 2016/02199-7, 2015/14817-4). ECM and RVR also acknowledge the fellowships granted by CNPq, Brazil (Grants Nos. 303732/2015-6, 305221/2014-0). We are grateful to Dr. Luciano Pereira and Dr. Paulo R. L. Bittencourt for helping us with sap flow sensors and also to V.V. Sampaio for technical support in anatomical analyses. The authors are thankful to two anonymous reviewers for critical comments that improved significantly our paper.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Miranda, M.T., da Silva, S.F., Moura, B.B. et al. Hydraulic redistribution in Citrus rootstocks under drought. Theor. Exp. Plant Physiol. 30, 165–172 (2018). https://doi.org/10.1007/s40626-018-0111-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-018-0111-8