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Overexpression of an Aeluropus littoralis Parl. potassium transporter gene, AlHAK1, in cotton enhances potassium uptake and salt tolerance

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Abstract

Potassium (K) deficiency and salinity are major environmental stresses affecting the growth and agricultural production of cotton (Gossypium hirsutum) plants worldwide. In an effort to improve potassium uptake and tolerance to salt stress through genetic engineering, we inserted AlHAK1 into cotton via Agrobacterium-mediated transformation, and then transgenic lines were obtained. To test their response to K-starvation and salt stress, we cultured seedlings from the wild type (WT) and three homozygous overexpression lines (T3 generation) in plastic pots and treated them with a modified half-strength Hoagland’s solution supplemented with different concentrations of potassium or sodium: NT (normal treatment with standard amounts of K and Na), KT (additional 0.05 mM KCl), ST (additional 150 mM NaCl), or KST (0.05 mM KCl plus 150 mM NaCl). After 15 days, all transgenic lines exhibited significantly larger values for shoot and root lengths and biomass (shoot dry weight or root dry weight) when compared with WT plants. Most root morphological parameters for the transgenics were also increased, e.g., total lengths, specific root lengths and surface areas. However, average root diameters were significantly lower than that of the WT (P < 0.05 or P < 0.01). Under salt-stress conditions, the ratios for K+/Na+ were higher in the leaves and roots of transgenic plants, and they also had less malondialdehyde and hydrogen peroxide (H2O2) than the WT tissues. Those responses paralleled greater activities by the antioxidant enzymes superoxide dismutase and peroxidase. We clearly demonstrated that cotton plants transformed with a high-affinity K+ transporter gene have enhanced K+ uptake and salt tolerance. These findings could serve as a promising step toward the development of new cotton cultivars with improved potassium uptake and tolerance to salt stress, and they have significant implications for increasing crop yields on high-salinity soils where potassium levels are low.

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References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Appel RD, Bairoch A, Hochstrasser DF (1994) A new generation of information retrieval tools for biologists: the example of the ExPASy WWW server. Trends Biochem Sci 19:258–260

    Article  CAS  PubMed  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bañuelos MA, Garcia de Blas B, Cubero B, Rodriguez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795

    Article  PubMed Central  PubMed  Google Scholar 

  • Brouder SM, Cassman KG (1994) Evaluation of a mechanistic model of potassium uptake by cotton in vermiculitic soil. Soil Sci Soc Am J 58:1174–1183

    Article  Google Scholar 

  • Cabrera E, Álvarez MC, Martín Y, Siverio JM, Ramos J (2012) K+ uptake systems in the yeast Hansenula polymorpha. Transcriptional and post-translational mechanisms involved in high-affinity K+ transporter regulation. Fungal Genet Biol 49:755–763

    Article  CAS  PubMed  Google Scholar 

  • Cassman KG, Roberts BA, Kerby TK, Bryant DC, Higashi SL (1989) Soil potassium balance and cumulative cotton response to annual potassium additions on a vermiculitic soil. Soil Sci Soc Am J 53:805–812

    Article  CAS  Google Scholar 

  • Cope JT (1981) Effects of 50 years of fertilization with phosphorus and potassium on soil test levels and yields at six locations. Soil Sci Soc of Am J 45:342–347

    Article  CAS  Google Scholar 

  • Dong HZ, Kong XQ, Li WJ, Tang W, Zhang DM (2010) Effects of plant density and nitrogen and potassium fertilization on cotton yield and uptake of major nutrients in two fields with varying fertility. Field Crops Res 119:106–113

    Article  Google Scholar 

  • Fulgenzi FR, Peralta ML, Mangano S, Danna CH, Vallejo AJ, Puigdomenech P, Santa-Maria GE (2008) The ionic environment controls the contribution of the barley HvHAK1 transporter to potassium acquisition. Plant Physiol 147:252–262

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gierth M, Mäser P (2007) Potassium transporters in plants-involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gould JH, Magallanes-Cedeno M (1998) Adaptation of cotton shoot apex culture to Agrobacterium-mediated transformation. Plant Mol Biol Rep 16:1–10

    Article  Google Scholar 

  • Grabov A (2007) Plant KT/KUP/HAK potassium transporters: single family–multiple functions. Ann Bot 99:1035–1041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hammou KA, Rubio L, Fernández JA, García-Sánchez MJ (2014) Potassium uptake in the halophyte Halimione portulacoides L. Aellen. Environ Exp Bot 107:15–24

    Article  Google Scholar 

  • Horie T, Sugawara M, Okada T, Taira K, Kaothien-Nakayama P, Katsuhara M, Shinmyo A, Nakayama H (2011) Sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J Biosci Bioengr 111:346–356

    Article  CAS  Google Scholar 

  • Horton P, Nakai K (1997) Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 5:147–152

    CAS  PubMed  Google Scholar 

  • Jiang CC, Xia Y, Chen F, Lu JW, Wang YH (2011) Plant growth, yield components, economic responses, and soil indigenous K uptake of two cotton genotypes with different K-efficiencies. Agric Sci China 10:705–713

    Article  CAS  Google Scholar 

  • Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytol 97:1–13

    Article  CAS  Google Scholar 

  • Liu JF, Zhao CY, Ma J, Zhang Y, Li MG, Yan GJ, Wang XF, Ma ZY (2011) Agrobacterium-mediated transformation of cotton (Gossypium hirsutum L.) with a fungal phytase gene improves phosphorus acquisition. Euphytica 181:31–40

