Plant and Soil

, Volume 427, Issue 1–2, pp 213–230 | Cite as

Molecular characterization of GmSTOP1 homologs in soybean under Al and proton stress

  • Ying Zhou
  • ZhenMing Yang
  • Li Gong
  • RongKun Liu
  • HaoRan Sun
  • JiangFeng You
Regular Article


Background and aims

The Sensitive to Proton Rhizotoxicity1 (STOP1) transcription factor has been implicated in the regulation of aluminium (Al) stress and proton toxicity for several plant species. This study aimed to characterize STOP1 homologs in soybean.


Five GmSTOP1 homologs were studied by transcriptional expression, subcellular localization and overexpression experiments.


Five GmSTOP1 homologs were nuclear-localized and exhibited transactivation activity. They constitutively expressed throughout the whole soybean plant. Their expressions were increased from 2 h, peaked at 4 h, returned to basal levels for the remaining duration of Al treatment but varied in aptitude and genotype. They were sensitive to pH conditions with various responses. Overexpression of GmSTOP1a in soybean hairy root increased the expression of the malate transporter gene GmALMT1, and decreased Al accumulation under Al stress. Its overexpression also regulated some pH-sensitive genes, including GmSTOP1c and GmCIPK23. Overexpression of GmSTOP1a in Arabidopsis slightly increase its Al resistance, and partially restored the root growth of the atstop1 mutant under Al stress.


GmSTOP1a contributes to both proton and Al resistance and plays a role similar to that of AtSTOP1. The functions of other four GmSTOP1 genes need further clarified.


Aluminum toxicity Soybean Cys2His2 zinc finger protein Transcriptional regulation Proton resistance 





Cauliflower mosaic virus


Sensitive to Proton Rhizotoxicity1


Aluminum resistance transcription factor 1



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

Supplementary material

11104_2018_3645_MOESM1_ESM.doc (64 kb)
ESM 1 (DOC 63 kb)


