Skip to main content
SpringerLink
Log in

Signal transduction during aluminum-induced secretion of organic acids in plants

  • Reviews
  • Published:
Biologia Plantarum

Abstract

An excess of aluminum (Al) is a major factor limiting crop production in acidic soils. Secretion of organic acids (OAs) from the root apex of diverse plant species or genotypes via activation of anion channels has been recognized as the most important mechanism of Al exclusion. Citric, oxalic, and malic acids are the most effective OAs in detoxifying Al. In this review, we summarize biochemical properties of OAs secreted by plants. We also highlight the molecular mechanisms of Al signal perception, Al transport, signal regulators associated with OAs secretion, as well as interactions between Al and hormone signaling pathways. Based on a comprehensive understanding of the relationship between signal modulators and regulation of expression of relevant genes, a signal transduction model for Al-induced OAs secretion is proposed.

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

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

ALS:

aluminum sensitive

DAG:

diacyl glycerol

DTZ:

distal transition zone

EZ:

elongation zone

IP3:

inositol-1,4,5-triphosphate

MAPK:

mitogen-activated protein kinase

MATE:

multi-drug and toxic compound extrusion

miRNAs:

microRNAs

Nramp:

natural resistance-associated macrophage protein

Nrat:

Nramp aluminum transporter

OA:

organic acid

PA:

polyamine

PI:

phenylisothiocyanate

PIP2:

phospholipid phosphatidylinositol-4,5-bisphophate

PLC:

phospholipase C

PM:

plasma membrane

ROS:

reactive oxygen species

SA:

salicylic acid

SNP:

sodium nitroprusside

STAR:

sensitive to Al rhizotoxicity

References

  • Blancaflor, E.B., Jones, D.L., Gilroy, S.: Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. — Plant Physiol. 118: 159–172, 1998.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clarkson, D.T.: The effect of aluminium and some trivalent metal cations on cell division in the root apices of Allium cepa. — Ann. Bot. 29: 309–315, 1965.

    Google Scholar 

  • Collins, N.C., Shirley, N.J., Saeed, M., Pallotta, M., Gustafson, J.P.: An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). — Genetics 179: 669–682, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delhaize, E., Gruber, B.D., Ryan, P.R.: The roles of organic anion permeases in aluminium resistance and mineral nutrition. — FEBS Lett. 581: 2255–2262, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Delhaize, E., Ryan, P.R., Hebb, D.M., Yamamoto, Y., Sasaki, T., Matsumoto, H.: Engineering high-level aluminum tolerance in barley with the ALMT1 gene. — Proc. nat. Acad. Sci. USA 101: 15249–15254, 2004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gielen, H., Remans, T., Vangronsveld, J., Cuypuers, A.: MicroRNAs in metal stress: specific roles or secondary responses? — Int. J. mol. Sci. 13: 15826–15847, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gunse, B., Poschenrieder, C., Barcelo, J.: The role of ethylene metabolism in the short-term responses to aluminum by roots of two maize cultivars different in Al-resistance. — Environ. exp. Bot. 43: 73–81, 2000.

    Article  CAS  Google Scholar 

  • Hayes, J.E., Ma, J.F.: Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots. — J. exp. Bot. 388: 1753–1759, 2003.

    Article  Google Scholar 

  • He, H., He, L., Gu, M.: Role of microRNAs in aluminum stress in plants. — Plant Cell Rep. 33: 831–836, 2014.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hoekenga, O., Vision, T.J., Shaff, J.E., Monforte, A.J., Lee, G.P., Howell, S.H., Kochian, L.V.: Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. — Plant Physiol. 132: 936–948, 2003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoekenga, O.A., Maron, L.G., Pineros, M.A., Cancado, G.M., Shaff, J., Kobayashi, Y., Ryan, P.R., Dong, B., Sasaki, T., Matsumoto, H., Yamamoto, Y., Koyama, H., Kochian, L.V.: AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. — Proc. nat. Acad. Sci. USA 103: 9738–9743, 2006.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Horst, W.J., Schmohl, N., Kollmeier, M., Baluska, F., Sivaguru, M.: Does aluminum affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? — Plant Soil 215: 163–174, 1999.

