Activation of potassium released from soil by root-secreted organic acids in different varieties of tobacco (Nicotiana tabacum)
Zhi-Xiao Yang A B , Shi-Zhou Yu B , Ying-Chao Lin B , Wei-Jun Zhang C , Yi Wang B , Ren-Gang Wang B , Shi-Xiao Xu A , Tie-Zhao Yang A and Gang Xue A DA College of Tobacco Science, Henan Agricultural University, Zhengzhou, 45002, PR China.
B Guizhou Academy of Tobacco Science, Guiyang, 550081, PR China.
C Fenggang Tobacco Filiale of Guizhou Province Tobacco Company, Fenggang 564200, China.
D Corresponding author. Email: linyingxian2006@163.com
Functional Plant Biology 47(4) 318-326 https://doi.org/10.1071/FP19137
Submitted: 21 May 2019 Accepted: 19 November 2019 Published: 14 February 2020
Abstract
Organic acids secreted from the roots of plants play important roles in nutrient acquisition and metal detoxification; however, the precise underlying mechanisms of these processes remain poorly understood. In the present study we examined the content of organic acids exuded from roots and the effects of these organic acids on the activation of slowly available potassium (K) at different K levels, including normal K supply and K-deficient conditions. In addition, the study system also comprised a high-K tobacco variety (ND202) and two common ones (K326 and NC89). Our results showed that high-K varieties exhibited significantly higher contents of organic acids in its root exudates and available K in both rhizosphere and non-rhizosphere soils than the other varieties. This research also suggested that a cyclic process in which soil was acidified after being complexed by organic acids was involved in the release of slowly available K, and that this process primarily depended on the soil pH at high organic acids concentrations, but the complexation of organic ligands became dominant at low concentrations. In conclusion, tobacco roots secrete organic acids to increase available K content and improve the utilisation rate of soil K. High-K varieties probably enhance slowly available K activation by secreting relatively high amounts of organic acids, thus leading to more available K in soil for absorption by plants.
Additional keywords: acidification, available K, complexation, rhizosphere, utilization.
References
Ae N, Arihara J, Okada K, Yoshiham T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in cropping system of the India subcontinent. Science 248, 477–480.| Phosphorus uptake by pigeon pea and its role in cropping system of the India subcontinent.Crossref | GoogleScholarGoogle Scholar | 17815599PubMed |
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell & Environment 32, 666–681.
| Regulation and function of root exudates.Crossref | GoogleScholarGoogle Scholar |
Bao SD (2000) ‘Soil agricultural chemistry analysis.’ (China Agriculture Press: Beijing)
Bowsher AW, Ali R, Harding SA, Tsai CJ, Donovan LA (2015) Analysis of wild sunflower (Helianthus annuus L.) root exudates using gas chromatography-mass spectrometry. Journal of Plant Nutrition and Soil Science 178, 776–786.
| Analysis of wild sunflower (Helianthus annuus L.) root exudates using gas chromatography-mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M, Borriss R, Von-Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition and Soil Science 174, 3–11.
| Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency.Crossref | GoogleScholarGoogle Scholar |
Chen LH, Yang XM, Raza W, Li JH, Liu YX, Qiu MH, Zhang FG, Shen QR (2011) Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Applied Microbiology and Biotechnology 89, 1653–1663.
| Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers.Crossref | GoogleScholarGoogle Scholar |
Chiang PN, Wang MK, Chiu CY, Chou SY (2006) Effects of cadmium amendments on low-molecular weight organic acid exudates in rhizosphere soils of tobacco and sunflower. Environmental Toxicology 21, 479–488.
| Effects of cadmium amendments on low-molecular weight organic acid exudates in rhizosphere soils of tobacco and sunflower.Crossref | GoogleScholarGoogle Scholar | 16944509PubMed |
Chou CH (2010) Role of allelopathy in sustainable agriculture: use of allelochemicals as naturally occurring bio-agrochemicals. Allelopathy Journal 25, 3–16.
Cong RH, Li XK, Lu JW, Ma YP, Liao ZW, Jiang CC (2009) Effect of low-molecular-water organic acids on transformation of potassium in red soil and yellow cinnamon soil in south china. Turang Xuebao 46, 532–536.