    Article  CAS  Google Scholar 

  • Mansour MM (2014) The plasma membrane transport systems and adaptation to salinity. J Plant Physiol 171:1787–1800

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Atienza J, Jiang X, Garcia de Blas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nieves-Cordones M, Alemán F, Martinez 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. Plant Mol 3:326–333

    Article  CAS  Google Scholar 

  • 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 171:688–695

    Article  CAS  PubMed  Google Scholar 

  • Pettigrew WT (2003) Relationships between insufficient potassium and crop maturity in cotton. Agron J 95:1323–1329

    Article  Google Scholar 

  • Ranieri A, Petacco F, Castagna A, Soldatini GF (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Sci 159:159–167

    Article  CAS  PubMed  Google Scholar 

  • Rengel Z, Damon PM (2008) Crops and genotypes differ in efficiency of potassium uptake and use. Physiol Plant 133:624–636

    Article  CAS  PubMed  Google Scholar 

  • Rubio F, Santa-Maria GE, Rodriguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Plant Physiol 109:34–43

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-Navarro A (1997) The HAK1 gene of barley belongs to a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289

    Article  PubMed Central  PubMed  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Intl Conf Intell Syst Mol Biol 6:175–182

    CAS  Google Scholar 

  • Su H, Golldack D, Zhao CS, Bohnert HJ (2002) The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Su Q, Feng SY, An LJ, Zhang GH (2007) Cloning and functional expression in Saccharomyces cerevisiae of a K+ transporter, AlHAK1, from the graminaceous halophyte, Aeluropus littoralis. Biotechnol Lett 29:1959–1963

    Article  CAS  PubMed  Google Scholar 

  • Tian XL, Wang GW, Yang FQ, Yang PZ, Duan LS, Li ZH (2008) Differences in tolerance to low-potassium supply among different types of cultivars in cotton (Gossypium hirsutum L.). Acta Agron Sin 34:1770–1780

    Article  CAS  Google Scholar 

  • Tomoaki H, Mitsuo S, Tomoyuki O, Koichiro T, Pulla KN, Maki K, Atsuhiko S, Hideki N (2011) Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J Biosci Bioeng 111:346–356

    Article  Google Scholar 

  • Wang N, Hua HB, Egriny A, Eneji ZH, Duan LS, Tian XL (2012) Genotypic variations in photosynthetic and physiological adjustment to potassium deficiency in cotton (Gossypium hirsutum L.). J Photochem Photobiol B 110:1–8

    Article  CAS  PubMed  Google Scholar 

  • Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xia Y, Jiang CC, Chen F, Lu JW, Wang YH (2011) Differences in growth and potassium-use efficiency of two cotton genotypes. Commun Soil Sci Plant 42:132–143

    Article  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu J, Tian XL, Egriny A, Eneji ZH (2014) Functional characterization of GhAKT1, a novel Shaker-like K+ channel gene involved in K+ uptake from cotton (Gossypium hirsutum). Gene 545:61–71

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Gao Q, Sun C, Li W, Gu S, Xu C (2009) Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativa L.). J Genet Genom 36:161–172

    Article  CAS  Google Scholar 

  • Yang FQ, Wang GW, Zhang ZY, Egrinya Eneji A, Egrinya Eneji LS, Li ZH, Tian XL (2011) Genotypic variations in potassium uptake and utilization in cotton. J Plant Nutr 34:83–97

    Article  CAS  Google Scholar 

  • Yao X, Horie I, Xue S, Leung HY, Katsuhara M, Brodsky DE, Wu Y, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang ZY, Tian XL, Duan LS, Wang BM, He ZP, Li ZH (2007) Differential responses of conventional and Bt-transgenic cotton to potassium deficiency. J Plant Nutr 30:659–670

    Article  CAS  Google Scholar 

  • Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009a) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang ZY, Wang QL, Li ZH, Duan LS, Tian XL (2009b) Effects of potassium deficiency on root growth of cotton seedlings and its physiological mechanisms. Acta Agron Sin 35:718–723

    CAS  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of Hebei Province (No. C C2013201219), the Introduce Talents Start Scientific Research Projects of Hebei University (2014-277), Cutting-edge and Characteristic Disciplines of Biology (Botany) and Key subject of Biochemistry and Molecular Biology. The authors are grateful to Priscilla Licht for critical reading of this manuscript.

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Authors and Affiliations

  1. College of Life Sciences, Hebei University, Baoding, 071002, China

    J. F. Liu, S. L. Zhang, H. L. Tang & L. J. Dong

  2. North China Key Laboratory for Crop Germplasm Resources of Education Ministry, Agricultural University of Hebei, Baoding, 071002, China

    L. Z. Wu

  3. Institute of Cash Crops, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang, 050051, Hebei, China

    L. D. Liu

  4. Academy of Agriculture and Forestry Sciences of Langfang, Langfang, 065000, Hebei, China

    W. L. Che

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  1. J. F. Liu
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Correspondence to J. F. Liu.

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J. F. Liu and S. L. Zhang have contributed equally to this work.

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Liu, J.F., Zhang, S.L., Tang, H.L. et al. Overexpression of an Aeluropus littoralis Parl. potassium transporter gene, AlHAK1, in cotton enhances potassium uptake and salt tolerance. Euphytica 203, 197–209 (2015). https://doi.org/10.1007/s10681-014-1310-2

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