    Article  CAS  Google Scholar 

  • Huang, C.F., Yamaji, N., Chen, Z., Ma, J.F.: A tonoplastlocalized half-size ABC transporter is required for internal detoxification of aluminum in rice. — Plant J. 69: 857–867, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Huang, C.F., Yamaji, N., Ma, J.F.: Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. — Plant Physiol. 153: 1669–1677, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang, C.F., Yamaji, N., Mitani, N., Yano, M., Nagamura, Y., Ma, J.F.: A bacterial-type ABC transporter is involved in aluminum tolerance in rice. — Plant Cell 21: 655–667, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iuchi, S., Koyama, H., Iuchi, A., Kobayashi, Y., Kitabayasgi, S., Kobayashi, Y., Ikka, T., Hirayama, T., Shinozaki, K., Kobayashi, M.: Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. — Proc. nat. Acad. Sci. USA 104: 9900–9905, 2007.

    Article  PubMed Central  PubMed  Google Scholar 

  • Jones, D.L., Kochian, L.V.: Aluminum inhibition of the inositol 1,4,5-trisphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity? — Plant Cell 7: 1913–1922, 1995.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kasai, M., Sasaki, M., Tanakamaru, S., Yamamoto, Y., Matsumoto, H.: Possible involvement of abscisic acid in increases in activities of two vacuolar H+-pumps in barley roots under aluminum stress. — Plant Cell Physiol. 34: 1335–1338, 1993.

    CAS  Google Scholar 

  • Kochian, L.V.: Cellular mechanisms of aluminum toxicity and resistance in plants. — Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 237–260, 1995.

    Article  CAS  Google Scholar 

  • Kochian, L.V., Hoekenga, O.A., Pineros, M.A.: How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. — Annu Rev Plant Biol. 55: 459–493, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Kollmeier, M., Dietrich, P., Bauer, C.S., Horst, W.J., Hedrich, R.: Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. — Plant Physiol. 126: 397–410, 2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kollmeier, M., Felle, H.H., Horst, W.J.: Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? — Plant Physiol. 122: 945–956, 2000.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kovermann, P., Meyer, S., Hörtensteiner, S., Picco, C., Scholz-Starke, J., Ravera, S., Lee, Y., Martinoia, E.: The Arabidopsis vacuolar malate channel is a member of the ALMT family. — Plant J. 52: 1169–1180, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Larsen, P.B., Geisler, M.J., Jones, C.A., Williams, K.M., Cancel, J.D.: ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. — Plant J. 41: 353–363, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Larsen, P.B., Cancel, J., Rounds, M., Ochoa, V.: Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. — Planta 225: 1447–1458, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Li, X.F., Ma, J.F., Matsumoto, H.: Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. — Plant Physiol. 123: 1537–1543, 2000.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ligaba, A., Katsuhara, M., Ryan, P.R., Shibasaka, M., Matsumoto, H.: The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. — Plant Physiol. 142: 1294–1303, 2006.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ligaba, A., Kochian, L., Pineros, M.: Phosphorylation at S384 regulates the activity of the TaALMT1 malate transporter that underlies aluminum resistance in wheat. — Plant J. 60: 411–423, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J.P., Magalhaes, J.V., Shaff, J., Kochian, L.V.: Aluminumactivated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. — Plant J. 57: 389–399, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J.P., Pineros, M.A., Kochian, L.V.: The role of aluminum sensing and signaling in plant aluminum resistance. — J. integr. Plant Biol. 56: 221–230, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Ma, J.F.: Role of organic acids in detoxification of aluminum in higher plants. — Plant Cell Physiol. 41: 383–390, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Ma, Z., Miyasaka, S.C.: Oxalate exudation by taro in response to Al. — Plant Physiol. 118: 861–865, 1998.