Cui JY, Ren L, Wang JG, Zhang FS (2002) Effect of organic acids on mobilization of K from K-bearing minerals and stochastic simulation of dynamic K release. Turang Xuebao 39, 341–350.
Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. Journal of Plant Physiology 171, 696–707.
| Mechanisms and physiological roles of K+ efflux from root cells.Crossref | GoogleScholarGoogle Scholar | 24685330PubMed |
Ding JH, Wang XX, Zhang TL, Li QM, Luo MB (2006) Optimization of RP-HPLC analysis of low molecular weight organic acids in soil. Journal of Liquid Chromatography & Related Technologies 29, 99–111.
| Optimization of RP-HPLC analysis of low molecular weight organic acids in soil.Crossref | GoogleScholarGoogle Scholar |
Gandner WK, Barber DA, Parberry DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil 70, 107–124.
Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2007) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17, 505–512.
| Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars.Crossref | GoogleScholarGoogle Scholar |
Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biology & Biochemistry 77, 69–80.
| Root exudates mediated interactions belowground.Crossref | GoogleScholarGoogle Scholar |
Hamamoto S, Uozumi N (2014) Organelle-localized potassium transport systems in plants. Journal of Plant Physiology 171, 743–747.
| Organelle-localized potassium transport systems in plants.Crossref | GoogleScholarGoogle Scholar | 24810770PubMed |
Hao WY, Ren LX, Ran W, Shen QR (2010) Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum. Plant and Soil 336, 485–497.
| Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum.Crossref | GoogleScholarGoogle Scholar |
He YC, Ma CL, Xu JH, Li Z (2011) A high-throughput screening strategy for nitrile-hydrolyzing enzymes based on ferric hydroxamate spectrophotometry. Applied Microbiology and Biotechnology 89, 817–823.
| A high-throughput screening strategy for nitrile-hydrolyzing enzymes based on ferric hydroxamate spectrophotometry.Crossref | GoogleScholarGoogle Scholar | 21038095PubMed |
Hoffland E, Fmdenegg GR, Nelmans JA (1989) Solubilization of rock phosphate by rape. I. Evaluation of the role of the nutrient uptake pattern. Plant and Soil 113, 155–160.
| Solubilization of rock phosphate by rape. I. Evaluation of the role of the nutrient uptake pattern.Crossref | GoogleScholarGoogle Scholar |
Huang XF, Chaparro JM, Reardon KF, Zhang RF, Shen QR, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92, 267–275.
| Rhizosphere interactions: root exudates, microbes, and microbial communities.Crossref | GoogleScholarGoogle Scholar |
Jia YB (2008) Study on the physiological mechanism of rice (Oryza sativa L.) with high K efficiency. PhD thesis, College of Environmental and Resource Science, Zhejiang University, Zhejiang, China.
Jiang L, Yang RZ, Lu YF, Cao SQ, Ci LK, Zhang JJ (2012) β-Aminobutyric acid-mediated tobacco tolerance to potassium deficiency. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 59, 781–787.
| β-Aminobutyric acid-mediated tobacco tolerance to potassium deficiency.Crossref | GoogleScholarGoogle Scholar |
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant and Soil 205, 25–44.
| Organic acids in the rhizosphere – a critical review.Crossref | GoogleScholarGoogle Scholar |
Kumar A, Bahadur I, Maurya BR, Raghuwanshi R, Meena VS, Singh DK, Dixit J (2015) Does a plant growth promoting rhizobacteria enhance agricultural sustainability? Journal of Pure & Applied Microbiology 9, 715–724.
Li JY, Niu LA, Zhang QC, Di HJ, Hao JM (2017a) Impacts of long-term lack of potassium fertilization on different forms of soil potassium and crop yields on the north China plains. Journal of Soils and Sediments 17, 1607–1617.
| Impacts of long-term lack of potassium fertilization on different forms of soil potassium and crop yields on the north China plains.Crossref | GoogleScholarGoogle Scholar |
Li SL, Xu C, Wang J, Guo B, Yang L, Chen JN, Ding W (2017b) Cinnamic, myristic and fumaric acids in tobacco root exudates induce the infection of plants by Ralstonia solanacearum. Plant and Soil 412, 381–395.
