Abstract
Main conclusion
To compensate for the lack of capacity for external salt storage in the epidermal bladder cells, quinoa plants employ tissue-tolerance traits, to confer salinity stress tolerance.
Abstract
Our previous studies indicated that sequestration of toxic Na+ and Cl− ions into epidermal bladder cells (EBCs) is an efficient mechanism conferring salinity tolerance in quinoa. However, some halophytes do not develop EBCs but still possess superior salinity tolerance. To elucidate the possible compensation mechanism(s) underlying superior salinity tolerance in the absence of the external salt storage capacity, we have selected four quinoa accessions with contrasting patterns of EBC development. Whole-plant physiological and electrophysiological characteristics were assessed after 2 days and 3 weeks of 400 mM NaCl stress. Both accessions with low EBC volume utilised Na+ exclusion at the root level and could maintain low Na+ concentration in leaves to compensate for the inability to sequester Na+ load in EBC. These conclusions were further confirmed by electrophysiological experiments showing higher Na+ efflux from roots of these varieties (measured by a non-invasive microelectrode MIFE technique) as compared to accessions with high EBC volume. Furthermore, accessions with low EBC volume had significantly higher K+ concentration in their leaves upon long-term salinity exposures compared to plants with high EBC sequestration ability, suggesting that the ability to maintain high K+ content in the leaf mesophyll was as another important compensation mechanism.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- BSM:
-
Basic salt media
- EBCs:
-
Epidermal bladder cells
- GORK:
-
Guard cell outward-rectifying K+ channel
- MIFE:
-
Microelectrode ion flux estimation
- NHX:
-
Na+(K+)/H+ exchanger
- SKOR:
-
Stelar K+ outward rectifier
- S(HBV):
-
Salt-sensitive accession with high bladder volume
- S(LBV):
-
Salt-sensitive accession with low bladder volume
- SOS1:
-
Salt overly sensitive 1
- T(HBV):
-
Salt-tolerant accession with high bladder volume
- T(LBV):
-
Salt-tolerant accession with low bladder volume
References
Adolf VI, Jacobsen S-E, Shabala S (2013) Salt tolerance mechanisms in quinoa (Chenopodium quinoa). Environ Exp Bot 92:43–54. https://doi.org/10.1016/j.envexpbot.2012.07.004
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431):1256–1258. https://doi.org/10.1126/science.285.5431.1256
Barkla BJ, Vera-Estrella R, Pantoja O (2012) Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Proteomics 12(18):2862–2865. https://doi.org/10.1002/pmic.201200152
Barragan V, Leidi EO, Andres Z, Rubio L, De Luca A, Fernandez JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142. https://doi.org/10.1007/s00299-019-02450-w
Bassil E, Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Curr Opin Plant Biol 22:1–6. https://doi.org/10.1016/j.pbi.2014.08.002
Bassil E, Tajima H, Liang Y-C, Ohto M-A, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011) The arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23:3482–3497. https://doi.org/10.1105/tpc.111.089581
Bassil E, Coku A, Blumwald E (2012) Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63(16):5727–5740. https://doi.org/10.1093/jxb/ers250
Bohm J, Messerer M, Muller HM, Scholz-Starke J, Gradogna A, Scherzer S, Maierhofer T, Bazihizina N, Zhang H, Stigloher C, Ache P, Al-Rasheid KAS, Mayer KFX, Shabala S, Carpaneto A, Haberer G, Zhu JK, Hedrich R (2018) Understanding the molecular basis of salt sequestration in epidermal bladder cells of Chenopodium quinoa. Curr Biol 28(19):3075–3085.e3077. https://doi.org/10.1016/j.cub.2018.08.004
Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng F, Jacobsen SE, Shabala S (2013) Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. Int J Mol Sci 14(5):9267–9285. https://doi.org/10.3390/ijms14059267
Bressan RA, Zhang C, Zhang H, Hasegawa PM, Bohnert HJ, Zhu JK (2001) Learning from the Arabidopsis experience The next gene search paradigm. Plant Physiol 127(4):1354–1360. https://doi.org/10.1104/pp.010752
Cao Y, Liang X, Yin P, Zhang M, Jiang C (2019) A domestication-associated reduction in K+-preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance. New Phytol 222(1):301–317. https://doi.org/10.1111/nph.15605
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28(10):1230–1246. https://doi.org/10.1111/j.1365-3040.2005.01364.x