    Article  PubMed Central  PubMed  Google Scholar 

  • Magalhaes, J.V., Liu, J.P., Guimaraes, C., Lana, U.G.P., Alves, V.M.C., Wang, Y.H., Schaffert, R.E., Hoekenga, O.A., Pineros, M.A., Shaff, J.E., Klein, P.E., Carneiro, N.P., Coelho, C.M., Trick, H.N., Kochian, L.V.: A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. — Natur. Genet. 39: 1156–1161, 2007.

    Article  CAS  Google Scholar 

  • Maron, L.G., Pineros, M.A., Guimaraes, C.T., Magalhaes, J.V., Pleiman, J.K., Mao, C., Shaff, J., Belicuas, S.N., Kochian, L.V.: 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, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Minocha, R., Long, S.: Simultaneous separation and quantitation of amino acids and polyamines of forest tree tissues and cell cultures within a single high-performance liquid chromatography run using dansyl derivatization. — J. Chromatogr. 1035: 63–73, 2004.

    Article  CAS  Google Scholar 

  • Pan, W.L., Jackson, W.A., Hopkins, A.G.: Aluminum inhibition of shoot lateral branches of Glycine max and reversal by exogenous cytokinin. — Plant Soil 120: 1–9, 1989.

    Article  CAS  Google Scholar 

  • Pineros, M., Kochian, L.V.: A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize, dentification and characterization of Al-induced anion channels. — Plant Physiol. 125: 292–305, 2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pineros, M., Magalhaes, J.V., Carvalho Alves, V.M., Kochian, L.V.: The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation on maize. — Plant Physiol. 129: 1194–1206, 2002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Poot-Poot, W., Hernandez-Sotomayor, S.M.T.: Aluminum stress and its role in the phospholipid signaling pathway in plants and possible biotechnological applications. — IUBMB Life 63: 864–872, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ryan, P.R., Delhaize, E., Randall, P.J.: Characterisation of Alstimulated efflux of malate from the apices of Al-tolerant wheat roots. — Planta 196: 103–110, 1995.

    Article  CAS  Google Scholar 

  • Ryan, P.R., Skerrett, M., Findlay, G.P., Delhaize, E., Tyerman, S.D.: Aluminum activates an anion channel in the apical cells of wheat roots. — Proc. nat. Acad. Sci. USA 94: 6547–6552, 1997.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan, P.R., Raman, H., Gupta, S., Horst, W.J., Delhaize, E.: A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. — Plant Physiol. 149: 340–351, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan, P.R., Tyerman, S.D., Sasaki, T., Furuichi, T., Yamamoto, Y., Zhang, W.H., Delhaize, E.: The identification of aluminum-resistance genes provides opportunities for enhancing crop production on acid soils. — J. exp. Bot. 62: 9–20, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Saber, N.E., Abdel-Moneim, A.M., Barakat, S.Y.: Role of organic acids in sunflower tolerance to heavy metals. — Biol. Plant. 42: 65–73, 1999.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sawaki, Y., Iuchi, S., Kobayashi, Y., Kobayashi, Y., Ikka, T., Sakurai, N., Fujita, M., Shinozaki, K., Shibata, D., Kobayashi, M., Koyama, H.: STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. — Plant Physiol. 150: 281–294, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shen, H., He, L.F., Sasaki, T., Yamamoto, Y., Zheng, S.J., Ligaba, A., Yan, X.L., Ahn, S.J., Yamaguchi, M., Sasakawa, H., Matsumoto, H.: 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. 138: 287–296, 2005.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shen, H., Ligaba, A., Yamaguchi, M., Osawa, H., Shibata, K., Yan, X.L., Matsumoto, H.: Effect of K-252a and abscisic acid on the efflux of citrate from soybean roots. — J. exp. Bot. 55: 663–671, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Sivaguru, M., Ezaki, B., He, Z.H., Tong, H., Osawa, H., Baluska, F., Volkmann, D., Matsumoto, H.: Aluminuminduced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. — Plant Physiol. 132: 2256–2266, 2003a.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sivaguru, M., Pike, S., Gassmann, W., Bashin, T.I.: Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. — Plant Cell Physiol. 44: 667–675, 2003b.