| Cinnamic, myristic and fumaric acids in tobacco root exudates induce the infection of plants by Ralstonia solanacearum.Crossref | GoogleScholarGoogle Scholar |
Liang CY, Piñeros MA, Tian J, Yao ZF, Sun LL, Liu JP, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMTl to improve soybean adaptation to acid soils. Plant Physiology 161, 1347–1361.
| Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMTl to improve soybean adaptation to acid soils.Crossref | GoogleScholarGoogle Scholar |
Ling N, Huang QW, Guo SW, Shen QR (2011) Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f.sp. niveum. Plant and Soil 341, 485–493.
| Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f.sp. niveum.Crossref | GoogleScholarGoogle Scholar |
Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiology 85, 315–317.
| Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings.Crossref | GoogleScholarGoogle Scholar | 16665693PubMed |
Marschner H (2012) ‘Marschner’s mineral nutrition of higher plants.’ 3rd edn. (Academic Press: Cambridge, UK)
Melo VDF, Corrêa GF, Ribeiro AN, Maschio PA (2005) Kinetics of potassium and magnesium release from clay minerals of soils in the Triângulo Mineiro region, Minas Gerais state, Brazil. Revista Brasileira de Ciência do Solo 29, 533–545.
| Kinetics of potassium and magnesium release from clay minerals of soils in the Triângulo Mineiro region, Minas Gerais state, Brazil.Crossref | GoogleScholarGoogle Scholar |
Mohan A, Girdhar M, Rehman H, Kumar A, Saggu S, Ansari AA (2015) Metal accumulation capability of weeds and their utilization in phytoremediation technology. In ‘Phytoremediation: management of environmental contaminants Vol. 2’. (Eds AA Ansari,·SS Gill, R Gill, G R Lanza, L Newman) pp. 343–357. (Springer: Cham, Switzerland)
Rengel Z, Damon PM (2008) Crops and genotypes differ in efficiency of potassium uptake and use. Physiologia Plantarum 133, 624–636.
| Crops and genotypes differ in efficiency of potassium uptake and use.Crossref | GoogleScholarGoogle Scholar | 18397208PubMed |
Shen H, Yan XL, Zhao M, Zheng SL, Wang XR (2002) Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates. Environmental and Experimental Botany 48, 1–9.
| Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates.Crossref | GoogleScholarGoogle Scholar |
Shi SJ, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM (2011) Effects of selected root exudate components on soil bacterial communities. FEMS Microbiology Ecology 77, 600–610.
| Effects of selected root exudate components on soil bacterial communities.Crossref | GoogleScholarGoogle Scholar |
Sison MLQ, Magbanua JPV, Bugante EC, Torres FG, Nayve FRP, Migo VP, Fernandez WL (2010) Agro-recycling of distillery effluent as liquid organic fertilizer for sugarcane. Philippine Journal of Crop Science 35, 1–8.
Song SK, Huang PM (1988) Dynamics of potassium release from potassium-bearing minerals as influenced by oxalic and citric acids. Soil Science Society of America Journal 52, 383–390.
| Dynamics of potassium release from potassium-bearing minerals as influenced by oxalic and citric acids.Crossref | GoogleScholarGoogle Scholar |
Trejo-Téllez LI, Stenzel R, Gomez-Merino FC, Schmitt JM (2010) Transgenic tobacco plants overexpressing pyruvate phosphate dikinase increase exudation of organic acids and decrease accumulation of aluminum in the roots. Plant and Soil 326, 187–198.
| Transgenic tobacco plants overexpressing pyruvate phosphate dikinase increase exudation of organic acids and decrease accumulation of aluminum in the roots.Crossref | GoogleScholarGoogle Scholar |
Wang Y, Wu WH (2015) Genetic approaches for improvement of the crop potassium acquisition and utilization efficiency. Current Opinion in Plant Biology 25, 46–52.
| Genetic approaches for improvement of the crop potassium acquisition and utilization efficiency.Crossref | GoogleScholarGoogle Scholar | 25941764PubMed |
Wang BX, Yang SH, Chen GH, Wu Y, Hou Y, Xu GW (2008) Simultaneous determination of non-volatile, semi-volatile, and volatile organic acids in tobacco by SIM-Scan mode GC-MS. Journal of Separation Science 31, 721–726.
| Simultaneous determination of non-volatile, semi-volatile, and volatile organic acids in tobacco by SIM-Scan mode GC-MS.Crossref | GoogleScholarGoogle Scholar |
Williams CH, Twine JR (1960) Flame photometric method for sodium, potassium and calcium. In ‘Modern methods of plant analysis’. (Eds K Peach, MV Tacey) pp. 3–5. (Springer-Verlag: Berlin)
Wu HS, Raza W, Liu DY, Wu CL, Mao ZS, Xu YC, Shen QR (2008) Allelopathic impact of artificially applied coumarin on Fusarium oxysporum f.sp. niveum. World Journal of Microbiology & Biotechnology 24, 1297–1304.
| Allelopathic impact of artificially applied coumarin on Fusarium oxysporum f.sp. niveum.Crossref | GoogleScholarGoogle Scholar | [In Chinese]
Wu YH, Xue LX, Xu ZC, Shao HF, Jin L, Huang WX, Liu CK (2013) Combined effects of root cutting, auxin application, and potassium fertilizer on growth, sugar: nicotine ratio, and organic potassium index of flue-cured tobacco. Acta Ecologica Sinica 33, 5686–5695.
| Combined effects of root cutting, auxin application, and potassium fertilizer on growth, sugar: nicotine ratio, and organic potassium index of flue-cured tobacco.Crossref | GoogleScholarGoogle Scholar |
Wu HM, Wu LK, Zhu Q, Wang JY, Qin XJ, Xu JH, Kong LF, Chen J, Lin S, Khan MU, Amjad H, Lin WX (2017) The role of organic acids on microbial deterioration in the Radix pseudostellariae rhizosphere under continuous monoculture regimes. Scientific Reports 7, 3497
| The role of organic acids on microbial deterioration in the Radix pseudostellariae rhizosphere under continuous monoculture regimes.Crossref | GoogleScholarGoogle Scholar |
Xi CF (1998) ‘China soil.’ (China Agriculture Press: Beijing)
Xue G, Lu LM, Yang TZ, Li XH, Xing XX, Xu SX (2016) Enhanced tolerance to low-K+ stress in tobacco plants, that ectopically express the CBL-interacting protein kinase CIPK23 gene. Czech Journal of Genetics and Plant Breeding 52, 77–82.
| Enhanced tolerance to low-K+ stress in tobacco plants, that ectopically express the CBL-interacting protein kinase CIPK23 gene.Crossref | GoogleScholarGoogle Scholar |
Yang TZ, Lu LM, Xia W, Fan JH (2007) Characteristics of potassium-enriched, flue-cured tobacco genotype in potassium absorption, accumulation, and in-ward potassium currents of root cortex. Agricultural Sciences in China 6, 1479–1486.
| Characteristics of potassium-enriched, flue-cured tobacco genotype in potassium absorption, accumulation, and in-ward potassium currents of root cortex.Crossref | GoogleScholarGoogle Scholar |
Yang YF, Yang ZX, Yu SZ, Chen HL (2019) Organic acids exuded from roots increase the available potassium content in the rhizosphere soil: a rhizobag experiment in Nicotiana tabacum. HortScience 1, 23–27.
| Organic acids exuded from roots increase the available potassium content in the rhizosphere soil: a rhizobag experiment in Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar |
Zeng FR, Chen S, Miao Y, Wu FB, Zhang GP (2008) Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environmental Pollution 155, 284–289.
| Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress.Crossref | GoogleScholarGoogle Scholar |
Zhang FG, Zhu Z, Yang XM, Ran W, Shen QR (2013) Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere. Applied Soil Ecology 72, 41–48.
| Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere.Crossref | GoogleScholarGoogle Scholar |
Zhou S, He Q, Wang XF, Ning M, Yang Y, Xu YB (2017) An insight into the roles of exogenous potassium salts on the thermal degradation of flue-cured tobacco. Journal of Analytical and Applied Pyrolysis 123, 385–394.
| An insight into the roles of exogenous potassium salts on the thermal degradation of flue-cured tobacco.Crossref | GoogleScholarGoogle Scholar |
Zörb C, Senbayram M, Peiter E (2014) Potassium in agriculture–status and perspectives. Journal of Plant Physiology 171, 656–669.
| Potassium in agriculture–status and perspectives.Crossref | GoogleScholarGoogle Scholar | 24140002PubMed |