SpringerLink
Log in

Nitric oxide mediates aluminum-induced citrate secretion through regulating the metabolism and transport of citrate in soybean roots

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Citrate secretion is a kind of typical strategy for plant against aluminum (Al) toxicity. However, the signaling process in Al-activated citrate secretion needs to be clarified.

Methods

Physiological and biochemical methods as well as gene expression analysis were employed to examine the regulatory roles of nitric oxide (NO) in Al-activated citrate secretion in soybean roots.

Results

Application of NO donor alleviated root growth inhibition and decreased Al content in Al-treated root apices. Al-induced NO production and citrate secretion were further elevated by NO donor, but inhibited by NO scavenger. Inhibition of citrate synthase (CS) or plasma membrane (PM) H+-ATPase activity significantly decreased Al-induced secretion of citrate, but inhibition of aconitase (ACO) activity enhanced citrate secretion under Al stress. Furthermore, NO mediated Al-stimulated CS and PM H+-ATPase activities, but decreased ACO activity under Al stress. Further investigation showed that NO modulated Al-activated transcriptional expression of CS and PM H+-ATPase as well as GmMATE. Overexpression of GmMATE in soybean hairy roots caused an enhanced Al-induced citrate efflux and Al resistance.

Conclusions

Our findings suggest that NO-dependent up-regulation of citrate synthesis and activation of PM H+-ATPase-coupled MATE transporter co-transport system participates in Al-activated citrate exudation, thus conferring plant resistance to Al toxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

ACO:

Aconitase

CS:

Citrate synthase

FC:

Fusicoccin

FCA:

Fluorocitric acid

HPLC:

High-performance liquid chromatography

PM:

Plasma membrane

MATE:

Multidrug and toxic compound extrusion

NO:

Nitric oxide

NOS:

Nitric oxide synthase

NR:

Nitrate reductase;

PTIO:

2-phenyl-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide

SNP:

Sodium nitroprusside

Sur:

Suramin

VA:

Vanadate

References

  • Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol 126:1381–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola over-expressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daspute AA, Kobayashi Y, Panda SK, Fakrudin B, Kobayashi Y, Tokizawa M, Iuchi S, Choudhary AK, Yamamoto YY, Koyama H (2018) Characterization of CcSTOP1; a C2H2-type transcription factor regulates Al tolerance gene in pigeonpea. Planta 247:201–214

    Article  CAS  PubMed  Google Scholar 

  • de la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568

    Article  PubMed  Google Scholar 

  • Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng W, Luo KM, Li ZG, Yang YW, Hu N, Wu Y (2009) Overexpression of Citrus junos mitochondrial citrate synthase gene in Nicotiana benthamiana confers aluminium tolerance. Planta 230:355–365

    Article  CAS  PubMed  Google Scholar 

  • Guo C, Chen Q, Zhao X, Chen X, Zhao Y, Wang L, Li K, Yu Y, Chen L (2013) Al-enhanced expression and interaction of 14-3-3 protein and plasma membrane H+-ATPase is related to Al-induced citrate secretion in an Al-resistant black soybean. Plant Mol Biol Report 31:1012–1024

    Article  CAS  Google Scholar 

  • Hayes JE, Ma JF (2003) Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots. J Exp Bot 54:1753–1759

    Article  CAS  PubMed  Google Scholar 

  • He H, Zhan J, He L, Gu M (2012) Nitric oxide signaling in aluminum stress in plants. Protoplasma 249:483–492

    Article  CAS  PubMed  Google Scholar 

  • He H, Huang W, Oo TL, Gu M, Zhan J, Wang A, He LF (2018) Nitric oxide suppresses aluminum-induced programmed cell death in peanut (Arachis hypoganea L.) root tips by improving mitochondrial physiological properties. Nitric Oxide 74:47–55. https://doi.org/10.1016/j.niox.2018.01.003

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Gao J, You J, Liang Y, Guan K, Yan S, Zhan M, Yang Z (2018) Identification of STOP1-like proteins associated with aluminum tolerance in sweet sorghum (Sorghum bicolor L.). Front Plant Sci 9:258

    Article  PubMed  PubMed Central  Google Scholar 

  • Kereszt A, Li D, Indrasumunar A, Nguyen CD, Nontachaiyapoom S, Kinkema M, Gresshoff PM (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc 2:948–952

    Article  CAS  PubMed  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang SQ, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci U S A 97:8849–8855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399

    Article  CAS  PubMed  Google Scholar 

  • Liu N, You J, Shi W, Liu W, Yang Z (2012) Salicylic acid involved in the process of aluminum induced citrate exudation in Glycine max L. Plant Soil 352:85–97

    Article  CAS  Google Scholar 

  • Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168:343–U607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Li Y, Wang W, Gai J, Li Y (2016) Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genomics 17:223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 41:383–390

    Article  CAS  PubMed  Google Scholar 

  • Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit Rev Plant Sci 24:267–281

    Article  CAS  Google Scholar 

  • Ma JF (2007) Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol 264:225–252

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997a) Detoxifying aluminium with buckwheat. Nature 390:569–570

    Article  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H (1997b) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38:1019–1025

    Article  CAS  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  CAS  PubMed  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang YH, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1116

    Article  CAS  PubMed  Google Scholar 

  • Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, Shaff J, Belicuas SN, Kochain LV (2010) Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61:728–740

    Article  CAS  PubMed  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35

    Article  CAS  PubMed  Google Scholar 

  • Peters RA (1961) Further experiments on the inhibition of aconitase by enzymically prepared fluorocitric acid. Biochem J 79:261–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pineros MA, Magalhaes JV, Alves VMC, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129:1194–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portillo F (2000) Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim Biophys Acta 1469:31–42

    Article  CAS  PubMed  Google Scholar 

  • Qiu QS, Su XF (1998) The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots. Aust J Plant Physiol 25:923–928

    CAS  Google Scholar 

  • Rangel AF, Rao IM, Braun HP, Horst WJ (2010) Aluminum resistance in common bean (Phaseolus vulgaris) involves induction and maintenance of citrate exudation from root apices. Physiol Plant 138:176–190

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: investigation of the spatial sensitivity and the role of the root cap in Al tolerance. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110

    Article  CAS  Google Scholar 

  • Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38

    Article  CAS  PubMed  Google Scholar 

  • Sasaki M, Yamamoto Y, Ma JF, Matsumoto H (1997) Early events induced by aluminum stress in elongating cells of wheat root. Soil Sci Plant Nutr 43:1009–1014

    Article  CAS  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 238:287–296

    Article  CAS  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 138:2475–2482

    Article  Google Scholar 

  • Sun C, Lu L, Liu L, Liu W, Yu Y, Liu X, Hu Y, ** C, Lin X (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250

    Article  CAS  PubMed  Google Scholar 

  • Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465–475

    Article  CAS  PubMed  Google Scholar 

  • Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM, Ramesh S, Tyerman SD, Delhaize E (2013) Transposon-mediated alteration of TaMATElB expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161:880–892

    Article  CAS  PubMed  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang HH, Liang XL, Wan Q, Wang XM, Bi YR (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307

    Article  CAS  PubMed  Google Scholar 

  • Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179:281–288

    Article  CAS  Google Scholar 

  • Wang HH, Huang JJ, Liang WH, Liang XL, Bi YR (2013) Involvement of putrescine and nitric oxide in aluminum tolerance by modulating citrate secretion from roots of red kidney bean. Plant Soil 366:479–490

    Article  CAS  Google Scholar 

  • Wang P, Yu W, Zhang J, Rengel Z, Xu J, Han Q, Chen L, Li K, Yu Y, Chen Q (2016) Auxin enhances aluminium-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H+-ATPase in soybean roots. Ann Bot 1178:933–940

    Article  CAS  Google Scholar 

  • Wang HH, Li Y, Hou JJ, Huang JJ, Liang WH (2017) Nitrate reductase-mediated nitric oxide production alleviates Al-induced inhibition of root elongation by regulating the ascorbate-glutathione cycle in soybean roots. Plant Soil 410:453–465

    Article  CAS  Google Scholar 

  • Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, **ng Y, Qi Y, Zhang N, Guo YD (2014) Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant Cell Physiol 55:1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Xu MY, You JF, Hou NN, Zhang HM, Chen G, Yang ZM (2010) Mitochondrial enzymes and citrate transporter contribute to the aluminium-induced citrate secretion from soybean (Glycine max) roots. Funct Plant Biol 37:478–482

    Article  CAS  Google Scholar 

  • Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumoto H (2001) Characterization of aluminium-induced citrate secretion in aluminium-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71

    Article  CAS  Google Scholar 

  • Yang JL, Zheng SJ, He YF, Matsumoto H (2005) Aluminum resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot 56:1197–1203

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Zhang L, Li YY, You JF, Wu P, Zheng SJ (2006) Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. Ann Bot 97:579–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JL, You JF, Li YY, Wu P, Zheng SJ (2007) Magnesium enhances aluminum-induced citrate secretion in rice bean roots by restoring plasma membrane H+-ATPase activity. Plant Cell Physiol 48:66–73

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Ji J, Wang H, Harris-Shultz KR, Abd Allah EF, Luo Y, Guan Y, Hu X (2016) Carbon monoxide interacts with auxin and nitric oxide to cope with iron deficiency in Arabidopsis. Front Plant Sci 7:112

    PubMed  PubMed Central  Google Scholar 

  • Zeng H, Feng X, Wang B, Zhu Y, Shen Q, Xu G (2013) Citrate exudation induced by aluminum is independent of plasma membrane H+-ATPase activity and coupled with potassium efflux from cluster roots of phosphorus-deficient white lupin. Plant Soil 366:389–400

    Article  CAS  Google Scholar 

  • Zhang J, Wei J, Li D, Kong X, Rengel Z, Chen L, Yang Y, Cui X, Chen Q (2017) The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. Front Plant Sci 8:1757

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Xu XY, Chen LQ, Yang JL, Zheng SJ (2012) Nitric oxide exacerbates Al-induced inhibition of root elongation in rice bean by affecting cell wall and plasma membrane properties. Phytochemistry 76:46–51

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (U1704121, 31301252, U1704101) and Science Foundation of the Henan Normal University for Outstanding Young Scholars (No. 14YQ003).

Author information

Authors and Affiliations

  1. College of Life Sciences, Henan Normal University, **nxiang, 453007, Henan, China

    Huahua Wang, Yangyang Zhang, Junjie Hou, Wenwen Liu, Junjun Huang & Weihong Liang

Authors
  1. Huahua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yangyang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junjie Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenwen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junjun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weihong Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Huahua Wang or Weihong Liang.

Additional information

Responsible Editor: Jian Feng Ma.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Zhang, Y., Hou, J. et al. Nitric oxide mediates aluminum-induced citrate secretion through regulating the metabolism and transport of citrate in soybean roots. Plant Soil 435, 127–142 (2019). https://doi.org/10.1007/s11104-018-3879-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3879-z

Keywords

Search

Navigation