    Article  CAS  PubMed  Google Scholar 

  • Sussman, M.R.: Molecular analysis of proteins in the plant plasma membrane. — Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 211–234, 1994.

    Article  CAS  Google Scholar 

  • Tian, Q.Y., Sun, D.H., Zhao, M.G., Zhang, W.H.: Inhibition of nitric oxide synthase (NOS) underlines aluminum-induced inhibition of root elongation in Hibiscus moscheutos. — New Phytol. 174: 322–331, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui, T., Yamaji, N., MA, J.F.: Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. — Plant Physiol. 156: 925–931, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang, Y.S., Yang, Z.M.: Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots Cassia tora L. — Plant Cell Physiol. 46: 1915–1923, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Xia, J., Yamaji, N., Kasai, T., Ma, J.F.: Plasma membranelocalized transporter for aluminum in rice. — Proc. nat. Acad. Sci. USA 107: 18381–18385, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xue, Y.J., Tao, L., Yang, Z.M.: Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. — J. Agr. Food Chem. 56: 9676–9684, 2008.

    Article  CAS  Google Scholar 

  • Yamaji, N., Huang, C.F., Nagao, S., Yano, M., Sato, Y., Nagamura, Y., Ma, J.F.: A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. — Plant Cell 21: 3339–3349, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang, J.L., You, J.F., Li, Y.Y., Wu, P., Zheng, S.J.: Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity. — Plant Cell Physiol. 48: 66–73, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J.L., Zhang, L., Li, Y.Y., You, J.F., Wu, P., Zheng, S.J.: Citrate transporters play a critical role in aluminumstimulated citrate efflux in rice bean (Vigna umbellata) roots. — Ann. Bot. 97: 579–584, 2006.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang, J.L., Zheng, S.J., He, Y.F., Matsumoto, H.: Aluminum resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly under Al stress. — J. exp. Bot. 56: 1197–1203, 2005.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yang, Z.M., Wang, J., Wang, S.H., Xu, L.L.: Salicylic acidinduced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. — Planta 217: 168–174, 2003.

    CAS  PubMed  Google Scholar 

  • Yang, Z.M., Yang, H., Wang, J., Wang, Y.S.: Aluminum regulation of citrate metabolism for Al-induced citrate efflux in the roots of Cassia tora L. — Plant Sci. 166: 1589–1594, 2004.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zhang, W.H., Ryan, P.R., Tyerman, S.D.: Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. — Plant Physiol. 125: 1459–1472, 2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao, Z., Ma, J.F., Sato, K., Takeda, K.: Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). — Planta 217: 794–800, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, S.J., Ma, J.F., Matsumoto, H.: High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. — Plant Physiol. 117: 745–751, 1998.

    Article  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cash Crops Research institute, Guangxi Academy of Agricultural Sciences, Nanning, 530007, P.R. China

    H. He

  2. College of Agronomy, Guangxi University, Nanning, 530004, P.R. China

    H. He, L. He & M. Gu

Authors
  1. H. He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. He.

Additional information

Acknowledgements: This work was supported by the National Natural Science Foundation of China (Grant Nos. 30960181 and 31260296) and the 2011 Guangxi Innovation Program for Graduates (GXU11T31076).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, H., He, L. & Gu, M. Signal transduction during aluminum-induced secretion of organic acids in plants. Biol Plant 59, 601–608 (2015). https://doi.org/10.1007/s10535-015-0537-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-015-0537-7

Additional key words

Search

Navigation