Regulation of Na<sup>+</sup> and K<sup>+</sup> homeostasis in plants: towards improved salt stress tolerance in crop plants

Almeida, Diego M.; Oliveira, M. Margarida; Saibo, Nelson J. M.

doi:10.1590/1678-4685-GMB-2016-0106

Diego M. Almeida

Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal.

M. Margarida Oliveira

Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal.

Nelson J. M. Saibo Send correspondence to Nelson J.M. Saibo. Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Av. da República, 2780-157 Oeiras, Portugal. E-mail: saibo@itqb.unl.pt

Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Oeiras, Portugal.

Send correspondence to Nelson J.M. Saibo. Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Av. da República, 2780-157 Oeiras, Portugal. E-mail: saibo@itqb.unl.pt

Figures (3)
Tables (2)

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Figure 1
Schematic representation showing key plasma and tonoplast membrane transporters, channels and pumps mediating Na⁺ and K⁺ homeostasis in plants under salt stress (adapted from Roy et al., 2014Roy SJ, Negrão S and Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115-124.). Na⁺ ions enter the cells via Non Selective Cation Channels (NSCCs) and possibly via other cation transporters not shown (symplast flow - blue arrow) and through the cell wall and intercellular spaces (apoplast flow - red arrow). The Na⁺/H⁺ antiporter SOS1 extrudes Na⁺ at the root soil interface, thus reducing the Na⁺ net influx of Na⁺. At the xylem parenchyma cells, HKT1-like proteins retrieve Na⁺ from the xylem sap, thereby restricting the amount of Na⁺ reaching the photosynthetic tissues. To translocate Na⁺ back to the root, ions unloaded from xylem may be transported into phloem via additional HKT1-like protein. In addition, HKT1-like proteins also load Na⁺ into shoot phloem, and then Na⁺ is transferred into roots via phloem, preventing Na⁺ accumulation in shoots. SOS1, localized in the xylem parenchyma cells, is also suggested to mediate Na⁺ efflux from xylem vessels under high salinity. Incoming Na⁺, in root and shoots, is stored in the large central vacuole by tonoplast-localized NHX exchangers (NHX1-4). Plasma membrane (PM) H⁺-ATPase (P-ATPase), PM H⁺-PPase (PM-PPase), tonoplast H⁺-ATPase (V-ATPase) and tonoplast H⁺-PPase (V-PPase) generate electrochemical potential gradient for secondary active transport.

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Figure 2
Schematic representation of a hypothetical Arabidopsis cell indicating subcellular localizations, functions, and regulations of NHXs antiporters (NHX1-6), plasma membrane H⁺-ATPase (P-ATPase), tonoplast H⁺-ATPase (V-ATPase), tonoplast H⁺-PPase (V-PPase) and SOS1 (adapted from Bassil et al., 2012Bassil E, Coku A and Blumwald E (2012) Cellular ion homeostasis: Emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63:5727-5740.). Trans-Golgi network (TGN), and prevacuolar compartment (PVC).

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Figure 3
Structural model of the plant V-ATPase adapted from Gaxiola et al. (2007)Gaxiola RA, Palmgren MG and Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204-2214.. The peripheral V₁ complex (blue) and the membrane integral V₀ complex (orange) are linked through a peripheral stalk formed by subunits a, C, E, G and H. Hydrolysis of ATP is coupled with H⁺ transport to the vacuole.

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Table 1
List of NHX antiporters including information about species, transport selectivity, tissue localization, sub-cellular localization and plant function for each NHX antiporter described in this review. No information available (N/A), Plasma membrane (PM), trans-Golgi network (TGN), and prevacuolar compartment (PVC).

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Table 2
List of HKT transporters including information about class, species, transport selectivity, tissue localization, subcellular localization and plant function for each HKT transporter described in this review. No information available (N/A), Plasma membrane (PM).

