Abstract
The potassium (K+) transporter/high-affinity K+/K+ uptake transporters (KT/HAK/KUP), which contribute to K+ uptake, transport and allocation, take an indispensible part in ion homeostasis, as well as in plant adaptation to disadvantageous environmental stresses. However, molecular mechanisms in terms of K+ nutrition in fruit crops are still largely unknown. In this work, we isolated 15 KT/HAK/KUP transporter genes in strawberry (designated as FveKUP1 to FveKUP15), and checked their expression under both normal and K+ deficient conditions. Quantitative real-time PCR analyses indicated that most FveKUPs were largely expressed in flowers, with a responsive expression to K+ deficiency. Among these FveKUPs, FveKUP8 was the most abundantly expressed gene in all tested tissues, and its expression was significantly reduced by K+ deficiency. Further functional complementation experiment in bacterial mutant indicated that FveKUP8 can utilize external K+ under neutral proton environment, and might be a dominant K+ transporter during the flowering of strawberry plants. Our findings suggest that FveKUP8 is involved in K+ homeostasis in strawberry, and could be used as a potential gene for the molecular breeding of high K+ efficiency plants.
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Abbreviations
- K+ :
-
Potassium
- g s :
-
Stomatal conductance
- PEG:
-
Polyethylene glycol
- P N :
-
Net photosynthetic rate
- qRT-PCR:
-
Quantitative real-time polymerase chain reaction
- Tr:
-
Transpiration rate
- Zn:
-
Zinc
References
Ahmad P, Abdel Latef AA, Abd_Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513. https://doi.org/10.3389/fpls.2016.00513
Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373
Baňuelos MA, Garciadeblas B, Cubero B, Rodríguez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–794
Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach. Q Rev Biol 161(2):140–141
Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65(5):1241–1257
Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: Functional genomics in an ecologically dominant plant species. Trends Plant Sci 9(1):49–56
Chen G, Liu C, Gao Z, Zhang Y, Jiang H, Zhu L, Ren D, Yu L, Xu G, Qian Q (2017) OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci 8:1885
Cherel I, Lefoulon C, Boeglin M, Sentenac H (2014) Molecular mechanisms involved in plant adaptation to low K(+) availability. J Exp Bot 65(3):833–848
Choudhary M, Jetley UK, Abash Khan M, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotox Environ Safe 66:204–209
Davies C, Shin R, Liu W, Thomas MR (2006) Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation. J Exp Bot 57:3209–3216
Demiral MA, Köseoglu AT (2005) Effect of potassium on yield, fruit quality, and chemical composition of greenhouse-grown aalia melon. J Plant Nutr 28:93–100
Deng WK, Wang YB, Liu ZX, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS ONE 9:e111988
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971
Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49(5):684–692
Epstein W, Buurman ET, McLaggan D, Naprstek J (1993) Multiple mechanisms, roles and controls of K+ transport in Escherichia coli. Biochem Soc Trans 21:1006–1010
Fu HH, Luan S (1998) AtKuP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–73
Gierth M, Maser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K(+) deprivation-induced high-affinity K(+) uptake and AKT1 K(+) channel contribution to K(+) uptake kinetics in Arabidopsis roots. Plant Physiol 137(3):1105–1114
Grabov A (2007) Plant KT/KUP/HAK potassium transporters: single family—multiple functions. Ann Bot 99:1035–1041
Gupta M, Qiu X, Wang L, **e W, Zhang CJ, **ong LZ, Lian XM, Zhang QF (2008) KT/HAK/KUP potassium transporters gene family and their whole-life cycle expression profile in rice (Oryza sativa). Mol Genet Genomics 280:437–452
Han M, Wu W, Wu WH, Yi W (2016) Potassium transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions. Mol Plant 9:437–446
Hartz TK, Johnstone PR, Francis DM, Miyao EM (2005) Processing tomato yield and fruit quality improved with potassium fertigation. HortScience 40:1862–1867
He C, Cui K, Duan A, Zeng Y, Zhang J (2012) Genome-wide and molecular evolution analysis of the poplar KT/HAK/KUP potassium transporter gene family. Ecol Evol 2(8):1996–2004
Hyun TK, Rim Y, Kim E, Kim JS (2014) Genome-wide and molecular evolution analyses of the KT/HAK/KUP family in tomato (Solanum lycopersicum L.). Genes Genom 36(3):365–374
Jung S, Staton M, Lee T, Blenda A, Svancara R, Abbott A, Main D (2008) GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acids Res 36:D1034–D1040
Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z (2013) Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25:1960–1978
Lebaudy A, Véry AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366
Lester GE, Jifon JL, Makus DJ (2010) Impact of potassium nutrition on postharvest fruit quality: Melon (Cucumis melo L.) case study. Plant Soil 335:117–131
Li J, Wang Z, Pang Z, Fang Q, Li C (2007) Effects of spraying KH2PO4 on the content of chlorophyll in leaf and leaf weight and fruit quality of peach cultivars. J Fruit Sci 24(4):533–536 (in Chinese)
Li M, Li Y, Li H, Wu G (2011) Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree Physiol 31:349–357
Mangano S, Silberstein S, Santa-Maria GE (2008) Point mutations in the barley HvHAK1 potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress. FEBS lett 582:3922–3928
Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2011) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ, Véry AA (2011) Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nava G, Dechen AR, Nachtigall RG (2007) Nitrogen and potassium fertilization affect apple fruit quality in Southern Brazil. Commun Soil Sci Plant 39:96–107
