Maintaining the activity and function of the shallow root system of plants is essential for withstanding drought stress, but the associated mechanism is poorly understood. By investigating sap flow in 14 lateral roots (LRs) randomly selected from trees of a Chinese white poplar (Populus tomentosa) plantation receiving three levels of irrigation, an unknown root water transport mode of simultaneous daytime bi-directional water flow was discovered. This mode existed in five LRs confined to the surface soil without attached sinker roots. In the longer term, the bi-directional water flow was correlated with the soil water content. However, within the day, it was associated with transpiration. Our data demonstrated that bi-directional root sap flow occurred during the day, and was driven by evaporative demand, further suggesting the existence of circumferential water movement in the LR xylem. We named this phenomenon evaporation-driven hydraulic redistribution (EDHR). A soil-root water transport model was proposed to encapsulate this water movement mode. EDHR may be a crucial drought-tolerance mechanism that allows plants to maintain shallow root survival and activity by promoting root water recharge under extremely dry conditions.

Chinese Society of Forestry Beijing China

Institute of Forest Botany Dendrology and Geobiocenology Mendel University Zemedelska 3 Brno 61300 Czech Republic

Ministry of Education Key Laboratory of Silviculture and Conservation Beijing Forestry University Beijing China

Plant and Food Research Fitzherbert Science Centre Palmerston North New Zealand

School of Ecology and Environment Inner Mongolia University Hohhot China

Zobrazit více v PubMed

Allen RG, Pereira LS, Raes D, Smith M (1998) Crop evapotranspiration-guidelines for computing crop water requirements-FAO Irrigation and drainage paper 56. Fao, Rome, 300:  D05109

Allison VJ, Yermakov Z, Miller RM, Jastrow JD, Matamala R (2007) Using landscape and depth gradients to decouple the impact of correlated environmental variables on soil microbial community composition. Soil Biol Biochem  39:  505–516

Armas C, Kim JH, Bleby TM, Jackson RB (2012) The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species. Oecologia  168:  11–22 PubMed

Atkinson JA, Rasmussen A, Traini R, Voß U, Sturrock C, Mooney SJ, Wells DM, Bennett MJ (2014) Branching out in roots: uncovering form, function, and regulation. Plant Physiol  166:  538–550 PubMed PMC

Banda J, Bellande K, von Wangenheim D, Goh T, Guyomarc’h S, Laplaze L, Bennett MJ (2019) Lateral root formation in Arabidopsis: a well-ordered LRexit. Trends Plant Sci  24:  826–839 PubMed

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 PubMed

Bleby TM, Mcelrone AJ, Jackson RB (2010) Water uptake and hydraulic redistribution across large woody root systems to 20 m depth. Plant Cell Environ  33:  2132–2148 PubMed

Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia  115:  306–311 PubMed

Burgess SSO, Pate JS, Adams MA, Dawson TE (2000) Seasonal water acquisition and redistribution in the Australian woody phreatophyte, Banksia prionotes. Ann Bot  85:  215–224

Burgess SSO, Bleby TM (2006) Redistribution of soil water by lateral roots mediated by stem tissues. J Exp Bot  57:  3283–3291 PubMed

Burgess SSO, Downey A (2014) SFM1 Sap Flow Meter Manual. ICT International Pty Ltd., Armidale, NSW, Australia

Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia  79:  1–5 PubMed

Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia  113:  151–161 PubMed

Campbell GS, Norman JM (1998) An Introduction to Environmental Biophysics, Ed 2. Springer, New York

Cardon ZG, Stark JM, Herron PM, Rasmussen JA (2013) Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc Natl Acad Sci USA  110:  18988–18993 PubMed PMC

David TS, Pinto CA, Nadezhdina N, Kurz-Besson C, Henriques MO, Quilho T, Cermak J, Chaves MM, Pereira JS, David JS (2013) Root functioning, tree water use and hydraulic redistribution in Quercus suber trees: a modeling approach based on root sap flow. For Ecol Manag  307:  136–146

Di N, Liu Y, Mead DJ, Xie Y, Jia L, Xi B (2018) Root-system characteristics of plantation-grown Populus tomentosa adapted to seasonal fluctuation in the groundwater table. Trees  32:  137–149

Domec JC, King JS, Noormets A, Treasure E, Gavazzi MJ,, Sun G, McNulty SG (2010) Hydraulic redistribution of soil water by roots affects whole‐stand evapotranspiration and net ecosystem carbon exchange. New Phytol  187:  171–183 PubMed

Domec JC, Ogée J, Noormets A, Jouangy J, Gavazzi M, Treasure E, Sun G, McNulty SG, King JS (2012) Interactive effects of nocturnal transpiration and climate change on the root hydraulic redistribution and carbon and water budgets of southern United States pine plantations. Tree Physiol  32:  707–723 PubMed

Fang C, Moncrieff JB (2005) The variation of soil microbial respiration with depth in relation to soil carbon composition. Plant Soil  268:  243–253

Ferreira MI, Green S, Conceição N, Fernández JE (2018) Assessing hydraulic redistribution with the compensated average gradient heat-pulse method on rain-fed olive trees. Plant Soil  425:  21–41