Transporter	Species	Transport selectivity	Tissue localization	Subcellular localization	Function in planta	Refs.
AtNHX1	Arabidopsis	Na⁺/K⁺	Roots: Vascular tissues Shoots: Floral and vascular tissues, guard cells, trichome.	Tonoplast	K⁺ homeostasis and pH regulation	*Rodríguez-Rosales et al., 2009Rodríguez-Rosales MP, Galvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O and Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265-276.; Bassil et al., 2011bBassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T and Blumwald E (2011b) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224-239.; Yokoi et al., 2002*Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM and Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529-539.
AtNHX2	Arabidopsis	Na⁺/K⁺	Roots Shoots: High in guard cells	Tonoplast	K⁺ homeostasis and pH regulation
AtNHX3	Arabidopsis	Na⁺/K⁺	Mainly in roots	Tonoplast	N/A
AtNHX4	Arabidopsis	Na⁺/K⁺	Shoots: Mainly in mature pollen and seeds	Tonoplast	N/A
AtNHX5	Arabidopsis	Na⁺/K⁺	Roots Shoots: High in guard cells	TGN, PVC	pH homeostasis in TGN, PVC
AtNHX6	Arabidopsis	Na⁺/K⁺	Roots Shoots: High in guard cells	TGN, PVC	pH homeostasis in TGN, PVC
AtNHX7/SOS1	Arabidopsis	Na⁺	Roots: Epidermal cells (particularly root tip), parenchyma cells lining the vasculature Shoots	PM	Na⁺ efflux	*Martínez-Atienza et al., 2007Martinéz-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM and Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001-1012.; Shi and Zhu, 2002Shi H and Zhu JK (2002) Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol 50:543-550.; Kronzucker and Britto, 2011*Kronzucker HJ and Britto DT (2011) Sodium transport in plants: A critical review. New Phytol 189:54-81.
AtNHX8	Arabidopsis	N/A	N/A	PM	N/A	N/A
OsNHX1	Rice	Na⁺/K⁺	Roots: Stela, emerging parts of lateral roots. Shoots: Basel part of seedling shoot, vascular bundle, flag leaf sheaths, panicles, guard cells, trichome.	Tonoplast	N/A	*Fukada et al., 2004Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H and Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146-159.; Fukada et al., 2011Fukuda A, Nakamura A, Hara N, Toki S and Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175-188.; Bassil et al., 2012*Bassil E, Coku A and Blumwald E (2012) Cellular ion homeostasis: Emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63:5727-5740.
OsNHX2	Rice	Na⁺/K⁺	Shoots: Flag leaf sheaths, panicles.	Tonoplast	N/A
OsNHX3	Rice	Na⁺/K⁺	Shoots: Flag leaf sheaths, panicles.	Tonoplast	N/A
OsNHX4	Rice	N/A	N/A	Tonoplast	N/A
OsNHX5	Rice	Na⁺/K⁺	Roots: Stela, emerging parts of lateral roots, root tip. Shoots: Basel part of seedling shoot, vascular bundle, flag leaf sheaths, panicles, pollen grain.	TGN, PVC	N/A
OsNHX7/OsSOS1	Rice	Na⁺	Roots and shoots	PM	Na⁺ efflux	*Martinéz-Atienza et al., 2007*Martinéz-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM and Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001-1012.

