Because of intense transpiration and growth, the needs of plants for water can be immense. Yet water in the soil is most often heterogeneous if not scarce due to more and more frequent and intense drought episodes. The converse context, flooding, is often associated with marked oxygen deficiency and can also challenge the plant water status. Under our feet, roots achieve an incredible challenge to meet the water demand of the plant’s aerial parts under such dramatically different environmental conditions. For this, they continuously explore the soil, building a highly complex, branched architecture. On shorter time scales, roots keep adjusting their water transport capacity (their so-called hydraulics) locally or globally. While the mechanisms that directly underlie root growth and development as well as tissue hydraulics are being uncovered, the signalling mechanisms that govern their local and systemic adjustments as a function of water availability remain largely unknown. A comprehensive understanding of root architecture and hydraulics as a whole (in other terms, root hydraulic architecture) is needed to apprehend the strategies used by plants to optimize water uptake and possibly improve crops regarding this crucial trait.
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Voesenek, L. A. & Bailey-Serres, J. Flood adaptive traits and processes: an overview. New Phytol. 206, 57–73 (2015).
Tan, X. et al. Plant water transport and aquaporins in oxygen-deprived environments. J. Plant Physiol. 227, 20–30 (2018).
Daryanto, S., Wang, L. & Jacinthe, P. A. Global synthesis of drought effects on maize and wheat production. PLoS ONE 11, e0156362 (2016).
Hirabayashi, Y. et al. Global flood risk under climate change. Nat. Clim. Change 3, 816–821 (2013).
Manik, S. M. N. et al. Soil and crop management practices to minimize the impact of waterlogging on crop productivity. Front. Plant Sci. 10, 140 (2019).
Du, T., Kang, S., Zhang, J. & Davies, W. J. Deficit irrigation and sustainable water-resource strategies in agriculture for China’s food security. J. Exp. Bot. 66, 2253–2269 (2015).
Kirkegaard, J. A. et al. Improving water productivity in the Australian Grains industry—a nationally coordinated approach. Crop Pasture Sci. 65, 583–601 (2014).
Davies, W. J. & Bennett, M. J. Achieving more crop per drop. Nat. Plants 1, 15118 (2015).
Tester, M. & Langridge, P. Breeding technologies to increase crop production in a changing world. Science 327, 818–822 (2010).
Millet, E. J. et al. Genome-wide analysis of yield in Europe: allelic effects vary with drought and heat scenarios. Plant Physiol. 172, 749–764 (2016).
Atkinson, J. A., Pound, M. P., Bennett, M. J. & Wells, D. M. Uncovering the hidden half of plants using new advances in root phenotyping. Curr. Opin. Biotechnol. 55, 1–8 (2019).
Jung, J. K. & McCouch, S. Getting to the roots of it: genetic and hormonal control of root architecture. Front. Plant Sci. 4, 186 (2013).
Lavenus, J. et al. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18, 450–458 (2013).
Petricka, J. J., Winter, C. M. & Benfey, P. N. Control of Arabidopsis root development. Annu. Rev. Plant Biol. 63, 563–590 (2012).
Lynch, J. P. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot. 112, 347–357 (2013).
Ogura, T. et al. Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178, 400–412 (2019).
Shahzad, Z. & Amtmann, A. Food for thought: how nutrients regulate root system architecture. Curr. Opin. Plant. Biol. 39, 80–87 (2017).
Tuberosa, R. et al. Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol. Biol. 48, 697–712 (2002).
Ruta, N., Liedgens, M., Fracheboud, Y., Stamp, P. & Hund, A. QTLs for the elongation of axile and lateral roots of maize in response to low water potential. Theor. Appl. Genet. 120, 621–631 (2010).
Gao, Y. & Lynch, J. P. Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). J. Exp. Bot. 67, 4545–4557 (2016).
Sebastian, J. et al. Grasses suppress shoot-borne roots to conserve water during drought. Proc. Natl Acad. Sci. USA 113, 8861–8866 (2016).
Uga, Y. et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 45, 1097–1102 (2013).
Jiang, N. et al. Three-dimensional time-lapse analysis reveals multiscale relationships in maize root systems with contrasting architectures. Plant Cell 31, 1708–1722 (2019).
Band, L. R. et al. Multiscale systems analysis of root growth and development: modeling beyond the network and cellular scales. Plant Cell 24, 3892–3906 (2012).
Rellan-Alvarez, R., Lobet, G. & Dinneny, J. R. Environmental control of root system biology. Annu. Rev. Plant Biol. 67, 619–642 (2016).
