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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

ZxNHX1 indirectly participates in controlling K+ homeostasis in the xerophyte Zygophyllum xanthoxylum

Tian-Ge Gao A , Cui-Min Ma A , Hui-Jun Yuan A B , Hai-Shuang Liu A , Qing Ma A , Timothy J. Flowers C and Suo-Min Wang https://orcid.org/0000-0003-0027-8822 A D
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, PR China.

B School of Life Science and Engineering, Lanzhou University of Technology, Lanzhou 730050, PR China.

C Department of Evolution Behaviour and Environment, School of Life Sciences, University of Sussex, Falmer, Brighton, Sussex BN1 9QG, UK.

D Corresponding author. Email: smwang@lzu.edu.cn

Functional Plant Biology - https://doi.org/10.1071/FP20185
Submitted: 24 June 2020  Accepted: 6 November 2020   Published online: 7 December 2020

Abstract

The succulent xerophyte Zygophyllum xanthoxylum (Bunge) Engl. can absorb Na+ from the soil as an osmoticum in order to resist osmotic stress. The tonoplast Na+/H+ antiporter ZxNHX1 is essential for maintaining the salt-accumulation characteristics of Z. xanthoxylum by compartmentalizing Na+ into vacuoles. Previous results revealed that the silencing of ZxNHX1 greatly decreased Na+ accumulation in Z. xanthoxylum under 50 mM NaCl due to the weakened compartmentalisation; in addition, K+ concentration also significantly reduced in ZxNHX1-RNAi lines. Yet, whether the reduction of K+ concentration was directly triggered by the silencing of ZxNHX1 remains unclear. In this study, the growth parameters and expression levels of ZxSOS1, ZxHKT1;1, ZxAKT1 and ZxSKOR were measured in wild-type and ZxNHX1-RNAi lines under control or –0.5 MPa osmotic stress. The results showed that the silencing of ZxNHX1 inhibited the plant growth, decreased Na+ concentration in leaves, reduced the transcript abundance of ZxSOS1 and dramatically increased that of ZxHKT1;1 in roots of Z. xanthoxylum under osmotic stress; whereas tissue K+ concentrations and the expression level of ZxSKOR displayed no significant variations, and the expression of ZxAKT1 were significantly reduced in ZxNHX1-RNAi lines under osmotic stress, compared with the wild type. These results suggest that in Z. xanthoxylum, ZxNHX1 can maintain the normal growth by compartmentalizing Na+ into vacuoles, and regulate the spatial distribution of Na+ indirectly by affecting the expressions of ZxSOS1 and ZxHKT1;1. Moreover, the silencing of ZxNHX1 is not the main reason that led to the reduction of K+ concentration in ZxNHX1-RNAi lines under 50 mM NaCl, and ZxNHX1 might be indirectly involved in regulating K+ homeostasis.

Keywords: K+ transport, Na+ transport, osmotic stress, succulent, xerophyte, ZxNHX1, Zygophyllum xanthoxylum.


References

Agarwal PK, Shukla PS, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Molecular Biotechnology 54, 102–123.
Bioengineering for salinity tolerance in plants: state of the art.Crossref | GoogleScholarGoogle Scholar | 22539206PubMed |

Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Letters 581, 2247–2254.
Na+ transport in plants.Crossref | GoogleScholarGoogle Scholar | 17459382PubMed |

Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 10455050PubMed |

Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández 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. The Plant Cell 24, 1127–1142.
Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22438021PubMed |

Bassil E, Zhang S, Gong H, Tajima H, Blumwald E (2019) Cation specificity of vacuolar NHX-type cation/H+ antiporters. Plant Physiology 179, 616–629.
Cation specificity of vacuolar NHX-type cation/H+ antiporters.Crossref | GoogleScholarGoogle Scholar | 30498025PubMed |

Blumwald E, Poole RJ (1987) Salt tolerance in suspension cultures of sugar beet-induction of Na+/H+ antiport activity at the tonoplast by growth in salt. Plant Physiology 83, 884–887.
Salt tolerance in suspension cultures of sugar beet-induction of Na+/H+ antiport activity at the tonoplast by growth in salt.Crossref | GoogleScholarGoogle Scholar | 16665356PubMed |

Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 18662937PubMed |

Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends in Plant Science 19, 371–379.
Plant salt-tolerance mechanisms.Crossref | GoogleScholarGoogle Scholar | 24630845PubMed |

Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology 28, 89–121.
The mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |

Franks PJ (2006) Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients. Plant, Cell & Environment 29, 584–592.
Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients.Crossref | GoogleScholarGoogle Scholar |

Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. The Plant Journal 34, 788–801.
Sodium transport and HKT transporters: the rice model.Crossref | GoogleScholarGoogle Scholar | 12795699PubMed |

Gu M, Li N, Shao T, Long X, Brestic M, Shao H, Li JB, Mbarki S (2016) Accumulation capacity of ions in cabbage (Brassica oleracea L.) supplied with sea water. Plant, Soil and Environment 62, 314–320.
Accumulation capacity of ions in cabbage (Brassica oleracea L.) supplied with sea water.Crossref | GoogleScholarGoogle Scholar |

Guo Q, Wang P, Ma Q, Zhang JL, Bao AK, Wang SM (2012) Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora. Functional Plant Biology 39, 1047–1057.
Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora.Crossref | GoogleScholarGoogle Scholar | 32480854PubMed |

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 15012199PubMed |

Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends in Plant Science 14, 660–668.
HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants.Crossref | GoogleScholarGoogle Scholar | 19783197PubMed |

Ivashikina N, Hedrich R (2005) K+ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. The Plant Journal 41, 606–614.
K+ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels.Crossref | GoogleScholarGoogle Scholar | 15686523PubMed |