Petersen TN, Brunak S, Von HG, Nielsen H (2010) SIGNALP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786
Qiao X, Li M, Li LT, Yin H, Wu JY, Zhang SL (2015) Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear (Pyrus bretschneideri) and five other Rosaceae species. BMC Plant Biol 15:12
Ramarkers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P (2001) Trh1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13:139–151
Rubio F, Santa-Maria GE, Rodriguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109:34–43
Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman TL, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW Jr, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Lopez Girona E, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116
Song ZZ, Su YH (2013) Distinctive potassium-accumulation capability of alligatorweed (Alternanther philoxeroides) links to high-affinity potassium transport facilitated by K+-uptake systems. Weed Sci 61:77–84
Song ZZ, Yang SY, Zhu H, ** M, Su YH (2014) Heterologous expression of an alligatorweed high-affinity potassium transporter gene enhances salinity tolerance in Arabidopsis. Am J Bot 101:840–850
Song ZZ, Yang SY, Zuo J, Su YH (2014) Over-expression of ApKUP3 enhances potassium nutritional status and drought tolerance in transgenic rice. Biol Plant 58(4):649–658
Song ZZ, Duan CL, Guo SL, Yang Y, Feng YF, Ma RJ, Yu ML (2015) Potassium contributes to zinc stress tolerance in peach (Prunus persica) seedlings by enhancing photosynthesis and the antioxidant defense system. Genet Mol Res 14(3):8338–8351
Song ZZ, Ma RJ, Yu ML (2015) Genome-wide analysis and identification of KT/HAK/KUP potassium transporter gene family in peach (Prunus persica). Genet Mol Res 14(1):774–787
Song ZZ, Guo SL, Zhang CH, Zhang BB, Ma RJ, Korir NK, Yu ML (2015) KT/HAK/KUP potassium transporter genes differentially expressed during fruit development, ripening, and postharvest shelf-life of ‘**ahui6’ peaches. Acta Physiol Plant 37:131
Song ZZ, Yang Y, Ma RJ, Xu JL, Yu ML (2015) Transcription of potassium transporter genes of KTHAKKUP family in peach seedlings and responses to abiotic stresses. Biol Plant 59(1):65–73
Song ZZ, Ma RJ, Zhang BB, Xu JL, Yu ML (2016) Expression of KT/HAK/KUP family genes during leaf development of peach and their responses to potassium fertilizer application. J Fruit Sci 33(6):257–267 (in Chinese)
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis uing maximum likelihood, evolutionary distance, 540 and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
Upadhyay A, Upadhyay AK, Bhirangi RA (2012) Expression of Na+/H+ antiporter gene in response to water and salinity stress in grapevine rootstocks. Biol Plant 56:762–766
Vallejo AJ, Peralta ML, Santa-Maria GE (2005) Expression of potassium-transporter coding genes, and kinetics of rubidium uptake, along a longitudinal root axis. Plant Cell Environ 28:850–862
Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603
Wang Y, Wu WH (2015) Genetic approaches for improvement of the crop potassium acquisition and utilization efficiency. Curr Opin Plant Biol 25:46–52
Wu J, Wang ZW, Shi ZB, Zhang S, Ming R, Zhu SL, Khan MA, Tao ST, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi KJ, Huang XS, Wang YT, Zhao X, Wu JY, Deng C, Gou CY, Zhou WL, Yin H, Qin GH, Sha YH, Tao Y, Chen H, Yang YA, Song Y, Zhan DL, Wang J, Li LT, Dai MS, Gu C, Wang YZ, Shi DH, Wang XW, Zhang HP, Zeng L, Zheng DM, Wang CL, Chen MS, Wang GB, **e L, Sovero V, Sha SF, Huang WJ, Zhang SJ, Zhang MY, Sun JM, Xu LL, Li Y, Liu X, Li QS, Shen JH, Wang JY, Paull RE, Bennetzen JL, Wang J, Zhang SL (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23(2):396–408
Yamasaki A, Yano T (2009) Effect of supplemental application of fertilizers on flower bud initiation and development of strawberry—possible role of nitrogen. Acta Hortic 842:765–768
Yang T, Zhang S, Hu Y, Wu F, Hu Q, Chen G, Cai J, Wu T, Moran N, Yu L, Xu G (2014) 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(2):945–959
Yurtseven E, Kesmez GD, Ünlükara A (2005) The effects of water salinity and potassium levels on yield, fruit quality and water consumption of a native central anatolian tomato species (Lycopersicon esculantum). Agric Water Manag 78:128–135
Zhang Z, Zhang J, Chen Y, Li R, Wang H, Wei J (2012) Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.). Mol Biol Rep 39:8465–8473
Zhao D, Oosterhuis DM, Bednarz CW (2001) Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosynthetica 39:103–109
Acknowledgements
This work was jointly supported by the following grants: the National Key R&D Program of China (2019YFD1000500), National Natural Science Foundations of China (31700524 and 31801837), the Science Foundations of of Shandong Province (ZR2016CB48), the Modern Agricultural Industry Technology System Innovation Team of Shandong Province of China (SDAIT-02-05), and Special Education Fund of Shandong Province (10000326).
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Supplementary file1 Supplemental Fig. 1 Basic information of conserved motifs identified in FveKUP proteins. The MEME (v4.12.0) online programwas used, as described by Bailey et al. (2006), to display the conserved motifs shared by FveKUP proteins (TIF 159 KB)
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Gao, Y., Yu, C., Zhang, K. et al. Identification and characterization of the strawberry KT/HAK/KUP transporter gene family in response to K+ deficiency. Acta Physiol Plant 43, 1 (2021). https://doi.org/10.1007/s11738-020-03172-3
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DOI: https://doi.org/10.1007/s11738-020-03172-3