Gaines KP, Stanley JW, Meinzer FC, McCulloh KA, Woodruff DR, Chen W, Adams TS, Lin H, Eissenstat DM (2016) Reliance on shallow soil water in a mixed-hardwood forest in central Pennsylvania. Tree Physiol  36:  444–458 PubMed PMC

Granier A ( 1987).  Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiol  3:  309–320 PubMed

Huang CW, Domec JC,, Ward EJ, Duman T, Manoli G, Parolari AJ, Katul GG (2017) The effect of plant water storage on water fluxes within the coupled soil–plant system. New Phytol  213:  1093–1106 PubMed

Jobbágy EG, Jackson RB (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry  53:  51–77

Jobbágy EG, Jackson RB (2004) The uplift of soil nutrients by plants: biogeochemical consequences across scales. Ecology  85:  2380–2389

Hultine KR, Williams DG, Burgess SSO, Keefer TO (2003) Contrasting patterns of hydraulic redistribution in three desert phreatophytes. Oecologia  135:  167–175 PubMed

Lee JE, Oliveira RS, Dawson TE, Fung I (2005) Root functioning modifies seasonal climate. Proc Natl Acad Sci USA  102:  17576–17581 PubMed PMC

Lee E, Kumar P, Barron-Gafford GA, Hendrys SM, Sanchez-Canete E, Minor RL, Colella T, Scott RL (2018) Impact of hydraulic redistribution on multispecies vegetation water use in a semiarid savanna ecosystem: an experimental and modeling synthesis. Water Resour Res  54:  4009–4027

Leffler AJ, Peek MS, Ryel RJ, Ivans CY, Caldwell MM (2005) Hydraulic redistribution through the root systems of senesced plants. Ecology  86:  633–642

Ludwig F, Dawson TE, Prins HHT, Berendse F, Kroon HD (2004) Below‐ground competition between trees and grasses may overwhelm the facilitative effects of hydraulic lift. Ecol Lett  7:  623–631

Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Develop  124:  33–44 PubMed

Marshall DC (1958) Measurements of sap flow in conifers by heat transport. Plant Physiol  33:  385–396 PubMed PMC

Nadezhdina N, David TS, David JS, Ferreira MI, Dohnal M, Tesar M, Gartner K, Leitgeb E, Nadezhdin V, Cermak J. , et al. (2010) Trees never rest: the multiple facets of hydraulic redistribution. Ecohydrology  3:  431–444

Nadezhdina N, Ferreira MI, Conceição N, Pacheco CA, Häusler M, David TS (2015) Water uptake and hydraulic redistribution under a seasonal climate: long‐term study in a rainfed olive orchard. Ecohydrology  8:  387–397

Nadezhdina N, Ferreira MI, Silva R, Pacheco CA (2008) Seasonal variation of water uptake of a Quercus suber tree in Central Portugal. Plant Soil  305:  105–119

Nadezhdina N, Steppe K, De Pauw DJ, Bequet R, Cermak J, Ceulemans R (2009) Stem‐mediated hydraulic redistribution in large roots on opposing sides of a Douglas‐fir tree following localized irrigation. New Phytol  184:  932–943 PubMed

Neumann RB, Cardon ZG (2012) The magnitude of hydraulic redistribution by plant roots: a review and synthesis of empirical and modeling studies. New Phytol  194:  337–352 PubMed

Passioura JB (1988) Water transport in and to roots. Ann Rev Plant Physiol Plant Mol Biol  39:  245–265

Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci  14:  399–408 PubMed

Prieto I, Ryel RJ (2014) Internal hydraulic redistribution prevents the loss of root conductivity during drought. Tree Physiol  34:  39–48 PubMed

Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia  73:  486–489 PubMed

Rodriguez‐Dominguez CM, Carins Murphy MR, Lucani C, Brodribb TJ (2018) Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytol  218:  1025–1035 PubMed

Scholz GF, Bucci SJ, Goldstein G, Moreira MZ, Meinzer FC, Domec JC, Villalobos-Vega R, Franco AC, Miralles-Wilhelm F (2008) Biophysical and life‐history determinants of hydraulic lift in Neotropical savanna trees. Funct Ecol  22:  773–786

Vilches-Barro A, Maizel A (2015) Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana.  Curr Opin Plant Biol  23:  31–38 PubMed

Waring RH, Whitehead D, Jarvis PG (1979) The contribution of stored water to transpiration in Scots pine. Plant Cell Environ  2:  309–317

Wang Q, Lintunen A, Zhao P, Shen W, Salmon Y, Chen X, Ouyang L, Zhu L, Ni G, Sun D,  et al. (2020) Assessing environmental control of sap flux of three tree species plantations in degraded hilly lands in South China. Forests  11:  206

Wang X, Tang C, Guppy CN, Sale PWG (2009) The role of hydraulic lift and subsoil P placement in P uptake of cotton (Gossypium hirsutum L.). Plant Soil  325:  263–275

Wu M, Zhang Y, Oya T, Marcati CR, Pereira L, Jansen S (2020). Root xylem in three woody angiosperm species is not more vulnerable to embolism than stem xylem. Plant Soil  450:  479–495

Yu T, Feng Q, Si J, Xi H, Li Z, Chen A (2013) Hydraulic redistribution of soil water by roots of two desert riparian phreatophytes in northwest China’s extremely arid region. Plant Soil  372:  297–308