Transporter	Species	Transport selectivity	Tissue localization	Subcellular localization	Function in planta	Refs.
Class I
AtHTK1;1	Arabidopsis	Na⁺	Roots: Xylem parenchyma, phloem Shoots: Phloem	PM	Unload Na⁺ from the xylem transpiration stream Load of Na⁺ into shoot pholem	*Berthomieu et al., 2003Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oik S, Yamada K, Cellier F, et al. (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004-2014.; Møller et al., 2009Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J and Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 7:2163-2178.; Sunarpi et al., 2005*Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, et al. (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J. 44:928-938.
OsHTK1;1	Rice	Na⁺	Roots: Similar as OsHKT2;1 Leaves: Bulliform cells and vascular tissues	PM	N/A	*Jabnoune et al., 2009*Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL, Conejero G, Rodríguez-Navarro A, Sentenac H, Guiderdoni E, Abdelly C, et al. (2009) Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955-1971.
OsHTK1;2	Rice	N/A	N/A	PM	N/A	*Wu et al., 2009*Wu Y, Hu Y and Xu G (2009) Interactive effects of potassium and sodium on root growth and expression of K+/Na+ transporter genes in rice. Plant Growth Regulation 57:271-280.
OsHTK1;3	Rice	Na⁺	Roots: Cortex and vascular tissues in the stele. Leaves: Bulliform cells and vascular tissues, mesophyll cells.	PM	N/A	*Jabnoune et al., 2009*Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL, Conejero G, Rodríguez-Navarro A, Sentenac H, Guiderdoni E, Abdelly C, et al. (2009) Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955-1971.
OsHTK1;4	Rice	N/A	Leaves sheaths	PM	Control of sheath to blade transfer of Na⁺	*Cotsaftis et al., 2012*Cotsaftis O, Plett D, Shirley N, Tester M and Hrmova M (2012) A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS ONE 7:e39865.
OsHTK1;5	Rice	Na⁺	Roots and Shoots: Xylem parenchyma	PM	Unload Na⁺ from the xylem transpiration stream	*Ren et al., 2005*Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S and Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141-1146.
TaHKT1;4	Wheat	Na⁺	Roots and Leaves	PM	Unload Na⁺ from the xylem transpiration stream	*Huang et al., 2006*Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES and Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol. 142:1718-1727.
TaHKT1;5	Wheat	Na⁺	Roots	PM	Unload Na⁺ from the xylem transpiration stream	*Byrt et al., 2007Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M and Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918-1928.;Munns et al., 2012*Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, et al. (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360-364.
Class II
OsHKT2;1	Rice	Na⁺/K⁺	Roots: Epidermis, exodermis, cortex differentiated into aerenchyma, stele (mainly pholem). Leaves: Bulliform cells, xylem, phloem, mesophyll cells.	PM	Nutritional Na⁺ uptake from the external medium.	*Jabnoune et al., 2009Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL, Conejero G, Rodríguez-Navarro A, Sentenac H, Guiderdoni E, Abdelly C, et al. (2009) Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955-1971.; Horie et al., 2007*Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G and Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 20:3003-3014.
OsHKT2;2	Rice	Na⁺/K⁺	Roots	PM	Na⁺ and K⁺ uptake under K⁺ starvation conditions.	*Yao et al., 2010Yao X, Horie T, Xue S, Leung HY, Katsuhara M, Brodsky DE, Wu Y and Schroeder JI (2010) Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol 152:341-355.; Oomen et al., 2012*Oomen RJ, Benito B, Sentenac H, Rodríguez-Navarro A, Talón M, Véry AA and Domingo C (2012) HKT2;2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. Plant J 71:750-762.
TaHKT2;1	Wheat	Na⁺/K⁺	Roots: Cortical and stele Leaves: Vasculature tissue of mesophyll.	PM	Na⁺ uptake from external medium.	Schachtman and Schroeder, 1994Schachtman DP and Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature.370:655-658.
HvHKT2;1	Barley	Na⁺/K⁺	Roots: Cortex. Leaves: Blade and sheath.	PM	K⁺ uptake at very low K⁺ concentrations (possible) and uptake of Na⁺ in the roots (possible).	Mian et a., 2011Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ and Very AA (2011) Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468-479.; *Haro et al., 2005*Haro R, Bañuelos MA, Senn ME, Barrero-Gil J and Rodríguez-Navarro A (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol. 139:1495-1506.

[1] Send correspondence to Nelson J.M. Saibo. Genomics of Plant Stress Unit, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Av. da República, 2780-157 Oeiras, Portugal. E-mail: saibo@itqb.unl.pt

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Regulation of Na⁺ and K⁺ homeostasis in plants: towards improved salt stress tolerance in crop plants

Abstract

Brasil

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Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants

Abstract

Regulation of Na⁺ and K⁺ homeostasis in plants: towards improved salt stress tolerance in crop plants