  1. Chen ZC, Yamaji N, Motoyama R, Ma JF (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633CrossRefPubMedPubMedCentralGoogle Scholar
  2. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliama. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  3. Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 aluminum tolerance mechanisms. New Phytol 208:456–468CrossRefPubMedGoogle Scholar
  5. Garcia-Oliveira AL, Benito C, Prieto P, de Andrade Menezes R, Rodrigues-Pousada C, Guedes-Pinto H, Martins-Lopes P (2013) Molecular characterization of TaSTOP1 homoelogues and their response to aluminum and proton (H+) toxicity in bread wheat (Triticum aestivum L.). BMC Plant Biol 13:134–145CrossRefPubMedPubMedCentralGoogle Scholar
  6. Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010CrossRefPubMedGoogle Scholar
  7. Horst WJ, Asher CJ, Cakmak L, Szulkiewicz P, Wissemeier AH (1992) Short-term response of soybean roots to aluminium. Plant Physiol 140:174–178CrossRefGoogle Scholar
  8. Huang S, Gao J, You JF, Liang Y, Guan K, Yan S, Zhan M, Yang Z (2018) Identification of STOP1-like proteins associated with aluminum tolerance in sweet sorghum. Front Plant Sci 9:258CrossRefPubMedPubMedCentralGoogle Scholar
  9. Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and co-regulates a key gene in aluminum tolerance. Proc Natl Acad Sci U S A 104:9900–9905CrossRefPubMedPubMedCentralGoogle Scholar
  10. Iuchi S, Kobayashi Y, Koyama H, Kobayashi M (2008) STOP1, a Cys2/His2 type zinc-finger protein, plays critical role in acid tolerance in Arabidopsis. Plant Signal Behav 3:128–132CrossRefPubMedPubMedCentralGoogle Scholar
  11. Iuchi S, Kobayashi Y, Koyama H, Kobayashi M (2009) STOP1, a Cys2/His2 type zinc-finger protein, plays critical role in acid soil tolerance in Arabidopsis. Plant Signal Behav 3(2):128–130Google Scholar
  12. Kiebowicz-Matuk A (2012) Involvement of plant C2H2-type zinc finger transcription factors in stress responses. Plant Sci 185:78–85CrossRefGoogle Scholar
  13. Kobayashi Y, Ohyama Y, Kobayashi Y, Ito H, Iuchi S, Fujita M, Zhao CR, Tanveer T, Ganesan M, Kobayashi M, Koyama H (2014) STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol Plant 7:311–322CrossRefPubMedGoogle Scholar
  14. Kochain LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  15. Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493CrossRefPubMedGoogle Scholar
  16. Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabdipsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–1458CrossRefPubMedGoogle Scholar
  17. Liang CY, Pineros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol 161:1347–1361CrossRefPubMedPubMedCentralGoogle Scholar
  18. Liu J, Magalhaes JV, Shaff J (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399CrossRefPubMedGoogle Scholar
  19. Livak KJ, and Schimittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delt][Delt] CT method. Methods 25:402–408Google Scholar
  20. Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. PNAS114:E3563Google Scholar
  21. Nian H, Yang ZM, Hang H, Yan X, Matsumoto H (2004) Citrate secretion induced by aluminum stress may not be a key mechanism responsile for differential aluminum tolerance of some genotypes. J Plant Nutr 27:2047–2066CrossRefGoogle Scholar
  22. Ohyama Y, Ito H, Kobayashi Y (2013) Characterization of AtSTOP1 orghologous genes in tobacco and other plant species. Plant Physiol 162:1937–1946CrossRefPubMedPubMedCentralGoogle Scholar
  23. Pannatier EG, Luster J, Zimmermann S et al (2005) Monitoring of water chemistry in forest soils: an Indicator for acidification. Chimia(Aarau) 59:989Google Scholar
  24. Sawaki Y, Iuchi S, Kobayasi Y (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281–294CrossRefPubMedPubMedCentralGoogle Scholar
  25. Sawaki Y, Kobayashi Y, Kihara-Doi T (2014) Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci 223:8–15CrossRefPubMedGoogle Scholar
  26. Subramanian S, Graham MY, Yu O et al (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 137:1345–1353CrossRefPubMedPubMedCentralGoogle Scholar
  27. Sun L, Liang C, Chen Z, Liu P, Tian J, Liu G, Liao H (2014) Superior aluminium (Al) tolerance of Stylosanthes, is achieved mainly by malate synthesis through an Al-enhanced malic enzyme, SgME1. New Phytol 202:209–219CrossRefPubMedGoogle Scholar
  28. Tang QY and Zhang CX (2012) Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Science 20(2):254–260Google Scholar
  29. Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomoto M, Tada Y, Yamamoto YY, Koyama H (2015) Senstive to proton rhizotoxicity1, calmodulin binding transcription activator2, and other transcription factors are involved in aluminum-activated malate transporter1 expression. Plant Physiol 167:991–1003CrossRefPubMedPubMedCentralGoogle Scholar
  30. Xia JX, Yamaji N, Ma JF (2013) A plasma membrane-localized small peptide is involved in rice aluminum tolerance. Plant J 76:345–355PubMedGoogle Scholar
  31. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349CrossRefPubMedPubMedCentralGoogle Scholar
  32. Yamaji N, Fujii MD, Yokosho K et al (2015) Possibility of trade-off between acidic and alkaline soil adaptation in graminaceous plants. Proceedings of the 9th international symposium on plant-soil interactions at low pH Dubrovnik, Croatia, October 18-23:77–78Google Scholar
  33. Yang ZM, Sivaguru M, Horst WJ, Matsumoto H (2000) Aluminium tolerance is achieved by exudation of citric acid from roots of soybean ( Glycine max ). Physiol Plant 110:72–77CrossRefGoogle Scholar
  34. Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumotob H (2001) Characterization of aluminium-induced citrate secretion in aluminium-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71CrossRefGoogle Scholar
  35. You JF, Zhang H, Liu N, Gao L, Kong L, Yang Z (2011) Transcriptomic responses to aluminum stress in soybean roots. Genome 54:923–933CrossRefPubMedGoogle Scholar
  36. Zhou Y, Yang Z, Xu Y, Sun H, Sun Z, Lin B, Sun W, You J (2018) Soybean NADP-malic enzyme functions in malate and citrate metabolism and contributes to their efflux under Al stress. Front Plant Sci 8:2246. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ying Zhou
    • 1
  • ZhenMing Yang
    • 1
  • Li Gong
    • 1
  • RongKun Liu
    • 1
  • HaoRan Sun
    • 1
  • JiangFeng You
    • 1
  1. 1.Laboratory of Soil and Plant Molecular Genetics, College of Plant ScienceJilin UniversityChangchunChina

Personalised recommendations