Maurel, C. et al. Aquaporins in plants. Physiol. Rev. 95, 1321–1358 (2015).
Bramley, H., Turner, N. C., Turner, D. W. & Tyerman, S. D. Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol. 150, 348–364 (2009).
Hachez, C., Moshelion, M., Zelazny, E., Cavez, D. & Chaumont, F. 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 (2006).
Barberon, M. et al. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447–459 (2016).
Wang, P. et al. Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants. Sci. Rep. 9, 4227 (2019).
Shahzad, Z. et al. A potassium-dependent oxygen sensing pathway regulates plant root hydraulics. Cell 167, 87–98 (2016).
Tang, N. et al. Natural variation at XND1 impacts root hydraulics and trade-off for stress responses in Arabidopsis. Nat Commun. 9, 3884 (2018).
Doussan, C., Vercambre, G. & Pages, L. Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption — distribution of axial and radial conductances in maize. Ann. Bot. 81, 225–232 (1998).
Doussan, C., Pages, L. & Vercambre, G. Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption — model description. Ann. Bot. 81, 213–223 (1998).
Lobet, G., Pages, L. & Draye, X. A modeling approach to determine the importance of dynamic regulation of plant hydraulic conductivities on the water uptake dynamics in the soil-plant-atmosphere system. Ecol. Model. 290, 65–75 (2014).
Couvreur, V. et al. Going with the flow: multiscale insights into the composite nature of water transport in roots. Plant Physiol. 178, 1689–1703 (2018).
Meunier, F., Couvreur, V., Draye, X., Vanderborght, J. & Javaux, M. Towards quantitative root hydraulic phenotyping: novel mathematical functions to calculate plant-scale hydraulic parameters from root system functional and structural traits. J. Math. Biol. 75, 1133–1170 (2017).
Zarebanadkouki, M., Kroener, E., Kaestner, A. & Carminati, A. Visualization of root water uptake: quantification of deuterated water transport in roots using neutron radiography and numerical modeling. Plant Physiol. 166, 487–499 (2014).
Pierret, A., Doussan, C. & Pages, L. Spatio-temporal variations in axial conductance of primary and first order lateral roots of a maize crop as predicted by a model of the hydraulic architecture of root systems. Plant Soil 282, 117–126 (2006).
Draye, X., Kim, Y., Lobet, G. & Javaux, M. Model-assisted integration of physiological and environmental constraints affecting the dynamic and spatial patterns of root water uptake from soils. J. Exp. Bot. 8, 2145–2155 (2010).
Matsuo, N., Ozawa, K. & Mochizuki, T. Genotypic differences in root hydraulic conductance of rice (Oryza sativa L.) in response to water regimes. Plant Soil 316, 25–34 (2009).
Marguerit, E., Brendel, O., Lebon, E., Van Leeuwen, C. & Ollat, N. Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytol. 194, 416–429 (2012).
Péret, B. et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991–998 (2012).
Deak, K. I. & Malamy, J. Osmotic regulation of root system architecture. Plant J. 43, 17–28 (2005).
Dinneny, J. R. Developmental responses to water and salinity in root systems. Annu. Rev. Cell Dev. Biol. 35, 239–257 (2019).
Rosales, M. A., Maurel, C. & Nacry, P. Abscisic acid coordinates dose-dependent developmental and hydraulic responses of roots to water deficit. Plant Physiol. 180, 2198–2211 (2019).
Vandeleur, R., Niemietz, C., Tilbrook, J. & Tyerman, S. D. Role of aquaporins in root responses to irrigation. Plant Soil 274, 141–161 (2005).
Hachez, C. et al. Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. Plant Cell Environ. 35, 185–198 (2012).
Caldeira, C. F., Jeanguenin, L., Chaumont, F. & Tardieu, F. Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance. Nat. Commun. 5, 5365 (2014).
Ramachandran, P., Wang, G., Augstein, F., de Vries, J. & Carlsbecker, A. Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165. Development 145, dev159202 (2018).
Rowe, J. H., Topping, J. F., Liu, J. & Lindsey, K. Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol. 211, 225–239 (2016).
Li, X., Chen, L., Forde, B. G. & Davies, W. J. The biphasic root growth response to abscisic acid in Arabidopsis involves interaction with ethylene and auxin signalling pathways. Front. Plant Sci. 8, 1493 (2017).
Moriwaki, T., Miyazawa, Y., Kobayashi, A. & Takahashi, H. Molecular mechanisms of hydrotropism in seedling roots of Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 100, 25–34 (2013).
