Structural Biology of Salt and Drought Tolerance in Plants


Climate disruption is an increasing pressure on food supply worldwide. Consequently, it is required to develop strategies to improve the yield of crops under abiotic stress as plants have to endure novel adverse environmental conditions. Among them, drought and salinity constrain agricultural productivity most dramatically. Many of the plant adaptive responses occur at the cell membrane. There, the communication between those processes that are disrupted as a consequence of the adverse environmental stimuli and those involved in the plant adaptive response is established. The available data show that this communication is achieved by a regulated localisation of different signalling molecules to the vicinity of ion channels and transporters. The structural characterisation of those complexes constitutes a major challenge to understand the mechanism to confer plant resistance to stress and to implement novel biotechnological approaches to ensure food security.

Key Concepts

  • The understanding at the molecular level of the mechanisms for plant adaptation to drought and salinity helps to implement novel biotechnological approaches to ensure food security.
  • The cytosolic levels of the phytohormone abscisic acid (ABA) and the Ca2+ ion (Ca2+) act as a molecular switch to plant adaptive response to stress.
  • Plant cell response to abiotic stress is mediated by supramolecular complexes that are formed in the vicinity or at the cell membrane.
  • Structural biology has provided the bases for ABA and Ca2+ roles as they affect the molecular architecture of the signalling complexes regulating plant response.
  • The structural information can be used to drive a genetic approach and for the identification of small molecules that can be used as new agrochemicals for plant improvement.

Keywords: protein structure; plant biology; abiotic stress; signal transduction; abscisic acid; agriculture

Figure 1. Plant response to drought and salt stresses. Root cells incorporate Na+ from the soil to the cytosol through low‐affinity channels. Cell response includes extruding Na+ ions from the cell to the vascular system; there they are transported by diffusion to the leaves where it is compartmentalised into the vacuoles. If the water availability is scarce, plant prevents water transpiration by the closure of the stomata. These processes involve the Ca2+‐ and ABA‐mediated regulation of ion channels and transporters to prevent misadjustments of intracellular ion homeostasis.
Figure 2. Structural biology of the ABA‐mediated responses to drought. (a) Schematic representation of the proteins involved in the pathway. (b) Structural basis of ABA signalling. Cartoon representation of the structures of the SlPYL1 ABA receptor (PYR/PYL), the ABA‐mediated complex between HAB1 and CsPYL1 (PP2C–ABA–PYR/PYL), the SnRK2.6/OST1 (active SnRK2) and the HAB1–SnRK2.6/OST1 complex (PP2C–SnRK2). The inset represents details of the ABA‐binding pocket showing the ABA molecule totally buried by the latch and gate loops of PYR/PYL and the interaction with PP2C. (c) A superimposition of the structures of the apo form of CsPYL1 (Apo), the complex of CsPYL1 with ABA (ABA) and the ternary complex CsPYL1–ABA–HAB1 (ABA–PP2C). (d) A cartoon representation showing that the gate loop of the PYR/PYL ABA receptor and the activation loop of the SnRK2 kinase compete for the active site of PP2C, these interactions being mutually exclusive (see references in the text; the PDB codes are 5MOA, 5MN0, 3ZUT, 3UJG, 5MMQ and 5MMX).
Figure 3. The structure‐based chemical‐biology approach for plant performance under drought stress. (a) Chemical structures of ABA and quinabactin (left); superimposition of the ABA‐binding pocket of the PYL2 in complex with ABA and QN (right). (b) Details comparing the hydrogen bond and hydrophobic interaction of ABA and QN with the PYL2 ABA‐binding site (PDB codes: 3KB3, 4LA7). (c) Close view of the ligand binding site of the AtPYL2 in complex with pyrabactin (PDB code 3MNH) (left), the modelled complex between SlPYL1–ABA and PBI686; the structure of the ternary complex CsPYL1–ABA–PP2C is overlaid in semitransparent mode to highlight the predicted clashes between the PBI686 and F70 and L96 from the CsPYL1 in closed conformation (centre); and AtPYR1 in complex with AS6 (PDB code 3WG8) (right). The gate and the latch loops are highlighted in blue and cyan colours, respectively. Ligands are represented in a stick mode. The insets on each panel represent the chemical structures of the antagonist molecules.
Figure 4. Structural biology of the Ca2+‐ and ABA‐mediated response to salt stress. (a) Scheme showing the molecular mechanism of action of the plant cellular machinery dedicated to respond to salt stress. (b) Structural model of the activation of SOS1 Na+ extrusion by the CBL–CIPK complex SOS3–SOS2 and PP2C‐type phosphatase. (c) Domain organisation of CBL and CIPK proteins. (d) On the left, molecular surface representation of the crystallographic structure of the Ca2+ sensor SOS3 bound to the regulatory domain of the kinase SOS2 (ribbons), showing how SOS3 sequesters the self‐inhibitory domain of SOS2 leaving at the opposite side the PPI protein phosphatase interaction domain. On the right, the structure of the CIPK23 kinase domain that activates AKT1‐mediated K+ transport is depicted. The cavity where the self‐inhibitory NAF motif inserts to block kinase activity is shown as a light‐green volume. The activation domain (magenta) displays a close conformation and reaches the NAF docking region, thus stabilising an inactive conformation of the kinase. A black dashed line has been depicted to understand how the kinase and regulatory domain of CIPKs are segregated in the CBL–CIPK complex. The same colour code has been used throughout the figure for a better comprehension of the mechanism of action of these proteins.