Chen ZH, Cuin TA, Zhou MX, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15–16):4245–4255
Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34(6):947–961. https://doi.org/10.1111/j.1365-3040.2011.02296.x
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123(Pt 9):1468–1479. https://doi.org/10.1242/jcs.064352
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65(5):1259–1270. https://doi.org/10.1093/jxb/eru004
Feki K, Quintero FJ, Khoudi H, Leidi EO, Masmoudi K, Pardo JM, Brini F (2014) A constitutively active form of a durum wheat Na+/H+ antiporter SOS1 confers high salt tolerance to transgenic Arabidopsis. Plant Cell Rep 33(2):277–288. https://doi.org/10.1007/s00299-013-1528-9
Feng H, Tang Q, Cai J, Xu B, Xu G, Yu L (2019) Rice OsHAK16 functions in potassium uptake and translocation in shoot, maintaining potassium homeostasis and salt tolerance. Planta 250(2):549–561. https://doi.org/10.1007/s00425-019-03194-3
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179(4):945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94(5):647–655. https://doi.org/10.1016/s0092-8674(00)81606-2
Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Poree F, Boucherez J, Lebaudy A, Bouchez D, Véry AA, Simonneau T (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100(9):5549–5554. https://doi.org/10.1073/pnas.0733970100
Ishikawa T, Cuin TA, Bazihizina N, Shabala S (2018) Xylem ion loading and its implications for plant abiotic stress tolerance. Adv Bot Res 87:267–301. https://doi.org/10.1016/bs.abr.2018.09.006
Jiang X, Leidi EO, Pardo JM (2010) How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal Behav 5(7):792–795. https://doi.org/10.4161/psb.5.7.11767
Kiani-Pouya A, Roessner U, Jayasinghe NS, Lutz A, Rupasinghe T, Bazihizina N, Bohm J, Alharbi S, Hedrich R, Shabala S (2017) Epidermal bladder cells confer salinity stress tolerance in the halophyte quinoa and Atriplex species. Plant Cell Environ 40(9):1900–1915. https://doi.org/10.1111/pce.12995
Kiani-Pouya A, Rasouli F, Bazihizina N, Zhang H, Hedrich R, Shabala S (2019) A large-scale screening of quinoa accessions reveals an important role of epidermal bladder cells and stomatal patterning in salinity tolerance. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2019.103885
Lei B, Huang Y, Sun J, Xie J, Niu M, Liu Z, Fan M, Bie Z (2014) Scanning ion-selective electrode technique and X-ray microanalysis provide direct evidence of contrasting Na+ transport ability from root to shoot in salt-sensitive cucumber and salt-tolerant pumpkin under NaCl stress. Physiol Plant 152(4):738–748. https://doi.org/10.1111/ppl.12223
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Marschner H, George E, Römheld V (1995) Preface to second edition. In: Marschner H (ed) Mineral nutrition of higher plants. Academic Press, London, pp vii–viii. https://doi.org/10.1016/b978-012473542-2/50001-8
Maughan PJ, Turner TB, Coleman CE, Elzinga DB, Jellen EN, Morales JA, Udall JA, Fairbanks DJ, Bonifacio A (2009) Characterization of salt overly sensitive 1 (SOS1) gene homoeologs in quinoa (Chenopodium quinoa). Genome 52:647–657. https://doi.org/10.1139/G09-041
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59(1):651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Munns R, Passioura JB, Colmer TD, Byrt CS (2019) Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol. https://doi.org/10.1111/nph.15862
Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40(9):832–847. https://doi.org/10.1071/fp12389
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99(12):8436–8441. https://doi.org/10.1073/pnas.122224699
Rubio F, Nieves-Cordones M, Horie T, Shabala S (2019) Doing ‘business as usual’ comes with a cost: evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions. New Phytol. https://doi.org/10.1111/nph.15852
Ruiz-Carrasco K, Antognoni F, Coulibaly AK, Lizardi S, Covarrubias A, Martinez EA, Molina-Montenegro MA, Biondi S, Zurita-Silva A (2011) Variation in salinity tolerance of four lowland genotypes of quinoa (Chenopodium quinoa) as assessed by growth, physiological traits, and sodium transporter gene expression. Plant Physiol Biochem 49(11):1333–1341. https://doi.org/10.1016/j.plaphy.2011.08.005
Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497(7447):60–66. https://doi.org/10.1038/nature11909
Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60(3):709–712. https://doi.org/10.1093/jxb/erp013
Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112(7):1209–1221. https://doi.org/10.1093/aob/mct205
Shabala S, Mackay A (2011) Ion transport in halophytes. Adv Bot Res 57:151–199. https://doi.org/10.1016/b978-0-12-387692-8.00005-9
Shabala SN, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113(1):111–118. https://doi.org/10.1104/pp.113.1.111
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141(4):1653–1665. https://doi.org/10.1104/pp.106.082388
Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends Plant Sci 19(11):687–691. https://doi.org/10.1016/j.tplants.2014.09.001
Shabala S, Bose J, Fuglsang AT, Pottosin I (2016a) On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. J Exp Boty 67:1015–1031
Shabala L, Zhang J, Pottosin I, Bose J, Zhu M, Fuglsang AT, Velarde-Buendia A, Massart A, Hill CB, Roessner U, Bacic A, Wu H, Azzarello E, Pandolfi C, Zhou M, Poschenrieder C, Mancuso S, Shabala S (2016b) Cell-type-specific H+-ATPase activity in root tissues enables K+ retention and mediates acclimation of barley (Hordeum vulgare) to salinity stress. Plant Physiol 172(4):2445–2458. https://doi.org/10.1104/pp.16.01347
Shao Q, Han N, Ding T, Zhou F, Wang B (2014) SsHKT1;1 is a potassium transporter of the C3 halophyte (Suaeda salsa) that is involved in salt tolerance. Funct Plant Biol 41(8):790–802
Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14(2):465–477. https://doi.org/10.1105/tpc.010371
Ullah A, Dutta D, Fliegel L (2016) Expression and characterization of the SOS1 Arabidopsis salt tolerance protein. Mol Cell Biochem 415(1–2):133–143. https://doi.org/10.1007/s11010-016-2685-2
Venema K, Belver A, Marin-Manzano MC, Rodriguez-Rosales MP, Donaire JP (2003) A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. J Biol Chem 278:22453–22459. https://doi.org/10.1371/journal.pone.0078098
Véry A-A, Nieves-Cordones M, Daly M, Khan I, Fizames C, Sentenac H (2014) Molecular biology of K+ transport across the plant cell membrane: what do we learn from comparison between plant species? J Plant Physiol 171(9):748–769. https://doi.org/10.1016/j.jplph.2014.01.011
Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots: a procedure to isolate protoplasts from this tissue and a patch-clamp exploration of salt passageways into xylem vessels. Plant Physiol 105(3):799–813. https://doi.org/10.1104/pp.105.3.799
Wu H, Zhu M, Shabala L, Zhou M, Shabala S (2015) K+ retention in leaf mesophyll, an overlooked component of salinity tolerance mechanism: a case study for barley. J Integr Plant Biol 57(2):171–185. https://doi.org/10.1111/jipb.12238
Wu H, Zhang X, Giraldo JP, Shabala S (2018) It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant Soil 431(1–2):1–17. https://doi.org/10.1007/s11104-018-3770-y
Wu H, Shabala L, Zhou M, Su N, Wu Q, Ul-Haq T, Zhu J, Mancuso S, Azzarello E, Shabala S (2019) Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance. Plant J. https://doi.org/10.1111/tpj.14424
Xu H, Jiang X, Zhan K, Cheng X, Chen X, Pardo JM, Cui D (2008) Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Arch Biochem Biophys 473(1):8–15. https://doi.org/10.1016/j.abb.2008.02.018
Zeng F, Shabala S, Maksimovic JD, Maksimovic V, Bonales-Alatorre E, Shabala L, Yu M, Zhang G, Zivanovic BD (2018) Revealing mechanisms of salinity tissue tolerance in succulent halophytes: a case study for Carpobrotus rossi. Plant Cell Environ 41(11):2654–2667. https://doi.org/10.1111/pce.13391
Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98(22):12832–12836. https://doi.org/10.1073/pnas.231476498
Zou C, Chen A, Xiao L, Muller HM, Ache P, Haberer G, Zhang M, Jia W, Deng P, Huang R, Lang D, Li F, Zhan D, Wu X, Zhang H, Bohm J, Liu R, Shabala S, Hedrich R, Zhu JK, Zhang H (2017) A high-quality genome assembly of quinoa provides insights into the molecular basis of salt bladder-based salinity tolerance and the exceptional nutritional value. Cell Res 27:1327–1340. https://doi.org/10.1038/cr.2017.124
Acknowledgements
This work was supported by Australian Research Council DP150101663 grant to S.S.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kiani-Pouya, A., Rasouli, F., Shabala, L. et al. Understanding the role of root-related traits in salinity tolerance of quinoa accessions with contrasting epidermal bladder cell patterning . Planta 251, 103 (2020). https://doi.org/10.1007/s00425-020-03395-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03395-1