Bao, Y. et al. Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc. Natl Acad. Sci. USA 111, 9319–9324 (2014).
von Wangenheim, D. et al. Early developmental plasticity of lateral roots in response to asymmetric water availability. Nat. Plants 6, 73–77 (2020).
Orman-Ligeza, B. et al. The xerobranching response represses lateral root formation when roots are not in contact with water. Curr. Biol. 28, 3165–3173 (2018).
Tournaire-Roux, C. et al. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393–397 (2003).
Sauter, M. Root responses to flooding. Curr. Opin. Plant Biol. 16, 282–286 (2013).
Yamauchi, T. et al. Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling. Proc. Natl Acad. Sci. USA 116, 20770–20775 (2019).
Eysholdt-Derzso, E. & Sauter, M. Root bending is antagonistically affected by hypoxia and ERF-mediated transcription via auxin signaling. Plant Physiol. 175, 412–423 (2017).
Waidmann, S. et al. Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nat. Commun. 10, 3540 (2019).
Shabala, S., Shabala, L., Barcelo, J. & Poschenrieder, C. Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ. 37, 2216–2233 (2014).
Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).
Hamilton, E. S. et al. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350, 438–441 (2015).
Martiniere, A. et al. Osmotic stress activates two reactive oxygen species pathways with distinct effects on protein nanodomains and diffusion. Plant Physiol. 179, 1581–1593 (2019).
Shkolnik, D., Nuriel, R., Bonza, M. C., Costa, A. & Fromm, H. MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted Ca2+ signal essential for root water tracking in Arabidopsis. Proc. Natl Acad. Sci. USA 115, 8031–8036 (2018).
Puertolas, J., Conesa, M. R., Ballester, C. & Dodd, I. C. Local root abscisic acid (ABA) accumulation depends on the spatial distribution of soil moisture in potato: implications for ABA signalling under heterogeneous soil drying. J. Exp. Bot. 66, 2325–2334 (2015).
McLean, E. H., Ludwig, M. & Grierson, P. F. Root hydraulic conductance and aquaporin abundance respond rapidly to partial root-zone drying events in a riparian Melaleuca species. New Phytol. 192, 664–675 (2011).
Takahashi, F. et al. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556, 235–238 (2018).
Robbins, N. E. II & Dinneny, J. R. Growth is required for perception of water availability to pattern root branches in plants. Proc. Natl Acad. Sci. USA 115, E822–E831 (2018).
Dietrich, D. et al. Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat. Plants 3, 17057 (2017).
Orosa-Puente, B. et al. Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362, 1407–1410 (2018).
Holdsworth, M. J., Vicente, J., Sharma, G., Abbas, M. & Zubrycka, A. The plant N-degron pathways of ubiquitin-mediated proteolysis. J. Integr. Plant Biol. 62, 70–89 (2019).
Hartman, S. et al. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat. Commun. 10, 4020 (2019).
Eysholdt-Derzso, E. & Sauter, M. Hypoxia and the group VII ethylene response transcription factor HRE2 promote adventitious root elongation in Arabidopsis. Plant Biol. 21 (Suppl. 1), 103–108 (2019).
Shukla, V. et al. Endogenous hypoxia in lateral root primordia controls root architecture by antagonizing auxin signaling in Arabidopsis. Mol. Plant 12, 538–551 (2019).
Char, S. N. et al. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol. J. 15, 257–268 (2017).
Wang, X. et al. Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat. Genet. 48, 1233–1241 (2016).
Mao, H. et al. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat. Commun. 6, 8326 (2015).
This work was supported in part by the Agence Nationale de la Recherche (ANR-11-BSV6-018) and the European Research Council (ERC-2017-ADG-788553).
The authors declare no competing interests.
Peer review information Nature Plants thanks Malcolm Bennett and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Maurel, C., Nacry, P. Root architecture and hydraulics converge for acclimation to changing water availability. Nat. Plants 6, 744–749 (2020). https://doi.org/10.1038/s41477-020-0684-5
Tuning drought resistance by using a root-specific expression transcription factor PdNF-YB21 in Arabidopsis thaliana
Plant Cell, Tissue and Organ Culture (PCTOC) (2021)
Aquaporins, and not changes in root structure, provide new insights into physiological responses to drought, flooding, and salinity
Journal of Experimental Botany (2021)
Chloride nutrition improves drought resistance by enhancing water deficit avoidance and tolerance mechanisms
Journal of Experimental Botany (2021)
The Arabidopsis TETRATRICOPEPTIDE THIOREDOXIN-LIKE 1 Gene Is Involved in Anisotropic Root Growth during Osmotic Stress Adaptation