Bassil E and Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX‐type cation/H transporters. Current Opinion in Plant Biology 22C: 1–6.

Batistic O, Sorek N, Schultke S, Yalovsky S and Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20: 1346–1362.

Batistic O and Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochimica et Biophysica Acta 1820: 1283–1293.

Belda‐Palazon B, Rodriguez L, Fernandez MA, et al. (2016) FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant Cell 28: 2291–2311.

Cao M, Liu X, Zhang Y, et al. (2013) An ABA‐mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Research 23: 1043–1054.

Chaves‐Sanjuan A, Sanchez‐Barrena MJ, Gonzalez‐Rubio JM, et al. (2014) Structural basis of the regulatory mechanism of the plant CIPK family of protein kinases controlling ion homeostasis and abiotic stress. Proceedings of the National Academy of Sciences of the United States of America 111: E4532–E4541.

Daram P, Urbach S, Gaymard F, Sentenac H and Cherel I (1997) Tetramerization of the AKT1 plant potassium channel involves its C‐terminal cytoplasmic domain. EMBO Journal 16: 3455–3463.

Diaz M, Sanchez‐Barrena MJ, Gonzalez‐Rubio JM, et al. (2016) Calcium‐dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proceedings of the National Academy of Sciences of the United States of America 113: E396–E405.

Dupeux F, Santiago J, Betz K, et al. (2011) A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO Journal 30: 4171–4184.

Fujii H, Chinnusamy V, Rodrigues A, et al. (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660–664.

Furihata T, Maruyama K, Fujita Y, et al. (2006) Abscisic acid‐dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences of the United States of America 103: 1988–1993.

Gierth M, Maser P and Schroeder JI (2005) The potassium transporter AtHAK5 functions in K(+) deprivation‐induced high‐affinity K(+) uptake and AKT1 K(+) channel contribution to K(+) uptake kinetics in Arabidopsis roots. Plant Physiology 137: 1105–1114.

Gonzalez‐Guzman M, Rodriguez L, Lorenzo‐Orts L, et al. (2014) Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. Journal of Experimental Botany 65: 4451–4464.

Guo Y, Halfter U, Ishitani M and Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13: 1383–1400.

Hao Q, Yin P, Li W, et al. (2011) The molecular basis of ABA‐independent inhibition of PP2Cs by a subclass of PYL proteins. Molecular Cell 42: 662–672.

Lee SC, Lan WZ, Kim BG, et al. (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proceedings of the National Academy of Sciences of the United States of America 104: 15959–15964.

Ma Y, Szostkiewicz I, Korte A, et al. (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064–1068.

Macarron R, Banks MN, Bojanic D, et al. (2011) Impact of high‐throughput screening in biomedical research. Nature Reviews. Drug Discovery 10: 188–195.

Mansilla A, Chaves‐Sanjuan A, Campillo NE, et al. (2017) Interference of the complex between NCS‐1 and Ric8a with phenothiazines regulates synaptic function and is an approach for fragile X syndrome. Proceedings of the National Academy of Sciences of the United States of America 114: E999–E1008.

Melcher K, Ng LM, Zhou XE, et al. (2009) A gate‐latch‐lock mechanism for hormone signalling by abscisic acid receptors. Nature 462: 602–608.

Melcher K, Xu Y, Ng LM, et al. (2010) Identification and mechanism of ABA receptor antagonism. Nature Structural & Molecular Biology 17: 1102–1108.

Miyazono K, Miyakawa T, Sawano Y, et al. (2009) Structural basis of abscisic acid signalling. Nature 462: 609–614.

Moreno‐Alvero M, Yunta C, Gonzalez‐Guzman M, et al. (2017) Structure of ligand‐bound intermediates of crop ABA receptors highlights PP2C as necessary ABA co‐receptor. Molecular Plant 10: 1250–1253.

Mosquna A, Peterson FC, Park SY, et al. (2011) Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist‐bound conformation. Proceedings of the National Academy of Sciences of the United States of America 108: 20838–20843.

Munemasa S, Hauser F, Park J, et al. (2015) Mechanisms of abscisic acid‐mediated control of stomatal aperture. Current Opinion in Plant Biology 28: 154–162.

Nishimura N, Sarkeshik A, Nito K, et al. (2010) PYR/PYL/RCAR family members are major in‐vivo ABI1 protein phosphatase 2C‐interacting proteins in Arabidopsis. Plant Journal 61: 290–299.