Janz D, Polle A (2012) Harnessing salt for woody biomass production. Tree Physiology 32, 1–3.
Harnessing salt for woody biomass production.Crossref | GoogleScholarGoogle Scholar | 22262675PubMed |

Kim HY, Choi EH, Min MK, Hwang H, Moon SJ, Yoon I, Byun MO, Kim BG (2015) Differential gene expression of two outward-rectifying shaker-like potassium channels OsSKOR and OsGORK in rice. Journal of Plant Biology 58, 230–235.
Differential gene expression of two outward-rectifying shaker-like potassium channels OsSKOR and OsGORK in rice.Crossref | GoogleScholarGoogle Scholar |

Liu FL, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environmental and Experimental Botany 54, 33–40.
Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying.Crossref | GoogleScholarGoogle Scholar |

Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiology 32, 4–13.
Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar | 21979327PubMed |

Ma Q, Li YX, Yuan HJ, Hu J, Wei L, Bao AK, Zhang JL, Wang SM (2014) ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum. Plant and Soil 374, 661–676.
ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar |

Ma Q, Hu J, Zhou XR, Yuan HJ, Kumar T, Luan S, Wang SM (2017) ZxAKT1 is essential for K+ uptake and K+/Na+ homeostasis in the succulent xerophyte Zygophyllum xanthoxylum. The Plant Journal 90, 48–60.
ZxAKT1 is essential for K+ uptake and K+/Na+ homeostasis in the succulent xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar | 28008679PubMed |

Maathuis FJ, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Annals of Botany 84, 123–133.
K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios.Crossref | GoogleScholarGoogle Scholar |

Martìnez JP, Leden JF, Lutts S (2003) Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency in relation to osmotic adjustment in two populations of Atriplex halimus L. Plant Growth Regulation 41, 63–73.
Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency in relation to osmotic adjustment in two populations of Atriplex halimus L.Crossref | GoogleScholarGoogle Scholar |

Martínez JP, Kinet JM, Lutts S, Bajji M (2005) NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. Journal of Experimental Botany 56, 2421–2431.
NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L.Crossref | GoogleScholarGoogle Scholar | 16043453PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 18444910PubMed |

Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive Na+/H+ antiporter during salinity stress. Plant Physiology 136, 2548–2555.
Protection of plasma membrane K+ transport by the salt overly sensitive Na+/H+ antiporter during salinity stress.Crossref | GoogleScholarGoogle Scholar | 15347782PubMed |

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. Proceedings of the National Academy of Sciences of the United States of America 99, 8436–8441.
Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3.Crossref | GoogleScholarGoogle Scholar | 12034882PubMed |

Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiology 132, 1041–1052.
Na+/H+ exchange activity in the plasma membrane of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12805632PubMed |

Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112, 1209–1221.
Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops.Crossref | GoogleScholarGoogle Scholar | 24085482PubMed |

Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 18724408PubMed |

Shi H, Quintero FJ, Pardo JM, Zhu J (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465–477.
The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants.Crossref | GoogleScholarGoogle Scholar | 11884687PubMed |

Subbarao GV, Wheeler RM, Stutte GW (2000) Feasibility of substituting sodium for potassium in crop plants for advanced life support systems. Journal of Life Support and Biosphere Science 7, 225–232.

Sunarpi , Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. The Plant Journal 44, 928–938.
Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells.Crossref | GoogleScholarGoogle Scholar | 16359386PubMed |

Tahjib-Ul-Arif M, Sohag AAM, Afrin S, Bashar KK, Afrin T, Mahamud AGMSU, Polash MAS, Hossain MT, Sohel MAT, Brestic M, Murata Y (2019) Differential response of sugar beet to long-term mild to severe salinity in a soil-pot culture. Agriculture 9, 222–240.

Tang X, Mu X, Shao H, Wang H, Brestic M (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology 35, 425–437.
Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology.Crossref | GoogleScholarGoogle Scholar | 24738851PubMed |

Ueda A, Kanechi M, Uno Y, Inagaki N (2003) Photosynthetic limitations of a halophyte sea aster (Aster tripolium L.) under water stress and NaCl stress. Journal of Plant Research 116, 63–68.
Photosynthetic limitations of a halophyte sea aster (Aster tripolium L.) under water stress and NaCl stress.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annual Review of Plant Biology 64, 451–476.
Potassium transport and signaling in higher plants.Crossref | GoogleScholarGoogle Scholar | 23330792PubMed |

Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. Journal of Arid Environments 56, 525–539.
The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China.Crossref | GoogleScholarGoogle Scholar |

Wang SM, Zhao GQ, Gao YS, Tang ZC, Zhang CL (2005) Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat. Journal of Plant Nutrition 27, 1841–1857.
Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat.Crossref | GoogleScholarGoogle Scholar |

Wu GQ, Xi JJ, Wang Q, Bao AK, Ma Q, Zhang JL, Wang SM (2011) The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. Journal of Plant Physiology 168, 758–767.
The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought.Crossref | GoogleScholarGoogle Scholar | 21216025PubMed |

Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science 10, 615–620.
Developing salt-tolerant crop plants: challenges and opportunities.Crossref | GoogleScholarGoogle Scholar | 16280254PubMed |

Yan K, Shao HB, Shao CY, Chen P, Zhao SJ, Brestic M, Chen XB (2013) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiologiae Plantarum 35, 2867–2878.
Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone.Crossref | GoogleScholarGoogle Scholar |

Yuan HJ, Ma Q, Wu GQ, Wang P, Hu J, Wang SM (2015) ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Annals of Botany 115, 495–507.
ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport.Crossref | GoogleScholarGoogle Scholar | 25252687PubMed |

Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. Journal of Arid Environments 87, 153–160.
NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar |