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Tetraploid exhibits more tolerant to salinity than diploid in sugar beet (Beta vulgaris L.)

  • Guo-Qiang WuEmail author
  • Li-Yuan Lin
  • Qi Jiao
  • Shan-Jia Li
Original Article
  • 64 Downloads

Abstract

Soil salinity is one of the major environmental stress factors limiting crops growth, development, and productivity worldwide. The aim of this study was to compare differences of salinity tolerance between diploid (cv. TY03209) and tetraploid (cv. TY03410) seedlings of sugar beet (Beta vulgaris L.) treated with various concentrations (0, 50, 100, 200, and 300 mM) of NaCl. Our results indicated that fresh weight (FW) and dry weight (DW) of shoot in tetraploid were remarkably higher than those in diploid when subjected to various concentrations of NaCl (except for FW under 200 mM). At 200 and 300 mM NaCl, tetraploid obviously accumulated less Na+ in its shoots and roots compared with diploid. However, there were no differences in K+ accumulation between tetraploid and diploid under salinity stress. Our results also showed tetraploid displayed a smaller Na+/K+ ratio and a stronger selective capacity for K+ over Na+ than diploid when exposed to high-salt stress (300 mM). Furthermore, it was observed that tetraploid possessed a bigger net K+ uptake rate and a smaller net Na+ uptake rate compared to diploid at high-salt condition. We also investigated the relative expression levels of six genes related to K+ and Na+ transport in roots of diploid and tetraploid by qRT-PCR method, and found that BvHKT1;1, BvNHX1, BvSKOR, and BvSOS1 were induced by additional 50 mM NaCl, and their transcript abundances in tetraploid were relatively higher than those in diploid. The expression level of BvAKT1 was down-regulated in tetraploid during 3–48 h of salt treatment, whilst basically remained unchanged in diploid. It was observed that the transcript abundance of BvHAK5 in diploid displayed the reduced trend with the prolonging of salt treatment time compared to tetraploid. In addition, soluble sugars contents were obviously higher in tetraploid than in diploid exposed to 100, 200, and 300 mM NaCl. Taken together, these results suggested that tetraploid exhibited more tolerant to salinity stress than diploid in sugar beet by accumulating less Na+ and more soluble sugars, and by maintaining lower Na+/K+ ratio and greater capacity of selective absorption for K+ over Na+. The results of this study provide insights into physiological and molecular consequences of polyploidization in sugar beet.

Keywords

Sugar beet Diploid Tetraploid Na+ toxicity Na+ and K+ transporters Salinity tolerance 

Abbreviations

AKT1

Arabidopsis K+ transporter 1

ANOVA

Analysis of variance

BT

Before treatments

Ct

Cycle threshold

DW

Dry weight

FW

Fresh weight

HAK5

High-affinity K+ transporter 5

HKT1

High-affinity K+ transporter 1

KT

K+ transporter

KUP

K+ uptake protein

RFW

Root fresh weigh

NXH1

Tonoplast Na+/H+ antiporter 1

qRT-PCR

Quantitative reverse transcription-polymerase chain reaction

SA

Selective absorption for K+ over Na+

SE

Standard error

SKOR

Shaker-like K+ outward rectifying channel

SOS1

Salt overly sensitive 1

ST

Selective transport for K+ over Na+

TEA

Tetraethylammonium

UV

Ultra violet

XPCs

Xylem parenchyma cells

Notes

Acknowledgements

The research was supported jointly by the National Natural Science Foundation of China (Grant nos. 31860404 and 31460101) and the Natural Science Foundation of Gansu Province, China (18JR3RA152). We thank Dr. Chun-Mei Wang for assistance with Na+ and K+ measurement. We are also grateful to Prof. Hua-Zhong Wang, from Heilongjiang University, China, kindly providing seeds of two sugar beet cultivars for this research.