Nunez‐Ramirez R, Sanchez‐Barrena MJ, Villalta I, et al. (2012) Structural insights on the plant salt‐overly‐sensitive 1 (SOS1) Na(+)/H(+) antiporter. Journal of Molecular Biology 424: 283–294.

Okamoto M, Peterson FC, Defries A, et al. (2013) Activation of dimeric ABA receptors elicits guard cell closure, ABA‐regulated gene expression, and drought tolerance. Proceedings of the National Academy of Sciences of the United States of America 110: 12132–12137.

Osakabe Y, Yamaguchi‐Shinozaki K, Shinozaki K and Tran LS (2013) Sensing the environment: key roles of membrane‐localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany 64: 445–458.

Pardo JM (2010) Biotechnology of water and salinity stress tolerance. Current Opinion in Biotechnology 21: 185–196.

Park SY, Fung P, Nishimura N, et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068–1071.

Park SY, Peterson FC, Mosquna A, et al. (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520: 545–548.

Peterson FC, Burgie ES, Park SY, et al. (2010) Structural basis for selective activation of ABA receptors. Nature Structural & Molecular Biology 17: 1109–1113.

Pizzio GA, Rodriguez L, Antoni R, et al. (2013) The PYL4 A194T mutant uncovers a key role of PYR1‐LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signaling and plant drought resistance. Plant Physiology 163: 441–455.

Qadir M and Oster JD (2004) Crop and irrigation management strategies for saline‐sodic soils and waters aimed at environmentally sustainable agriculture. Science of the Total Environment 323: 1–19.

Quintero FJ, Martinez‐Atienza J, Villalta I, et al. (2011) Activation of the plasma membrane Na/H antiporter salt‐overly‐sensitive 1 (SOS1) by phosphorylation of an auto‐inhibitory C‐terminal domain. Proceedings of the National Academy of Sciences of the United States of America 108: 2611–2616.

Rajagopalan N, Nelson KM, Douglas AF, et al. (2016) Abscisic acid analogues that act as universal or selective antagonists of phytohormone receptors. Biochemistry 55: 5155–5164.

Rodriguez PL and Lozano‐Juste J (2015) Unnatural agrochemical ligands for engineered abscisic acid receptors. Trends in Plant Science 20: 330–332.

Saez A, Robert N, Maktabi MH, et al. (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiology 141: 1389–1399.

Sanchez‐Barrena MJ, Martinez‐Ripoll M, Zhu JK and Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. Journal of Molecular Biology 345: 1253–1264.

Sanchez‐Barrena MJ, Martinez‐Ripoll M and Albert A (2013) Structural biology of a major signaling network that regulates plant abiotic stress: the CBL‐CIPK mediated pathway. International Journal of Molecular Sciences 14: 5734–5749.

Santiago J, Dupeux F, Round A, et al. (2009a) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462: 665–668.

Santiago J, Rodrigues A, Saez A, et al. (2009b) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant Journal 60: 575–588.

Serrano R and Rodriguez‐Navarro A (2001) Ion homeostasis during salt stress in plants. Current Opinion in Cell Biology 13: 399–404.

Shi J, Kim KN, Ritz O, et al. (1999) Novel protein kinases associated with calcineurin B‐like calcium sensors in Arabidopsis. Plant Cell 11: 2393–2405.

Soon FF, Ng LM, Zhou XE, et al. (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335: 85–88.

Takeuchi J, Okamoto M, Akiyama T, et al. (2014) Designed abscisic acid analogs as antagonists of PYL‐PP2C receptor interactions. Nature Chemical Biology 10: 477–482.

Umezawa T, Sugiyama N, Mizoguchi M, et al. (2009) Type 2C protein phosphatases directly regulate abscisic acid‐activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 106: 17588–17593.

Vlad F, Rubio S, Rodrigues A, et al. (2009) Protein phosphatases 2C regulate the activation of the Snf1‐related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21: 3170–3184.

Yang Z, Liu J, Tischer SV, et al. (2016) Leveraging abscisic acid receptors for efficient water use in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 113: 6791–6796.

Yuan X, Yin P, Hao Q, et al. (2010) Single amino acid alteration between valine and isoleucine determines the distinct pyrabactin selectivity by PYL1 and PYL2. Journal of Biological Chemistry 285: 28953–28958.

Zhao Y, Chan Z, Gao J, et al. (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proceedings of the National Academy of Sciences of the United States of America 113: 1949–1954.

Zhu JK (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6: 441–445.

Further Reading

Food and Agriculture Organization of the United Nations (2016) FAOs' Work on Climate Change Conference, 2016. Food and Agriculture Organization of the United Nations,‐i6273e.pdf

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Sánchez‐Barrena, María J, Martinez‐Ripoll, Martín, and Albert, Armando(Mar 2018) Structural Biology of Salt and Drought Tolerance in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0027628]