Skip to main content
SpringerLink
Log in

Functional characterization of three MATE genes in relation to aluminum-induced citrate efflux from soybean root

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

Abstract

Background and aims

Citrate transporters responsible for Aluminum (Al)-induced citrate efflux have not been identified in soybean.

Method

Three soybean multi-drug and toxic compound extrusion (MATE) family genes were characterized by transcriptional expression, subcellular localization and overexpression experiments.

Results

GmMATE75, GmMATE79 and GmMATE87 are localized to plasma membrane. Their over-expression respectively resulted in more citrate efflux and less Al contents in soybean hairy roots, alleviated root elongation inhibition in Arabidopsis and partially restored root growth in atmate mutant under Al stress. Al increased their transcriptional expression at either the root apex or the base zone. Cu2+, Cd2+, La3+ increased the expression of GmMATE79 and GmMATE87. Ten day of –Fe culture increased the expression of GmMATE75 and GmMATE79. Al treatment extended β-glucuronidase (GUS) staining from central cylinder to cortical and epidermis cells for pGmMATE75::GUS or pGmMATE79::GUS soybean hairy roots transformation. But GUS staining restricted within central cylinder for pGmMATE87::GUS transformation with or without Al treatment.

Conclusion

GmMATE75, GmMATE79 and GmMATE87 are plasma-membrane-localized citrate transporters and have capabilities to increase citrate efflux. They played different role in Al-induced citrate secretion from soybean because their different tissue localization and expression patterns.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

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

Similar content being viewed by others

Abbreviations

Al:

Aluminum

CaMV:

Cauliflower mosaic virus

GFP:

Green Fluorescent protein

MATE:

Multidrug and toxic compound extrusion

References

  • Abdelhaleem H, Carter TE, Rufty TW, Boerma HR, Li Z (2014) Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol Breeding 33:851–862

    CAS  Google Scholar 

  • Bianci-Hall CM, Carter TE, Rufty TW, Arellano C, Boerma HR, Ashley DA (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci 38:513–522

    Google Scholar 

  • Bianci-Hall CM, Carter TE, Bailey MA, Mian MAR, Rufty TW, Ashley DA (2000) Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci 40:538–544

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum-Aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiol 103:695–702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan W, Lou HQ, Gong YL, Liu MY, Cao MJ, Liu Y, Yang JL, Zheng SJ (2015) Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and Al tolerance mechanisms. New Phytol 208:456–468

    CAS  PubMed  Google Scholar 

  • Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF (2012) Acquisition of aluminum tolerance by modification of a single gene in barley. Nat Commun 3:713

    PubMed  Google Scholar 

  • Fujii M, Yokosho K, Yamaji N, Yamane M, Saisho D, Sato K, Ma JF (2018) Retrotransposon insertion and DNA methylation regulate aluminum tolerance in European barley accessions. Plant Physiol 178(2):716–727

    Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) an aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    CAS  PubMed  Google Scholar 

  • Horst WJ, Asher CJ, Cakmak L, Szulkiewicz P, Wissemeier AH (1992) Short-term response of soybean roots to aluminum. Plant Physiol 140:174–178

    CAS  Google Scholar 

  • Kochian LV, Pineros MA, Liu JP, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598

    CAS  PubMed  Google Scholar 

  • Lei GJ, Yokosho K, Yamaji N, Ma JF (2017) Two MATE transporters with different subcellular localization are involved in Al tolerance in buckwheat. Plant Cell Physiol 58(12):2179–2189

    CAS  PubMed  Google Scholar 

  • Li GZ, Wang ZQ, Yokosho K, Ding B, Fan W, Gong QQ, Li GX, Wu YR, Yang JL, Ma JF, Zheng SJ (2018) Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol 219:149–162

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Liu MY, Chen WW, Xu JM, Fan W, Yang JL, Zheng SJ (2013) The role of VuMATE1 expression in aluminum-inducible citrate secretion in rice bean (Vigna umbellata) roots. J Exp Bot 64:1795–1804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Li Y, Wang W, Gai JY, 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

    PubMed  PubMed Central  Google Scholar 

  • Liu MY, Lou HQ, Chen WW, Pineros MA, Xu JM, Fan W, Kochian LV, Zheng SJ, Yang JL (2018) Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant Cell Environ 41(4):809–822

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161

    CAS  PubMed  Google Scholar 

  • Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, Shaff J, Belicuas SN, Kochian 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

    CAS  PubMed  Google Scholar 

  • Maron LG, Guimarães CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Pro Natl Acad Sci 110:5241–5246

    CAS  Google Scholar 

  • Nian H, Yang ZM, Hang H, Yan X, Matsumoto H (2004) Citrate secretion induced by aluminum stress may not be a key mechanism responsible for differential aluminum tolerance of some genotypes. J Plant Nutri 27:2047–2066

    CAS  Google Scholar 

  • Qi B, Koriir P, Zhao T, Yu DY, Chen SY, Gai JY (2008) Mapping quantitative toxin tolerance in NJRIKY recombinant inbred line population of soybean (Glycine max). J Intergr Plant Biol 50:1085–1095

    Google Scholar 

  • Rogers EE, Wu XL, Stacey G, Nguyen HT (2009) Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 166:1453–1459

    CAS  PubMed  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    CAS  PubMed  Google Scholar 

  • Sawaki T, Kihara-Doi T, Kobayashi Y, Nishikubo N, Kawazu T, Koyama H, Sato S (2013) Characterization of Al-responsive citrate excretion and citrate-transporting MATEs in Eucalyptus camaldulensis. Planta 237:979–989

    CAS  PubMed  Google Scholar 

  • Sharma AD, Sharma H, Lightfoot DA (2010) The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population. Theor Appl Genet 122:687–694

    Google Scholar 

  • Silva IR, Smyth TJ, Raper CD, Carter TE, Rufty TW (2001) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol Plant 112:200–210

    CAS  PubMed  Google Scholar 

  • Subramanian S, Graham MY, Yu O, Graham TL (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiol 137:1345–1353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun LL, Liang CY, Chen ZJ, Liu PD, Tian J, Liu GD, Liao H (2014) Superior aluminum (Al) tolerance of Stylosanthes is achieved mainly by malate synthesis through an Al-enhanced malic enzyme. SgME1 New phyt 202:209–219

    CAS  Google Scholar 

  • Takanashi K, Yokosho K, Saeki K, Sugiyama A, Sato S, Tabata S (2013) LjMATE1: a citrate transporter responsible for iron supply to the nodule infection zone of lotus japonicus. Plant &Cell Physiol 54:585–594

    CAS  Google Scholar 

  • Takanashi K, Shitan N, Yazaki K (2014) The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotech 31:417–430

    CAS  Google Scholar 

  • Tang QY, Zhang CX (2012) Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20(2):254–260 (in China)

    PubMed  Google Scholar 

  • Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM, Ramesh S, Tyerman SD, Delhaize E (2013) Transposon mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161:880–892

    CAS  PubMed  Google Scholar 

  • Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, Xing 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

    CAS  PubMed  Google Scholar 

  • Xu MY, You JF, Hou NN, Zhang HM, Chen GA, Yang ZM (2010) Mitochondrial enzymes and citrate transporter contribute to the aluminum-induced citrate secretion from soybean (Glycine max) roots. Funct Plant Biol 37:886–892

    Google Scholar 

  • Yang ZM, Sivaguru M, Horst WJ, Matsumoto H (2000) Aluminum tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max). Physiol Plant 110:72–77

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Yang XY, Yang JL, Zhou Y, Pineros MA, Kochian LV, Li GX, Zheng SJ (2011) A De nove synthesist citrate transporter, multidrug and toxic compound extrusion, implicates in Al-activated citrate efflux in rice bean (Vigna umbellata) root apex. Plant Cell Environ 34:2138–2148

    CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37:296–303

    CAS  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2011) An Al-induced MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069

    CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2016a) OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. J Exp Bot 67:5485–5494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF (2016b) Retrotransposon-mediated aluminum tolerance through enhanced expression of the citrate transporter OsFRDL4. Plant Physiol 172:2327–2336

    CAS  PubMed  PubMed Central  Google Scholar 

  • You JF, Zhang HM, Liu N, Gao LL, Kong LN, Yang ZM (2011) Transcriptomic responses to aluminium stress in soybean roots. Genome 54:923–933

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang J, Guo JL, Zhou FL, Singh S, Xu X, Xie Q, Yang ZB, Huang CF (2018) F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Aarbidopsis. PNAS 116:319–327. https://doi.org/10.1073/pnas.1814426116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou GF, Pereira JF, Delhaize E, Zhou M, Jurandir V, Magalhaes JV, Peter PR (2014) Enhancing the aluminum tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J Exp Bot 65:2381–2390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Yang ZM, Sun HR, Sun ZT, Lin B, Sun WJ, You JF (2018a) Soybean NADP-malic enzyme functions in malate and citrate metabolism and contributes to their efflux under Al stress. Frontiers Plant Sci 8:2246

    Google Scholar 

  • Zhou Y, Yang ZM, Gong L, Liu RK, Sun HR, You JF (2018b) Molecular characterization of GmSTOP1 homologs in soybean under Al and proton stress. Plant Soil 427(1–2):213–270

    CAS  Google Scholar 

Download references

Acknowledgements

Financial support for this research was provided by the National Natural Science Foundation of China (No. 31372124) and Jilin Natural Science Foundation of China (20130101084JC).

Author information

Author notes

  1. Ying Zhou and Zhengbiao Wang contributed equally to this work.

Authors and Affiliations

  1. Jilin Province Engineering Laboratory of Plant Genetic Improvement, College of Plant Science, Jilin University, 5333 Xi An Road, Changchun, 130062, China

    Ying Zhou, Zhengbiao Wang, Li Gong, Anle Chen, Ning Liu, Sha Li, Haoran Sun, Zhenming Yang & Jiangfeng You

Authors
  1. Ying Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhengbiao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anle Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ning Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sha Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Haoran Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhenming Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jiangfeng You
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhenming Yang or Jiangfeng You.

Additional information

Responsible Editor: Jian Feng Ma.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 8058 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Y., Wang, Z., Gong, L. et al. Functional characterization of three MATE genes in relation to aluminum-induced citrate efflux from soybean root. Plant Soil 443, 121–138 (2019). https://doi.org/10.1007/s11104-019-04192-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04192-w

Keywords

Search

Navigation