References

  1. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2011) Root K+ acquisition in plants: The Arabidopsis thaliana model. Plant Cell Physiol 52:1603–1612PubMedGoogle Scholar
  2. Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opin Biotech 13:146–150PubMedGoogle Scholar
  3. Ardie SW, Liu SK, Takano T (2010) Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis. Plant Cell Rep 29:865–874PubMedGoogle Scholar
  4. Arzani A, Ashraf M (2016) Smart engineering of genetic resources for enhanced salinity tolerance in crop plants. Crit Rev Plant Sci 35:146–189Google Scholar
  5. Banjara M, Zhu L, Shen G, Payton P, Zhang H (2012) Expression of an Arabidopsis sodium/proton antiporter gene (AtNHX1) in peanut to improve salt tolerance. Plant Biotech Rep 6:59–67Google Scholar
  6. Bao AK, Guo ZG, Zhang HF, Wang SM (2009) A procedure for assessing the salt tolerance of Lucerne (Medicago sativa L.) cultivar seedlings by combining agronomic and physiological indicators. New Zeal. J Agr Res 52:435–442Google Scholar
  7. Beyaz R, Alizadeh B, Gürel S, Özcan FS, Yildiz M (2013) Sugar beet (Beta vulgaris L.) growth at different ploidy levels. Caryologia 66:90–95Google Scholar
  8. Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494PubMedGoogle Scholar
  9. Chao DY, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, Salt DE (2013) Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341:658–659PubMedPubMedCentralGoogle Scholar
  10. Chen LH, Zhang B, Xu ZQ (2008) Salt tolerance conferred by overexpression of Arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1 in common buckwheat (Fagopyrum esculentum). Transgenic Res 17:121–132PubMedGoogle Scholar
  11. Chen SL, Hawighorst P, Sun J, Polle A (2014) Salt tolerance in Populus: significance of stress signaling networks, mycorrhization, and soil amendments for cellular and whole-plant nutrition. Environ Exp Bot 107:113–124Google Scholar
  12. Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507PubMedGoogle Scholar
  13. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379PubMedPubMedCentralGoogle Scholar
  14. Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. J Plant Physiol 171:696–707PubMedGoogle Scholar
  15. Dohm JC, Minoche AE, Holtgräwe D, Capellagutiérrez S, Zakrzewski F, Tafer H, Rupp O, Sörensen TR, Stracke R, Reinhardt R (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549PubMedGoogle Scholar
  16. Dong Y, Fan G, Zhao Z, Xu E, Deng M, Wang L, Niu S (2017) Transcriptome-wide profiling and expression analysis of two accessions of Paulownia australis under salt stress. Tree Genet Genomes 13:97Google Scholar
  17. Duan HR, Ma Q, Zhang JL, Hu J, Bao AK, Wei L, Wang Q, Luan S, Wang SM (2015) The inward-rectifying K+ channel SsAKT1 is a candidate involved in K+ uptake in the halophyte Suaeda salsa under saline condition. Plant Soil 395:173–187Google Scholar
  18. Flowers TJ, Colmer TD (2010) Salinity tolerance in halophytes. New Phytol 179:945–963Google Scholar
  19. Fuchs I, Stölzle S, Ivashikina N, Hedrich R (2005) Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221:212–221PubMedGoogle Scholar
  20. Gao HJ, Yang HY, Bai JP, Liang XY, Lou Y, Zhang JL, Niu SQ, Chen YL (2015) Ultrastructural and physiological responses of potato (Solanum tuberosum L.) plantlets to gradient saline stress. Front Plant Sci.  https://doi.org/10.3389/fpls.2014.00787 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Garciadeblás B, Senn ME, Baňuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801PubMedGoogle Scholar
  22. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud J, Sentenac H (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655PubMedGoogle Scholar
  23. Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81PubMedGoogle Scholar
  24. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151PubMedPubMedCentralGoogle Scholar
  25. 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. Funct Plant Biol 39:1047–1057Google Scholar
  26. Guo Q, Meng L, Mao PC, Tian XX (2015) Salt tolerance in two tall wheatgrass species is associated with selective capacity for K+ over Na+. Acta Physiol Plant 37:1708Google Scholar
  27. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiology, biochemical, and molecular characterization. Int J Genomics 70:1596Google Scholar
  28. Hamamoto S, Horie T, Hauser F, Deinlein U, Schroeder JL, Uozumi N (2014) HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr Opin Bitech 32:113–120Google Scholar
  29. He AL, Niu SQ, Zhao Q, Li YS, Gou JY, Gao HJ, Suo SZ, Zhang JL (2018) Induced salt tolerance of perennial ryegrass by a novel bacterium strain from the rhizosphere of a desert shrub Haloxylon ammodendron. Int J Mol Sci 19:469PubMedCentralGoogle Scholar
  30. Hossain MS, ElSayed AI, Moore M, Dietz KJ (2017) Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet. J Exp Bot 68:1283–1298PubMedPubMedCentralGoogle Scholar
  31. Hu J, Ma Q, Kumar T, Duan HR, Zhang JL, Yuan HJ, Wang Q, Khan SA, Wang P, Wang SM (2016) ZxSKOR is important for salinity and drought tolerance of Zygophyllum xanthoxylum by maintaining K+ homeostasis. Plant Growth Regul 80:195–205Google Scholar
  32. Huang LT, Zhao LN, Gao LW, Véry AA, Sentenac H, Zhang YD (2018) Constitutive expression of CmSKOR, an outward K+ channel gene from melon, in Arabidopsis thaliana involved in saline tolerance. Plant Sci 274:492–502Google Scholar
  33. Kaddour R, Nasri N, M’rah S, Berthomieu P, Lachaâl M (2009) Comparative effect of potassium in K and Na uptake and transport in two accessions of Arabidopsis thaliana during salinity stress. C R Biol 332:784–794PubMedGoogle Scholar
  34. Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189:54–81PubMedGoogle Scholar
  35. Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23Google Scholar
  36. Kumari A, Das P, Parida AK, Agarwal P (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537PubMedPubMedCentralGoogle Scholar
  37. Li J, Long Y, Qi GN, Li J, Xu ZJ, Wu WH, Wang Y (2014) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant Cell 26:3387–3402PubMedPubMedCentralGoogle Scholar
  38. Li Q, Yang A, Zhang WH (2017) Comparative studies on tolerance of rice genotypes differing in their tolerance to moderate salt stress. BMC Plant Biol 17:141PubMedPubMedCentralGoogle Scholar
  39. Li W, Xu G, Alli A, Yu L (2018) Plant HAK/KUP/KT K+ transporters: function and regulation. Semin Cell Dev Biol 74:133–141PubMedGoogle Scholar
  40. Liu K, Li L, Luan S (2006) Intracellular K+ sensing of SKOR, a shaker-type K+ channel from Arabidopsis. Plant J 46:260–268PubMedGoogle Scholar
  41. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408Google Scholar
  42. Lu Y, Lei JQ, Zeng FJ, Zhang B, Liu GJ, Liu B, Li XY (2017) Effect of NaCl-induced changes in growth, photosynthetic characteristics, water status and enzymatic antioxidant system of Calligonum caput-medusae seedlings. Photosynthetica 55:96–106Google Scholar
  43. Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves the photosynthesis and water status in succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13PubMedGoogle Scholar
  44. Ma Q, Li XY, 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 Soil 374:661–676Google Scholar
  45. 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. Plant J 90:48–60PubMedGoogle Scholar
  46. Maathuis FJ, Sanders D (1994) Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proc Natl Acad Sci USA 91:9272–9276PubMedGoogle Scholar
  47. Magaña C, Núñez-Sánchez N, Fernández-Cabanás VM, García P, Serrano A, Pérez-Marín D, Pemán JM, Alcalde E (2011) Direct prediction of bioethanol yield in sugar beet pulp using near infrared spectroscopy. Bioresour Technol 102:9542–9549PubMedGoogle Scholar
  48. Mishra A, Tanna B (2017) Halophytes: Potential resources for salt stress tolerance genes and promoters. Front Plant Sci 8:829PubMedPubMedCentralGoogle Scholar
  49. Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178PubMedPubMedCentralGoogle Scholar
  50. Monteiro F, Frese L, Castro S, Duarte MC, Paulo OS, Loureiro J, Romeiras MM (2018) Genetic and genomic tools to assist sugar beet improvement: the value of the crop wild relatives. Front Plant Sci 9:74PubMedPubMedCentralGoogle Scholar
  51. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedGoogle Scholar
  52. Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2010) The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3:326–333PubMedGoogle Scholar
  53. Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2014) K+ uptake in plant roots. The systems involved, their regulation and parallels in other organisms. J Plant Physiol 171:688–695PubMedGoogle Scholar
  54. Pan YQ, Guo H, Wang SM, Zhao B, Zhang JL, Ma Q, Yin HJ, Bao AK (2016) The photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens in response to salinity. Front Plant Sci 7:848PubMedPubMedCentralGoogle Scholar
  55. Pyo YJ, Gierth M, Schroeder JI, Cho MH (2010) High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and post germination growth under low potassium conditions. Plant Physiol 153:863–875PubMedPubMedCentralGoogle Scholar
  56. Radić S, Štefanić PP, Lepeduš H, Roje V, Pevalek-Kozlina B (2013) Salt tolerance of Centaurea ragusina L. is associated with efficient osmotic adjustment and increased antioxidative capacity. Environ Exp Bot 87:39–48Google Scholar
  57. Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146PubMedGoogle Scholar
  58. Riddle NC, Jiang H, An L, Doerge RW, Birchler JA (2010) Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet 120:341–353PubMedGoogle Scholar
  59. Romero-Aranda R, Bondada BR, Syvertsen JP, Grosser JW (1997) Leaf characteristics and net gas exchange of diploid and autotetraploid citrus. Ann Bot 79:153–160Google Scholar
  60. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124PubMedGoogle Scholar
  61. Rozema J, Flowers TJ (2008) Crops for a salinized world. Science 322:1478–1480PubMedGoogle Scholar
  62. Ruiz M, Quiñones A, Martínez-Alcántara B, Aleza P, Morillon R, Navarro L, Primo-Millo E, Martínez-Cuenca MS (2016) Effects of salinity on diploid (2x) and doubled diploid (4x) citrus macrophylla genotypes. Sci Hortic 207:33–40Google Scholar
  63. Sattler MC, Carvalho CR, Clarindo WR (2016) The polyploidy and its key role in plant breeding. Planta 243:281–296PubMedGoogle Scholar
  64. Schachtman DP, Lagudah ES, Munns R (1992) The expression of salt tolerance from Triticum tauschii in hexaploid wheat. Theor Appl Genet 84:714–719PubMedGoogle Scholar
  65. Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends Plant Sci 19:687–691PubMedGoogle Scholar
  66. Shi H, Lee BH, Wu SJ, Zhu JK (2002a) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85PubMedGoogle Scholar
  67. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002b) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477PubMedPubMedCentralGoogle Scholar
  68. Skorupa M, Gołębiewski M, Domagalski K, Kurnik K, Nahia KA, Złoch M, Tretyn A, Tyburski J (2016) Transcriptomic profiling of the salt stress response in excised leaves of the halophyte Beta vulgaris ssp. maritima Plant Sci 243:56–70PubMedGoogle Scholar
  69. Spettoli P, Cacco G, Ferrari G (1976) Comparative evaluation of the enzyme multiplicity in a diploid, a triploid and a tetraploid sugar beet variety. J Sci Food Agric 27:341–344PubMedGoogle Scholar
  70. Stupar RM, Bhaskar P, Yandell B, Rensink WA, Hart AL, Ouyang S, Veilleux RE, Busse JS, Erhardt RJ, Buell CR, Jiang J (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:2055–2067PubMedPubMedCentralGoogle Scholar
  71. Sunarpi HT, 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 JL, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938PubMedGoogle Scholar
  72. Tu Y, Jiang A, Gan L, Hossain M, Zhang JM, Peng B, Xiong Y, Song Z, Cai D, Xu W, Zhang J, He Y (2014) Genome duplication improves rice root resistance to salt stress. Rice 7:15PubMedPubMedCentralGoogle Scholar
  73. Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571PubMedPubMedCentralGoogle Scholar
  74. Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32:486–496PubMedGoogle Scholar
  75. Wang QL, Yu MD, Lu C, Wu CR, Jing CR (2011) Study on breeding and photosynthetic characteristics of new polyploidy variety for leaf and fruit-producing mulberry (Morus L). Sci Agric Sin 44:562–569Google Scholar
  76. Wang Z, Wang M, Liu L, Meng F (2013a) Physiological and proteomic responses of diploid and tetraploid black locust (Robinia pseudoacacia L.) subjected to salt stress. Int J Mol Sci 14:20299–20325PubMedPubMedCentralGoogle Scholar
  77. Wang X, Chang L, Wang B, Wang D, Li P, Wang L, Yi X, Huang P, Peng M, Guo A (2013b) Comparative proteomics of Thellungiella halophila leaves from plants subjected to salinity reveals the importance of chloroplastic starch and soluble sugars in halophyte salt tolerance. Mol Cell Proteomics 12:2174–2195PubMedPubMedCentralGoogle Scholar
  78. Wang P, Guo Q, Wang Q, Zhou XR, Wang SM (2015) PtAKT1 maintains selective absorption capacity for K+ over Na+ in halophyte Puccinellia tenuiflora under salt stress. Acta Physiol Plant 37:1–10Google Scholar
  79. Wu GQ, Xi JJ, Wang Q, Ma Q, Bao AK, Zhang JL, Wang SM (2011) The ZxNHX gene encoding tonoplast Na+/H+ antiporter in the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. J Plant Physiol 168:758–767PubMedGoogle Scholar
  80. Wu GQ, Liang N, Feng RJ, Zhang JJ (2013) Evaluation of salinity tolerance in seedlings of sugar beet (Beta vulgaris L.) cultivars using proline, soluble sugars and cation accumulation criteria. Acta Physiol Plant 35:2665–2674Google Scholar
  81. Wu GQ, Feng RJ, Liang N, Yuan HJ, Sun WB (2015a) Sodium chloride stimulates growth and alleviates sorbitol-induced osmotic stress in sugar beet seedlings. Plant Growth Regul 75:307–316Google Scholar
  82. Wu GQ, Shui QZ, Wang CM, Zhang JL, Yuan HJ, Li SJ, Liu ZJ (2015b) Characteristics of Na+ uptake in sugar beet (Beta vulgaris L.) seedlings under mild salt conditions. Acta Physiol Plant 37:70Google Scholar
  83. Xu J, Tian X, Eneji AE, Li Z (2014) Functional characterization of GhAKT1, a novel Shaker-like K+ channel gene involved in K+ uptake from cotton (Gossypium hirsutum). Gene 545:61–71PubMedGoogle Scholar
  84. Xue H, Zhang F, Zhang ZH, Fu JF, Wang F, Zhang B, Ma YY (2015) Differences in salt tolerance between diploid and autotetraploid apple seedlings exposed to salt stress. Sci Hortic 190:24–30Google Scholar
  85. Xue H, Zhang B, Tian JR, Chen MM, Zhang YY, Zhang ZH, Ma YY (2017) Comparison of the morphology, growth and development of diploid and autotetraploid ‘hanfu’ apple trees. Sci Hortic 225:277–285Google Scholar
  86. Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410PubMedPubMedCentralGoogle Scholar
  87. Yan K, Wu C, Zhang L, Chen X (2015) Contrasting photosynthesis and photoinhibition in tetraploid and its autodiploid honeysuckle (Lonicera japonica thunb.) under salt stress. Front Plant Sci 6:227PubMedPubMedCentralGoogle Scholar
  88. Yang C, Zhao L, Zhang H, Yang Z, Wang H, Wen S, Zhang C, Rustgi S, von Westtstein D, Liu B (2014a) Evolution of physiological responses to salt stress in hexaploidy wheat. Pro Natl Acad Sci USA 111:11882–11887Google Scholar
  89. Yang T, Zhang S, Hu Y, Wu F, Hu Q, Chen G, Cai J, Wu T, Moran N, Yu L, Xu G (2014b) The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166:945–959PubMedPubMedCentralGoogle Scholar
  90. Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: How do plants secrete salt? Front Plant Sci 7:435Google Scholar
  91. Yue LJ, Ma Q, Li SX, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. J Arid Environ 87:153–160Google Scholar
  92. Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22PubMedGoogle Scholar
  93. Zhang JL, Flowers TJ, Wang SM (2010) Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326:45–60Google Scholar
  94. Zhang H, Han B, Wang T, Chen SX, Li HY (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67PubMedGoogle Scholar
  95. Zhang L, Ma H, Chen T, Pen J, Yu S, Zhao X (2014) Morphological and physiological responses of cotton (Gossypium hirsutum L.) plants to salinity. Plos One 9:e112807PubMedPubMedCentralGoogle Scholar
  96. Zhou Y, Lai Z, Yin X, Yu S, Xu Y, Wang X, Cong X, Luo Y, Xu H, Jiang X (2016) Hyperactive mutant of a wheat plasma membrane Na+/H+ antiporter improves the growth and salt tolerance of transgenic tobacco. Pant Sci 253:176–186Google Scholar
  97. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.School of Life Science and EngineeringLanzhou University of TechnologyLanzhouPeople’s Republic of China

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